Biofilm

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Staphylococcus aureus biofilm on an indwelling catheter Staphylococcus aureus biofilm 01.jpg
Staphylococcus aureus biofilm on an indwelling catheter
Probable cyanobacteria in the vertical section of a silicified biofilm from the Lower Cretaceous. Very shallow hypersaline environment of the Urgonian carbonate platform of Provence, south eastern France. Algae in silicified sediment with evaporite crystals. Urgonian carbonate platform of Provence. 1.jpg
Probable cyanobacteria in the vertical section of a silicified biofilm from the Lower Cretaceous. Very shallow hypersaline environment of the Urgonian carbonate platform of Provence, south eastern France.
IUPAC definition

Aggregate of microorganisms in which cells that are frequently embedded within a self-produced matrix of extracellular polymeric substances (EPSs) adhere to each other and/or to a surface.

Contents

  • A biofilm is a system that can be adapted internally to environmental conditions by its inhabitants.
  • The self-produced matrix of extracellular polymeric substances, which is also referred to as slime, is a polymeric conglomeration generally composed of extracellular biopolymers in various structural forms. [1]

A biofilm is a syntrophic community of microorganisms in which cells stick to each other and often also to a surface. [2] [3] These adherent cells become embedded within a slimy extracellular matrix that is composed of extracellular polymeric substances (EPSs). [2] [3] The cells within the biofilm produce the EPS components, which are typically a polymeric combination of extracellular polysaccharides, proteins, lipids and DNA. [2] [3] [4] Because they have a three-dimensional structure and represent a community lifestyle for microorganisms, they have been metaphorically described as "cities for microbes". [5] [6]

Biofilms may form on living (biotic) or non-living (abiotic) surfaces and can be common in natural, industrial, and hospital settings. [3] [7] They may constitute a microbiome or be a portion of it. The microbial cells growing in a biofilm are physiologically distinct from planktonic cells of the same organism, which, by contrast, are single cells that may float or swim in a liquid medium. [8] Biofilms can form on the teeth of most animals as dental plaque, where they may cause tooth decay and gum disease.

Microbes form a biofilm in response to a number of different factors, [9] which may include cellular recognition of specific or non-specific attachment sites on a surface, nutritional cues, or in some cases, by exposure of planktonic cells to sub-inhibitory concentrations of antibiotics. [10] [11] A cell that switches to the biofilm mode of growth undergoes a phenotypic shift in behavior in which large suites of genes are differentially regulated. [12]

A biofilm may also be considered a hydrogel, which is a complex polymer that contains many times its dry weight in water. Biofilms are not just bacterial slime layers but biological systems; the bacteria organize themselves into a coordinated functional community. Biofilms can attach to a surface such as a tooth or rock, and may include a single species or a diverse group of microorganisms. Subpopulations of cells within the biofilm differentiate to perform various activities for motility, matrix production, and sporulation, supporting the overall success of the biofilm. [13] The biofilm bacteria can share nutrients and are sheltered from harmful factors in the environment, such as desiccation, antibiotics, and a host body's immune system. A biofilm usually begins to form when a free-swimming, planktonic bacterium attaches to a surface. [14] [ page needed ]

Origin and formation

Origin of biofilms

Biofilms are thought to have arisen during primitive Earth as a defense mechanism for prokaryotes, as the conditions at that time were too harsh for their survival. They can be found very early in Earth's fossil records (about 3.25 billion years ago) as both Archaea and Bacteria, and commonly protect prokaryotic cells by providing them with homeostasis, encouraging the development of complex interactions between the cells in the biofilm. [3]

Formation of biofilms

The formation of a biofilm begins with the attachment of free-floating microorganisms to a surface. [8] [5] The first colonist bacteria of a biofilm may adhere to the surface initially by the weak van der Waals forces and hydrophobic effects. [15] [16] If the colonists are not immediately separated from the surface, they can anchor themselves more permanently using cell adhesion structures such as pili. A unique group of Archaea that inhabit anoxic groundwater have similar structures called hami. Each hamus is a long tube with three hook attachments that are used to attach to each other or to a surface, enabling a community to develop. [17] [18] Hyperthermophilic archaeon Pyrobaculum calidifontis produce bundling pili which are homologous to the bacterial TasA filaments, a major component of the extracellular matrix in bacterial biofilms, which contribute to biofilm stability. [19] TasA homologs are encoded by many other archaea, suggesting mechanistic similarities and evolutionary connection between bacterial and archaeal biofilms. [19]

Biofilm of golden hydrophobic bacteria; ceiling of Golden Dome Cave, a lava tube in Lava Beds National Monument A114, Lava Beds National Monument, California, USA, Golden Dome Lava Tube Cave, 2004.jpg
Biofilm of golden hydrophobic bacteria; ceiling of Golden Dome Cave, a lava tube in Lava Beds National Monument

Hydrophobicity can also affect the ability of bacteria to form biofilms. Bacteria with increased hydrophobicity have reduced repulsion between the substratum and the bacterium. [21] Some bacteria species are not able to attach to a surface on their own successfully due to their limited motility but are instead able to anchor themselves to the matrix or directly to other, earlier bacteria colonists. Non-motile bacteria cannot recognize surfaces or aggregate together as easily as motile bacteria. [21]

During surface colonization bacteria cells are able to communicate using quorum sensing (QS) products such as N-acyl homoserine lactone (AHL). Once colonization has begun, the biofilm grows by a combination of cell division and recruitment. Polysaccharide matrices typically enclose bacterial biofilms. The matrix exopolysaccharides can trap QS autoinducers within the biofilm to prevent predator detection and ensure bacterial survival. [22] In addition to the polysaccharides, these matrices may also contain material from the surrounding environment, including but not limited to minerals, soil particles, and blood components, such as erythrocytes and fibrin. [21] The final stage of biofilm formation is known as development, and is the stage in which the biofilm is established and may only change in shape and size.[ citation needed ]

The development of a biofilm may allow for an aggregate cell colony (or colonies) to be increasingly tolerant [23] or resistant to antibiotics. Cell-cell communication or quorum sensing has been shown to be involved in the formation of biofilm in several bacterial species. [24]

Development

Mature biofilm structure Biofilm is characterised by heterogenous environment and the presence of a variety of subpopulations. A biofilm structure is composed of metabolically active (both resistant and tolerant) and non-active cells (viable but not culturable cells and persisters) as well as polymer matrix consisting of polysaccharide, extracellular DNA and proteins. Biofilm growth is associated with an escalated level of mutations and horizontal gene transfer which is promoted in due to the packed and dense structure. Bacteria in biofilms communicate by quorum sensing, which activates genes participating in virulence factors production. Mature biofilm structure.png
Mature biofilm structure 
Biofilm is characterised by heterogenous environment and the presence of a variety of subpopulations. A biofilm structure is composed of metabolically active (both resistant and tolerant) and non-active cells (viable but not culturable cells and persisters) as well as polymer matrix consisting of polysaccharide, extracellular DNA and proteins. Biofilm growth is associated with an escalated level of mutations and horizontal gene transfer which is promoted in due to the packed and dense structure. Bacteria in biofilms communicate by quorum sensing, which activates genes participating in virulence factors production.

Biofilms are the product of a microbial developmental process. [27] The process is summarized by five major stages of biofilm development, as shown in the diagram below: [28]

Five stages of biofilm development (1) Initial attachment, (2) Irreversible attachment, (3) Maturation I, (4) Maturation II, and (5) Dispersion. Each stage of development in the diagram is paired with a photomicrograph of a developing P. aeruginosa biofilm. All photomicrographs are shown to the same scale. Biofilm.jpg
Five stages of biofilm development 
(1) Initial attachment, (2) Irreversible attachment, (3) Maturation I, (4) Maturation II, and (5) Dispersion. Each stage of development in the diagram is paired with a photomicrograph of a developing P. aeruginosa biofilm. All photomicrographs are shown to the same scale.

Dispersal

Dispersal of cells from the biofilm colony is an essential stage of the biofilm life cycle. Dispersal enables biofilms to spread and colonize new surfaces. Enzymes that degrade the biofilm extracellular matrix, such as dispersin B and deoxyribonuclease, may contribute to biofilm dispersal. [29] [30] Enzymes that degrade the biofilm matrix may be useful as anti-biofilm agents. [31] [32] Evidence has shown that a fatty acid messenger, cis-2-decenoic acid, is capable of inducing dispersion and inhibiting growth of biofilm colonies. Secreted by Pseudomonas aeruginosa , this compound induces cyclo heteromorphic cells in several species of bacteria and the yeast Candida albicans . [33] Nitric oxide has also been shown to trigger the dispersal of biofilms of several bacteria species [34] [35] at sub-toxic concentrations. Nitric oxide has potential as a treatment for patients that have chronic infections caused by biofilms. [36]

It was generally assumed that cells dispersed from biofilms immediately go into the planktonic growth phase. However, studies have shown that the physiology of dispersed cells from Pseudomonas aeruginosa biofilms is highly different from that of planktonic and biofilm cells. [37] [38] Hence, the dispersal process is a unique stage during the transition from biofilm to planktonic lifestyle in bacteria. Dispersed cells are found to be highly virulent against macrophages and Caenorhabditis elegans, but highly sensitive towards iron stress, as compared with planktonic cells. [37]

Furthermore, Pseudomonas aeruginosa biofilms undergo distinct spatiotemporal dynamics during biofilm dispersal or disassembly, with contrasting consequences in recolonization and disease dissemination. [39] Biofilm dispersal induced bacteria to activate dispersal genes to actively depart from biofilms as single cells at consistent velocities but could not recolonize fresh surfaces. In contrast, biofilm disassembly by degradation of a biofilm exopolysaccharide released immotile aggregates at high initial velocities, enabling the bacteria to recolonize fresh surfaces and cause infections in the hosts efficiently. Hence, biofilm dispersal is more complex than previously thought, where bacterial populations adopting distinct behavior after biofilm departure may be the key to survival of bacterial species and dissemination of diseases.

Biofilm dispersal Honors Option-MMG.svg
Biofilm dispersal 

Properties

Biofilms are usually found on solid substrates submerged in or exposed to an aqueous solution, although they can form as floating mats on liquid surfaces and also on the surface of leaves, particularly in high humidity climates. Given sufficient resources for growth, a biofilm will quickly grow to be macroscopic (visible to the naked eye). Biofilms can contain many different types of microorganism, e.g. bacteria, archaea, protozoa, fungi and algae; each group performs specialized metabolic functions. However, some organisms will form single-species films under certain conditions. The social structure (cooperation/competition) within a biofilm depends highly on the different species present. [40]

Extracellular matrix

Scanning electron micrograph of mixed-culture biofilm, demonstrating in detail a spatially heterogeneous arrangement of bacterial cells and extracellular polymeric substances. Mixed-culture biofilm.jpg
Scanning electron micrograph of mixed-culture biofilm, demonstrating in detail a spatially heterogeneous arrangement of bacterial cells and extracellular polymeric substances.

The EPS matrix consists of exopolysaccharides, proteins and nucleic acids. [41] [42] [43] A large proportion of the EPS is more or less strongly hydrated, however, hydrophobic EPS also occur; one example is cellulose [44] which is produced by a range of microorganisms. This matrix encases the cells within it and facilitates communication among them through biochemical signals as well as gene exchange. The EPS matrix also traps extracellular enzymes and keeps them in close proximity to the cells. Thus, the matrix represents an external digestion system and allows for stable synergistic microconsortia of different species. [45] Some biofilms have been found to contain water channels that help distribute nutrients and signalling molecules. [46] This matrix is strong enough that under certain conditions, biofilms can become fossilized (stromatolites).

Bacteria living in a biofilm usually have significantly different properties from free-floating bacteria of the same species, as the dense and protected environment of the film allows them to cooperate and interact in various ways. [47] One benefit of this environment is increased resistance to detergents and antibiotics, as the dense extracellular matrix and the outer layer of cells protect the interior of the community. [48] [49] In some cases antibiotic resistance can be increased up to 5,000 times. [50] Lateral gene transfer is often facilitated within bacterial and archaeal biofilms [51] and can leads to a more stable biofilm structure. [52] Extracellular DNA is a major structural component of many different microbial biofilms. [53] Enzymatic degradation of extracellular DNA can weaken the biofilm structure and release microbial cells from the surface.

However, biofilms are not always less susceptible to antibiotics. For instance, the biofilm form of Pseudomonas aeruginosa has no greater resistance to antimicrobials than do stationary-phase planktonic cells, although when the biofilm is compared to logarithmic-phase planktonic cells, the biofilm does have greater resistance to antimicrobials. This resistance to antibiotics in both stationary-phase cells and biofilms may be due to the presence of persister cells. [54]

Habitats

Mats of bacterial biofilm color the hot springs in Yellowstone National Park. The longest raised mat area is about half a meter long. Bacteria mats near Grand Prismatic Spring in Yellowstone.JPG
Mats of bacterial biofilm color the hot springs in Yellowstone National Park. The longest raised mat area is about half a meter long.
Thermophilic bacteria in the outflow of Mickey Hot Springs, Oregon, approximately 20 mm thick. Thermophilic bacteria.jpg
Thermophilic bacteria in the outflow of Mickey Hot Springs, Oregon, approximately 20 mm thick.

Biofilms are ubiquitous in organic life. Nearly every species of microorganism have mechanisms by which they can adhere to surfaces and to each other. Biofilms will form on virtually every non-shedding surface in non-sterile aqueous or humid environments. Biofilms can grow in the most extreme environments: from, for example, the extremely hot, briny waters of hot springs ranging from very acidic to very alkaline, to frozen glaciers.

Biofilms can be found on rocks and pebbles at the bottoms of most streams or rivers and often form on the surfaces of stagnant pools of water. Biofilms are important components of food chains in rivers and streams and are grazed by the aquatic invertebrates upon which many fish feed. Biofilms are found on the surface of and inside plants. They can either contribute to crop disease or, as in the case of nitrogen-fixing rhizobia on root nodules, exist symbiotically with the plant. [55] Examples of crop diseases related to biofilms include citrus canker, Pierce's disease of grapes, and bacterial spot of plants such as peppers and tomatoes. [56]

Percolating filters

Percolating filters in sewage treatment works are highly effective removers of pollutants from settled sewage liquor. They work by trickling the liquid over a bed of hard material which is designed to have a very large surface area. A complex biofilm develops on the surface of the medium which absorbs, adsorbs and metabolises the pollutants. The biofilm grows rapidly and when it becomes too thick to retain its grip on the media it washes off and is replaced by newly grown film. The washed off ("sloughed" off) film is settled out of the liquid stream to leave a highly purified effluent. [57]

Slow sand filter

Slow sand filters are used in water purification for treating raw water to produce a potable product. They work through the formation of a biofilm called the hypogeal layer or Schmutzdecke in the top few millimetres of the fine sand layer. The Schmutzdecke is formed in the first 10–20 days of operation [58] and consists of bacteria, fungi, protozoa, rotifera and a range of aquatic insect larvae. As an epigeal biofilm ages, more algae tend to develop and larger aquatic organisms may be present including some bryozoa, snails and annelid worms. The surface biofilm is the layer that provides the effective purification in potable water treatment, the underlying sand providing the support medium for this biological treatment layer. As water passes through the hypogeal layer, particles of foreign matter are trapped in the mucilaginous matrix and soluble organic material is adsorbed. The contaminants are metabolised by the bacteria, fungi and protozoa. The water produced from an exemplary slow sand filter is of excellent quality with 90–99% bacterial cell count reduction. [59]

Rhizosphere

Plant-beneficial microbes can be categorized as plant growth-promoting rhizobacteria. [60] These plant growth-promoters colonize the roots of plants, and provide a wide range of beneficial functions for their host including nitrogen fixation, pathogen suppression, anti-fungal properties, and the breakdown of organic materials. [61] One of these functions is the defense against pathogenic, soil-borne bacteria and fungi by way of induced systemic resistance (ISR) [62] or induced systemic responses triggered by pathogenic microbes (pathogen-induced systemic acquired resistance). [63] Plant exudates act as chemical signals for host specific bacteria to colonize. [64] Rhizobacteria colonization steps include attractions, recognition, adherence, colonization, and growth. [61] Bacteria that have been shown to be beneficial and form biofilms include Bacillus, Pseudomonas, and Azospirillum . [65] [66] Biofilms in the rhizosphere often result in pathogen or plant induced systemic resistances. Molecular properties on the surface of the bacterium cause an immune response in the plant host. [64] These microbe associated molecules interact with receptors on the surface of plant cells, and activate a biochemical response that is thought to include several different genes at a number of loci. [64] Several other signaling molecules have been linked to both induced systemic responses and pathogen-induced systemic responses, such as jasmonic acid and ethylene. [61] Cell envelope components such as bacterial flagella and lipopolysaccharides, which are recognized by plant cells as components of pathogens. [67] Certain iron metabolites produced by Pseudomonas have also been shown to create an induced systemic response. [64] This function of the biofilm helps plants build stronger resistance to pathogens.

Plants that have been colonized by PGPR forming a biofilm have gained systemic resistances and are primed for defense against pathogens. This means that the genes necessary for the production of proteins that work towards defending the plant against pathogens have been expressed, and the plant has a "stockpile" of compounds to release to fight off pathogens. [64] A primed defense system is much faster in responding to pathogen induced infection, and may be able to deflect pathogens before they are able to establish themselves. [68] Plants increase the production of lignin, reinforcing cell walls and making it difficult for pathogens to penetrate into the cell, while also cutting off nutrients to already infected cells, effectively halting the invasion. [61] They produce antimicrobial compounds such as phytoalexins, chitinases, and proteinase inhibitors, which prevent the growth of pathogens. [63] These functions of disease suppression and pathogen resistance ultimately lead to an increase in agricultural production and a decrease in the use of chemical pesticides, herbicides, and fungicides because there is a reduced amount of crop loss due to disease. [69] Induced systemic resistance and pathogen-induced systemic acquired resistance are both potential functions of biofilms in the rhizosphere, and should be taken into consideration when applied to new age agricultural practices because of their effect on disease suppression without the use of dangerous chemicals.

Mammalian gut

Studies in 2003 discovered that the immune system supports biofilm development in the large intestine. This was supported mainly with the fact that the two most abundantly produced molecules by the immune system also support biofilm production and are associated with the biofilms developed in the gut. This is especially important because the appendix holds a mass amount of these bacterial biofilms. [70] This discovery helps to distinguish the possible function of the appendix and the idea that the appendix can help reinoculate the gut with good gut flora. However, modified or disrupted states of biofilms in the gut have been connected to diseases such as inflammatory bowel disease and colorectal cancer. [71]

Human environment

In the human environment, biofilms can grow in showers very easily since they provide a moist and warm environment for them to thrive. They can form inside water and sewage pipes and cause clogging and corrosion. On floors and counters, they can make sanitation difficult in food preparation areas. In soil, they can cause bioclogging. In cooling- or heating-water systems, they are known to reduce heat transfer. [72] Biofilms in marine engineering systems, such as pipelines of the offshore oil and gas industry, [73] can lead to substantial corrosion problems. Corrosion is mainly due to abiotic factors; however, at least 20% of corrosion is caused by microorganisms that are attached to the metal subsurface (i.e., microbially influenced corrosion).

Ship fouling

Bacterial adhesion to boat hulls serves as the foundation for biofouling of seagoing vessels. Once a film of bacteria forms, it is easier for other marine organisms such as barnacles to attach. Such fouling can reduce maximum vessel speed by up to 20%, prolonging voyages and consuming fuel. Time in dry dock for refitting and repainting reduces the productivity of shipping assets, and the useful life of ships is also reduced due to corrosion and mechanical removal (scraping) of marine organisms from ships' hulls.

Stromatolites

Stromatolites are layered accretionary structures formed in shallow water by the trapping, binding and cementation of sedimentary grains by microbial biofilms, especially of cyanobacteria. Stromatolites include some of the most ancient records of life on Earth, and are still forming today.

Dental plaque

Within the human body, biofilms are present on the teeth as dental plaque, where they may cause tooth decay and gum disease. These biofilms can either be in an uncalcified state that can be removed by dental instruments, or a calcified state which is more difficult to remove. Removal techniques can also include antimicrobials. [74]

Dental plaque is an oral biofilm that adheres to the teeth and consists of many species of both bacteria and fungi (such as Streptococcus mutans and Candida albicans), embedded in salivary polymers and microbial extracellular products. The accumulation of microorganisms subjects the teeth and gingival tissues to high concentrations of bacterial metabolites which results in dental disease. [75] Biofilm on the surface of teeth is frequently subject to oxidative stress [76] and acid stress. [77] Dietary carbohydrates can cause a dramatic decrease in pH in oral biofilms to values of 4 and below (acid stress). [77] A pH of 4 at body temperature of 37 °C causes depurination of DNA, leaving apurinic (AP) sites in DNA, [78] especially loss of guanine. [79]

Dental plaque biofilm can result in dental caries if it is allowed to develop over time. An ecologic shift away from balanced populations within the dental biofilm is driven by certain (cariogenic) microbiological populations beginning to dominate when the environment favors them. The shift to an acidogenic, aciduric, and cariogenic microbiological population develops and is maintained by frequent consumption of fermentable dietary carbohydrate. The resulting activity shift in the biofilm (and resulting acid production within the biofilm, at the tooth surface) is associated with an imbalance of demineralization over remineralization, leading to net mineral loss within dental hard tissues (enamel and then dentin), the symptom being a carious lesion, or cavity. By preventing the dental plaque biofilm from maturing or by returning it back to a non-cariogenic state, dental caries can be prevented and arrested. [80] [81] This can be achieved through the behavioral step of reducing the supply of fermentable carbohydrates (i.e. sugar intake) and frequent removal of the biofilm (i.e., toothbrushing). [80]

Intercellular communication

A peptide pheromone quorum sensing signaling system in S. mutans includes the competence stimulating peptide (CSP) that controls genetic competence. [82] [83] Genetic competence is the ability of a cell to take up DNA released by another cell. Competence can lead to genetic transformation, a form of sexual interaction, favored under conditions of high cell density and/or stress where there is maximal opportunity for interaction between the competent cell and the DNA released from nearby donor cells. This system is optimally expressed when S. mutans cells reside in an actively growing biofilm. Biofilm grown S. mutans cells are genetically transformed at a rate 10- to 600-fold higher than S. mutans growing as free-floating planktonic cells suspended in liquid. [82]

When the biofilm, containing S. mutans and related oral streptococci, is subjected to acid stress, the competence regulon is induced, leading to resistance to being killed by acid. [77] As pointed out by Michod et al., transformation in bacterial pathogens likely provides for effective and efficient recombinational repair of DNA damages. [84] It appears that S. mutans can survive the frequent acid stress in oral biofilms, in part, through the recombinational repair provided by competence and transformation.

Predator-prey interactions

Predator-prey interactions between biofilms and bacterivores, such as the soil-dwelling nematode Caenorhabditis elegans, had been extensively studied. Via the production of sticky matrix and formation of aggregates, Yersinia pestis biofilms can prevent feeding by obstructing the mouth of C. elegans. [85] Moreover, Pseudomonas aeruginosa biofilms can impede the slithering motility of C. elegans, termed as 'quagmire phenotype', resulting in trapping of C. elegans within the biofilms and preventing the exploration of nematodes to feed on susceptible biofilms. [86] This significantly reduced the ability of predator to feed and reproduce, thereby promoting the survival of biofilms. Pseudomonas aeruginosa biofilms can also mask their chemical signatures, where they reduced the diffusion of quorum sensing molecules into the environment and prevented the detection of C. elegans. [87]

Taxonomic diversity

Many different bacteria form biofilms, including gram-positive (e.g. Bacillus spp, Listeria monocytogenes , Staphylococcus spp, and lactic acid bacteria, including Lactobacillus plantarum and Lactococcus lactis ) and gram-negative species (e.g. Escherichia coli , or Pseudomonas aeruginosa ). [88] Cyanobacteria also form biofilms in aquatic environments. [89]

Biofilms are formed by bacteria that colonize plants, e.g. Pseudomonas putida , Pseudomonas fluorescens , and related pseudomonads which are common plant-associated bacteria found on leaves, roots, and in the soil, and the majority of their natural isolates form biofilms. [90] Several nitrogen-fixing symbionts of legumes such as Rhizobium leguminosarum and Sinorhizobium meliloti form biofilms on legume roots and other inert surfaces. [90]

Along with bacteria, biofilms are also generated by archaea [51] and by a range of eukaryotic organisms, including fungi e.g. Cryptococcus laurentii [91] and microalgae. Among microalgae, one of the main progenitors of biofilms are diatoms, which colonise both fresh and marine environments worldwide. [92] [93]

For other species in disease-associated biofilms and biofilms arising from eukaryotes, see below.

Infectious diseases

Biofilms have been found to be involved in a wide variety of microbial infections in the body, by one estimate 80% of all infections. [94] Infectious processes in which biofilms have been implicated include common problems such as bacterial vaginosis, urinary tract infections, catheter infections, middle-ear infections, formation of dental plaque, [95] gingivitis, coating contact lenses, [96] and less common but more lethal processes such as endocarditis, infections in cystic fibrosis, and infections of permanent indwelling devices such as joint prostheses, heart valves, and intervertebral disc. [97] [98] [99] The first visual evidence of a biofilm was recorded after spine surgery. [100] It was found that in the absence of clinical presentation of infection, impregnated bacteria could form a biofilm around an implant, and this biofilm can remain undetected via contemporary diagnostic methods, including swabbing. Implant biofilm is frequently present in "aseptic" pseudarthrosis cases. [100] [101] [102] Furthermore, it has been noted that bacterial biofilms may impair cutaneous wound healing and reduce topical antibacterial efficiency in healing or treating infected skin wounds. [103] The diversity of P. aeruginosa cells within a biofilm is thought to make it harder to treat the infected lungs of people with cystic fibrosis. [13] Early detection of biofilms in wounds is crucial to successful chronic wound management. Although many techniques have developed to identify planktonic bacteria in viable wounds, few have been able to quickly and accurately identify bacterial biofilms. Future studies are needed to find means of identifying and monitoring biofilm colonization at the bedside to permit timely initiation of treatment. [104]

It has been shown that biofilms are present on the removed tissue of 80% of patients undergoing surgery for chronic sinusitis. The patients with biofilms were shown to have been denuded of cilia and goblet cells, unlike the controls without biofilms who had normal cilia and goblet cell morphology. [105] Biofilms were also found on samples from two of 10 healthy controls mentioned. The species of bacteria from intraoperative cultures did not correspond to the bacteria species in the biofilm on the respective patient's tissue. In other words, the cultures were negative though the bacteria were present. [106] New staining techniques are being developed to differentiate bacterial cells growing in living animals, e.g. from tissues with allergy-inflammations. [107]

Research has shown that sub-therapeutic levels of β-lactam antibiotics induce biofilm formation in Staphylococcus aureus . This sub-therapeutic level of antibiotic may result from the use of antibiotics as growth promoters in agriculture, or during the normal course of antibiotic therapy. The biofilm formation induced by low-level methicillin was inhibited by DNase, suggesting that the sub-therapeutic levels of antibiotic also induce extracellular DNA release. [108] Moreover, from an evolutionary point of view, the creation of the tragedy of the commons in pathogenic microbes may provide advanced therapeutic ways for chronic infections caused by biofilms via genetically engineered invasive cheaters who can invade wild-types 'cooperators' of pathogenic bacteria until cooperator populations go to extinction or overall population 'cooperators and cheaters ' go to extinction. [109]

Pseudomonas aeruginosa

P. aeruginosa represents a commonly used biofilm model organism since it is involved in different types of biofilm-associated chronic infections. [41] Examples of such infections include chronic wounds, chronic otitis media, chronic prostatitis and chronic lung infections in cystic fibrosis (CF) patients. About 80% of CF patients have chronic lung infection, caused mainly by P. aeruginosa growing in a non-surface attached biofilms surround by PMN. [110] The infection remains present despite aggressive antibiotic therapy and is a common cause of death in CF patients due to constant inflammatory damage to the lungs. [41] In patients with CF, one therapy for treating early biofilm development is to employ DNase to structurally weaken the biofilm. [4] [111]

Biofilm formation of P. aeruginosa , along with other bacteria, is found in 90% of chronic wound infections, which leads to poor healing and high cost of treatment estimated at more than US$25 billion every year in the United States. [112] In order to minimize the P. aeruginosa infection, host epithelial cells secrete antimicrobial peptides, such as lactoferrin, to prevent the formation of the biofilms. [113]

Streptococcus pneumoniae

Streptococcus pneumoniae is the main cause of community-acquired pneumonia and meningitis in children and the elderly, and of sepsis in HIV-infected persons. When S. pneumoniae grows in biofilms, genes are specifically expressed that respond to oxidative stress and induce competence. [114] Formation of a biofilm depends on competence stimulating peptide (CSP). CSP also functions as a quorum-sensing peptide. It not only induces biofilm formation, but also increases virulence in pneumonia and meningitis.

It has been proposed that competence development and biofilm formation is an adaptation of S. pneumoniae to survive the defenses of the host. [84] In particular, the host's polymorphonuclear leukocytes produce an oxidative burst to defend against the invading bacteria, and this response can kill bacteria by damaging their DNA. Competent S. pneumoniae in a biofilm have the survival advantage that they can more easily take up transforming DNA from nearby cells in the biofilm to use for recombinational repair of oxidative damages in their DNA. Competent S. pneumoniae can also secrete an enzyme (murein hydrolase) that destroys non-competent cells (fratricide) causing DNA to be released into the surrounding medium for potential use by the competent cells. [115]

The insect antimicrobial peptide cecropin A can destroy planktonic and sessile biofilm-forming uropathogenic E. coli cells, either alone or when combined with the antibiotic nalidixic acid, synergistically clearing infection in vivo (in the insect host Galleria mellonella ) without off-target cytotoxicity. The multi-target mechanism of action involves outer membrane permeabilization followed by biofilm disruption triggered by the inhibition of efflux pump activity and interactions with extracellular and intracellular nucleic acids. [116]

Escherichia coli

Escherichia coli biofilms are responsible for many intestinal infectious diseases. [117] The Extraintestinal group of E. coli (ExPEC) is the dominant bacterial group that attacks the urinary system, which leads to urinary tract infections. [118] The biofilm formation of these pathogenic E. coli is hard to eradicate due to the complexity of its aggregation structure, and it has a significant contribution to developing aggressive medical complications, increase in hospitalization rate, and cost of treatment. [119] [120] The development of E. coli biofilm is a common leading cause of urinary tract infections (UTI) in hospitals through its contribution to developing medical device-associated infections. Catheter-associated urinary tract infections (CAUTI) represent the most common hospital-acquired infection due to the formation of the pathogenic E. coli biofilm inside the catheters. [121]

Staphylococcus aureus

Staphylococcus aureus pathogen can attack skin and lungs, leading to skin infection and pneumonia. [122] [123] Moreover, the biofilm infections network of S. aureus plays a critical role in preventing immune cells, such as macrophages from eliminating and destroying bacterial cells. [124] Furthermore, biofilm formation by bacteria, such as S. aureus, not only develops resistance against antibiotic medication but also develop internal resistance toward antimicrobial peptides (AMPs), leading to preventing the inhibition of the pathogen and maintaining its survival. [125]

Serratia marcescens

Serratia marcescens is a fairly common opportunistic pathogen that can form biofilms on various surfaces, including medical devices such as catheters and implants, as well as natural environments like soil and water. The formation of biofilms by S. marcescens is a serious concern because of its ability to adhere to and colonize surfaces, protecting itself from host immune responses and antimicrobial agents. This strength makes infections caused by S. marcescens challenging to treat, specifically in hospitals where the bacterium can cause severe, and specific, infections.

Research suggests that biofilm formation by S. marcescens is a process controlled by both nutrient cues and the quorum-sensing system. [126] Quorum sensing influences the bacterium's ability to adhere to surfaces and establish mature biofilms, whereas the availability of specific nutrients can enhance or inhibit biofilm development.

S. marcescens creates biofilms that ultimately develop into a highly porous, thread-like structure composed of chains of cells, filaments, and cell clusters. Research has shown that S. marcescens biofilms exhibit complex structural organization, including the formation of microcolonies and channels that facilitate nutrient and waste exchange. The production of extracellular polymeric substances (EPS) is a key factor in biofilm development, contributing to the bacterium's adhesion and resistance to antimicrobial agents. In addition to its role in healthcare-associated infections, S. marcescens biofilms have been implicated in the deterioration of industrial equipment and processes. For example, biofilm growth in cooling towers can lead to biofouling and reduced efficiency.

Efforts to control and prevent biofilm formation by S. marcescens involve the use of antimicrobial coatings on medical devices, the development of targeted biofilm disruptors, and improved sterilization protocols. Further research into the molecular mechanisms governing S. marcescens biofilm formation and persistence is crucial for developing effective strategies to combat its associated risks. The use of indole compounds has been studied to be used as protection against biofilm formation. [127]

Uses and impact

In medicine

It is suggested that around two-thirds of bacterial infections in humans involve biofilms. [50] [128] Infections associated with the biofilm growth usually are challenging to eradicate. [129] This is mostly due to the fact that mature biofilms display antimicrobial tolerance, and immune response evasions. [130] [41] Biofilms often form on the inert surfaces of implanted devices such as catheters, prosthetic cardiac valves and intrauterine devices. [131] Some of the most difficult infections to treat are those associated with the use of medical devices. [50] [101]

The rapidly expanding worldwide industry for biomedical devices and tissue engineering related products is already at $180 billion per year, yet this industry continues to suffer from microbial colonization. No matter the sophistication, microbial infections can develop on all medical devices and tissue engineering constructs. [130] 60-70% of hospital-acquired infections are associated with the implantation of a biomedical device. [130] This leads to 2 million cases annually in the U.S., costing the healthcare system over $5 billion in additional healthcare expenses. [130]

The level of antibiotic resistance in a biofilm is much greater than that of non-biofilm bacteria, and can be as much as 5,000 times greater. [50] The extracellular matrix of biofilm is considered one of the leading factors that can reduce the penetration of antibiotics into a biofilm structure and contributes to antibiotic resistance. [132] Further, it has been demonstrated that the evolution of resistance to antibiotics may be affected by the biofilm lifestyle. [133] Bacteriophage therapy can disperse the biofilm generated by antibiotic-resistant bacteria. [134]

It has been shown that the introduction of a small current of electricity to the liquid surrounding a biofilm, together with small amounts of antibiotic can reduce the level of antibiotic resistance to levels of non-biofilm bacteria. This is termed the bioelectric effect. [50] [135] The application of a small DC current on its own can cause a biofilm to detach from its surface. [50] A study showed that the type of current used made no difference to the bioelectric effect. [135]

In industry

Biofilms can also be harnessed for constructive purposes. For example, many sewage treatment plants include a secondary treatment stage in which waste water passes over biofilms grown on filters, which extract and digest organic compounds. In such biofilms, bacteria are mainly responsible for removal of organic matter (BOD), while protozoa and rotifers are mainly responsible for removal of suspended solids (SS), including pathogens and other microorganisms. Slow sand filters rely on biofilm development in the same way to filter surface water from lake, spring or river sources for drinking purposes. What is regarded as clean water is effectively a waste material to these microcellular organisms. Biofilms can help eliminate petroleum oil from contaminated oceans or marine systems. The oil is eliminated by the hydrocarbon-degrading activities of communities of hydrocarbonoclastic bacteria (HCB). [136] Biofilms are used in microbial fuel cells (MFCs) to generate electricity from a variety of starting materials, including complex organic waste and renewable biomass. [7] [137] [138] Biofilms are also relevant for the improvement of metal dissolution in bioleaching industry, [139] and aggregation of microplastics pollutants for convenient removal from the environment. [140] [141]

Food industry

Biofilms have become problematic in several food industries due to the ability to form on plants and during industrial processes. [142] Bacteria can survive long periods of time in water, animal manure, and soil, causing biofilm formation on plants or in the processing equipment. [143] The buildup of biofilms can affect the heat flow across a surface and increase surface corrosion and frictional resistance of fluids. [144] These can lead to a loss of energy in a system and overall loss of products. [144] Along with economic problems, biofilm formation on food poses a health risk to consumers due to the ability to make the food more resistant to disinfectants [142] As a result, from 1996 to 2010 the Centers for Disease Control and Prevention estimated 48 million foodborne illnesses per year. [142] Biofilms have been connected to about 80% of bacterial infections in the United States. [142]

In produce, microorganisms attach to the surfaces and biofilms develop internally. [142] During the washing process, biofilms resist sanitization and allow bacteria to spread across the produce, [142] especially via kitchen utensils. [145] This problem is also found in ready-to-eat foods, because the foods go through limited cleaning procedures before consumption [142] Due to the perishability of dairy products and limitations in cleaning procedures, resulting in the buildup of bacteria, dairy is susceptible to biofilm formation and contamination. [142] [144] The bacteria can spoil the products more readily and contaminated products pose a health risk to consumers. One species of bacteria that can be found in various industries and is a major cause of foodborne disease is Salmonella . [146] Large amounts of Salmonella contamination can be found in the poultry processing industry as about 50% of Salmonella strains can produce biofilms on poultry farms. [142] Salmonella increases the risk of foodborne illnesses when the poultry products are not cleaned and cooked correctly. Salmonella is also found in the seafood industry where biofilms form from seafood borne pathogens on the seafood itself as well as in water. [146] Shrimp products are commonly affected by Salmonella because of unhygienic processing and handling techniques [146] The preparation practices of shrimp and other seafood products can allow for bacteria buildup on the products. [146]

New forms of cleaning procedures are being tested to reduce biofilm formation in these processes which will lead to safer and more productive food processing industries. These new forms of cleaning procedures also have a profound effect on the environment, often releasing toxic gases into the groundwater reservoirs. [144] As a response to the aggressive methods employed in controlling biofilm formation, there are a number of novel technologies and chemicals under investigation that can prevent either the proliferation or adhesion of biofilm-secreting microbes. Latest proposed biomolecules presenting marked anti-biofilm activity include a range of metabolites such as bacterial rhamnolipids [147] and even plant- [148] and animal-derived alkaloids. [149]

In aquaculture

A biofilm from the Dead Sea Screen Shot 2017-12-13 at 1.40.19 PM.png
A biofilm from the Dead Sea

In shellfish and algal aquaculture, biofouling microbial species tend to block nets and cages and ultimately outcompete the farmed species for space and food. [150] Bacterial biofilms start the colonization process by creating microenvironments that are more favorable for biofouling species. In the marine environment, biofilms could reduce the hydrodynamic efficiency of ships and propellers, lead to pipeline blockage and sensor malfunction, and increase the weight of appliances deployed in seawater. [151] Numerous studies have shown that biofilm can be a reservoir for potentially pathogenic bacteria in freshwater aquaculture. [152] [153] [154] [155] Moreover, biofilms are important in establishing infections on the fish. [156] As mentioned previously, biofilms can be difficult to eliminate even when antibiotics or chemicals are used in high doses. [157] [158] The role that biofilm plays as reservoirs of bacterial fish pathogens has not been explored in detail but it certainly deserves to be studied.

Eukaryotic

Along with bacteria, biofilms are often initiated and produced by eukaryotic microbes. The biofilms produced by eukaryotes is usually occupied by bacteria and other eukaryotes alike, however the surface is cultivated and EPS is secreted initially by the eukaryote. [91] [92] [159] Both fungi and microalgae are known to form biofilms in such a way. Biofilms of fungal origin are important aspects of human infection and fungal pathogenicity, as the fungal infection is more resistant to antifungals. [160] [161]

In the environment, fungal biofilms are an area of ongoing research. One key area of research is fungal biofilms on plants. For example, in the soil, plant associated fungi including mycorrhiza have been shown to decompose organic matter and protect plants from bacterial pathogens. [162]

Biofilms in aquatic environments are often founded by diatoms. The exact purpose of these biofilms is unknown, however there is evidence that the EPS produced by diatoms facilitates both cold and salinity stress. [93] [163] These eukaryotes interact with a diverse range of other organisms within a region known as the phycosphere, but importantly are the bacteria associated with diatoms, as it has been shown that although diatoms excrete EPS, they only do so when interacting with certain bacteria species. [164] [165]

Horizontal gene transfer

Horizontal gene transfer is the lateral transfer of genetic material between cellular organisms. It happens frequently in prokaryotes, and less frequently in eukaryotes. In bacteria, horizontal gene transfer can occur through transformation (uptake of free floating DNA in the environment), transduction (virus mediated DNA uptake), or conjugation (transfer of DNA between pili structures of two adjacent bacteria). [166] Recent studies have also uncovered other mechanisms, such as membrane vesicle transmission or gene transfer agents. [167] Biofilms promote horizontal gene transfer in a variety of ways.

Transmission electron micrograph showing bacteria Escherichia coli that form extensive biofilms using a network of conjugative F-pili. Source: Jonasz Patkowski Escherichia coli forming biofilms via F-pilus.tif
Transmission electron micrograph showing bacteria Escherichia coli that form extensive biofilms using a network of conjugative F-pili. Source: Jonasz Patkowski

Bacterial conjugation has been shown to accelerate biofilm formation in difficult environment due to the robust connections established by the conjugative pili. [168] These connections can often foster cross-species transfer events due to the diverse heterogeneity of many biofilms. Additionally, biofilms are structurally confined by a polysaccharide matrix, providing the close spatial requirements for conjugation. Transformation is also frequently observed in biofilms. Bacterial autolysis is a key mechanism in biofilm structural regulation, providing an abundant source of competent DNA primed for transformative uptake. [169] [167] In some instances, inter-biofilm quorum sensing can enhance the competence of free floating eDNA, further promoting transformation. [167] Stx gene transfer through bacteriophage carriers has been witnessed within biofilms, which suggests that biofilms are also a suitable environment for transduction. [167] Membrane vesicles HGT occurs when released membrane vesicles (containing genetic information) fuse with a recipient bacteria, and release genetic material into the bacteria's cytoplasm. [167] Recent research has revealed that membrane vesicle HGT can promote single-strain biofilm formation, yet the role membrane vesicle HGT plays in the formation of multistrain biofilms is still unknown. [167] GTAs, or gene transfer agents, are phage-like particles produced by the host bacteria and contain random DNA fragments from the host bacteria genome. [167] HGT within biofilms can confer antibiotic resistance or increased pathogenicity across the biofilms' population, promoting biofilm homeostasis. [167]

Examples

Conjugative plasmids may encode biofilm-associated proteins, such as PtgA, PrgB, or PrgC which promote cell adhesion (required for early biofilm formation). [170] Genes encoding type III fimbriae are found in pOLA52 ( Klebsiella pneumoniae plasmid) which promote conjugative-pilus-dependent biofilm formation. [170]

Transformation commonly occurs within biofilms. A phenomenon called fratricide can be seen among streptococcal species in which cell-wall degrading enzymes are released, lysing neighboring bacteria and releasing their DNA. This DNA can then be taken up by the surviving bacteria (transformation). [170] Competence stimulating peptides may play an important role in biofilm formation among S. pneumoniae and S. mutans as well. [170] Among V. cholerae, the competence pilus itself promotes cell aggregation through pilus-pilus interactions at the beginning of biofilm formation. [170]

Phage invasion may play a role in biofilm life cycles, lysing bacteria and releasing their eDNA, which strengthens biofilm structures and can be taken up by neighboring bacteria in transformation. [170] Biofilm destruction caused by the E. coli phage Rac and the P. aeruginosa prophage Pf4 causes detachment of cells from the biofilm. [170] Detachment is a biofilm phenomenon which requires more study, but is hypothesized to proliferate the bacterial species that comprise the biofilm.

Membrane vesicle HGT has been witnessed occurring in marine environments, among Neisseria gonorrhoeae , Pseudomonas aeruginosa , Helicobacter pylori , and among many other bacterial species. [170] Even though membrane vesicle HGT has been shown as a contributing factor in biofilm formation, research is still required to prove that membrane vesicle mediated HGT occurs within biofilms. [167] [170] Membrane vesicle HGT has also been shown to modulate phage-bacteria interactions in Bacillus subtilis SPP1 phage-resistant cells (lacking the SPP1 receptor protein). Upon exposure to vesicles containing receptors, transduction of pBT163 (a cat-encoding plasmid) occurs, resulting in the expression of the SPP1 receptor protein, opening the receptive bacteria to future phage infection. [170]

Recent research has shown that the archaeal species H. volcanii has some biofilm phenotypes similar to bacterial biofilms such as differentiation and HGT, which required cell-cell contact and involved formation of cytosolic bridges and cellular fusion events. [171]

Cultivation devices

There is a wide variety of biofilm cultivation devices to mimic natural or industrial environments. Although it is important to consider that the particular experimental platform for biofilm research determines what kind of biofilm is cultivated and the data that can be extracted. These devices can be grouped into the following: [172]

See also

Related Research Articles

<i>Pseudomonas fluorescens</i> Species of bacterium

Pseudomonas fluorescens is a common Gram-negative, rod-shaped bacterium. It belongs to the Pseudomonas genus; 16S rRNA analysis as well as phylogenomic analysis has placed P. fluorescens in the P. fluorescens group within the genus, to which it lends its name.

<span class="mw-page-title-main">Phage therapy</span> Therapeutic use of bacteriophages to treat bacterial infections

Phage therapy, viral phage therapy, or phagotherapy is the therapeutic use of bacteriophages for the treatment of pathogenic bacterial infections. This therapeutic approach emerged at the beginning of the 20th century but was progressively replaced by the use of antibiotics in most parts of the world after the Second World War. Bacteriophages, known as phages, are a form of virus that attach to bacterial cells and inject their genome into the cell. The bacteria's production of the viral genome interferes with its ability to function, halting the bacterial infection. The bacterial cell causing the infection is unable to reproduce and instead produces additional phages. Phages are very selective in the strains of bacteria they are effective against.

A slime layer in bacteria is an easily removable, unorganized layer of extracellular material that surrounds bacteria cells. Specifically, this consists mostly of exopolysaccharides, glycoproteins, and glycolipids. Therefore, the slime layer is considered as a subset of glycocalyx.

<i>Pseudomonas aeruginosa</i> Species of bacterium

Pseudomonas aeruginosa is a common encapsulated, Gram-negative, aerobic–facultatively anaerobic, rod-shaped bacterium that can cause disease in plants and animals, including humans. A species of considerable medical importance, P. aeruginosa is a multidrug resistant pathogen recognized for its ubiquity, its intrinsically advanced antibiotic resistance mechanisms, and its association with serious illnesses – hospital-acquired infections such as ventilator-associated pneumonia and various sepsis syndromes. P. aeruginosa is able to selectively inhibit various antibiotics from penetrating its outer membrane - and has high resistance to several antibiotics. According to the World Health Organization P. aeruginosa poses one of the greatest threats to humans in terms of antibiotic resistance.

<i>Staphylococcus epidermidis</i> Species of bacterium

Staphylococcus epidermidis is a Gram-positive bacterium, and one of over 40 species belonging to the genus Staphylococcus. It is part of the normal human microbiota, typically the skin microbiota, and less commonly the mucosal microbiota and also found in marine sponges. It is a facultative anaerobic bacteria. Although S. epidermidis is not usually pathogenic, patients with compromised immune systems are at risk of developing infection. These infections are generally hospital-acquired. S. epidermidis is a particular concern for people with catheters or other surgical implants because it is known to form biofilms that grow on these devices. Being part of the normal skin microbiota, S. epidermidis is a frequent contaminant of specimens sent to the diagnostic laboratory.

<i>Stenotrophomonas maltophilia</i> Species of bacterium

Stenotrophomonas maltophilia is an aerobic, nonfermentative, Gram-negative bacterium. It is an uncommon bacterium and human infection is difficult to treat. Initially classified as Bacterium bookeri, then renamed Pseudomonas maltophilia, S. maltophilia was also grouped in the genus Xanthomonas before eventually becoming the type species of the genus Stenotrophomonas in 1993.

<span class="mw-page-title-main">Filamentation</span> Type of bacteria growth

Filamentation is the anomalous growth of certain bacteria, such as Escherichia coli, in which cells continue to elongate but do not divide. The cells that result from elongation without division have multiple chromosomal copies.

<span class="mw-page-title-main">Efflux pump</span> Protein complexes that move compounds, generally toxic, out of bacterial cells

An efflux pump is an active transporter in cells that moves out unwanted material. Efflux pumps are an important component in bacteria in their ability to remove antibiotics. The efflux could also be the movement of heavy metals, organic pollutants, plant-produced compounds, quorum sensing signals, bacterial metabolites and neurotransmitters. All microorganisms, with a few exceptions, have highly conserved DNA sequences in their genome that encode efflux pumps. Efflux pumps actively move substances out of a microorganism, in a process known as active efflux, which is a vital part of xenobiotic metabolism. This active efflux mechanism is responsible for various types of resistance to bacterial pathogens within bacterial species - the most concerning being antibiotic resistance because microorganisms can have adapted efflux pumps to divert toxins out of the cytoplasm and into extracellular media.

<i>Acinetobacter baumannii</i> Species of bacterium

Acinetobacter baumannii is a typically short, almost round, rod-shaped (coccobacillus) Gram-negative bacterium. It is named after the bacteriologist Paul Baumann. It can be an opportunistic pathogen in humans, affecting people with compromised immune systems, and is becoming increasingly important as a hospital-derived (nosocomial) infection. While other species of the genus Acinetobacter are often found in soil samples, it is almost exclusively isolated from hospital environments. Although occasionally it has been found in environmental soil and water samples, its natural habitat is still not known.

<span class="mw-page-title-main">Extracellular polymeric substance</span> Gluey polymers secreted by microorganisms to form biofilms

Extracellular polymeric substances (EPSs) are natural polymers of high molecular weight secreted by microorganisms into their environment. EPSs establish the functional and structural integrity of biofilms, and are considered the fundamental component that determines the physicochemical properties of a biofilm. EPS in the matrix of biofilms provides compositional support and protection of microbial communities from the harsh environments. Components of EPS can be of different classes of polysaccharides, lipids, nucleic acids, proteins, lipopolysaccharides, and minerals.

Persister cells are subpopulations of cells that resist treatment, and become antimicrobial tolerant by changing to a state of dormancy or quiescence. Persister cells in their dormancy do not divide. The tolerance shown in persister cells differs from antimicrobial resistance in that the tolerance is not inherited and is reversible. When treatment has stopped the state of dormancy can be reversed and the cells can reactivate and multiply. Most persister cells are bacterial, and there are also fungal persister cells, yeast persister cells, and cancer persister cells that show tolerance for cancer drugs.

Roberto Kolter is Professor of Microbiology, Emeritus at Harvard Medical School, an author, and past president of the American Society for Microbiology. Kolter has been a professor at Harvard Medical School since 1983 and was Co-director of Harvard's Microbial Sciences Initiative from 2003-2018. During the 35-year term of the Kolter laboratory from 1983 to 2018, more than 130 graduate student and postdoctoral trainees explored an eclectic mix of topics gravitating around the study of microbes. Kolter is a fellow of the American Association for the Advancement of Science and of the American Academy of Microbiology.

Biofilm formation occurs when free floating microorganisms attach themselves to a surface. Although there are some beneficial uses of biofilms, they are generally considered undesirable, and means of biofilm prevention have been developed. Biofilms secrete extracellular polymeric substance that provides a structural matrix and facilitates adhesion for the microorganisms; the means of prevention have thus concentrated largely on two areas: killing the microbes that form the film, or preventing the adhesion of the microbes to a surface. Because biofilms protect the bacteria, they are often more resistant to traditional antimicrobial treatments, making them a serious health risk. For example, there are more than one million cases of catheter-associated urinary tract infections (CAUTI) reported each year, many of which can be attributed to bacterial biofilms. There is much research into the prevention of biofilms.

<span class="mw-page-title-main">Rhamnolipid</span> Chemical compound

Rhamnolipids are a class of glycolipid produced by Pseudomonas aeruginosa, amongst other organisms, frequently cited as bacterial surfactants. They have a glycosyl head group, in this case a rhamnose moiety, and a 3-(hydroxyalkanoyloxy)alkanoic acid (HAA) fatty acid tail, such as 3-hydroxydecanoic acid.

Bacterial morphological plasticity refers to changes in the shape and size that bacterial cells undergo when they encounter stressful environments. Although bacteria have evolved complex molecular strategies to maintain their shape, many are able to alter their shape as a survival strategy in response to protist predators, antibiotics, the immune response, and other threats.

ESKAPE is an acronym comprising the scientific names of six highly virulent and antibiotic resistant bacterial pathogens including: Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter spp. The acronym is sometimes extended to ESKAPEE to include Escherichia coli. This group of Gram-positive and Gram-negative bacteria can evade or 'escape' commonly used antibiotics due to their increasing multi-drug resistance (MDR). As a result, throughout the world, they are the major cause of life-threatening nosocomial or hospital-acquired infections in immunocompromised and critically ill patients who are most at risk. P. aeruginosa and S. aureus are some of the most ubiquitous pathogens in biofilms found in healthcare. P. aeruginosa is a Gram-negative, rod-shaped bacterium, commonly found in the gut flora, soil, and water that can be spread directly or indirectly to patients in healthcare settings. The pathogen can also be spread in other locations through contamination, including surfaces, equipment, and hands. The opportunistic pathogen can cause hospitalized patients to have infections in the lungs, blood, urinary tract, and in other body regions after surgery. S. aureus is a Gram-positive, cocci-shaped bacterium, residing in the environment and on the skin and nose of many healthy individuals. The bacterium can cause skin and bone infections, pneumonia, and other types of potentially serious infections if it enters the body. S. aureus has also gained resistance to many antibiotic treatments, making healing difficult. Because of natural and unnatural selective pressures and factors, antibiotic resistance in bacteria usually emerges through genetic mutation or acquires antibiotic-resistant genes (ARGs) through horizontal gene transfer - a genetic exchange process by which antibiotic resistance can spread.

<span class="mw-page-title-main">Twitching motility</span> Form of crawling bacterial motility

Twitching motility is a form of crawling bacterial motility used to move over surfaces. Twitching is mediated by the activity of hair-like filaments called type IV pili which extend from the cell's exterior, bind to surrounding solid substrates, and retract, pulling the cell forwards in a manner similar to the action of a grappling hook. The name twitching motility is derived from the characteristic jerky and irregular motions of individual cells when viewed under the microscope. It has been observed in many bacterial species, but is most well studied in Pseudomonas aeruginosa, Neisseria gonorrhoeae and Myxococcus xanthus. Active movement mediated by the twitching system has been shown to be an important component of the pathogenic mechanisms of several species.

<span class="mw-page-title-main">Pho regulon</span> Phosphate regulatory mechanism in cells

The Phosphate (Pho) regulon is a regulatory mechanism used for the conservation and management of inorganic phosphate within the cell. It was first discovered in Escherichia coli as an operating system for the bacterial strain, and was later identified in other species. The Pho system is composed of various components including extracellular enzymes and transporters that are capable of phosphate assimilation in addition to extracting inorganic phosphate from organic sources. This is an essential process since phosphate plays an important role in cellular membranes, genetic expression, and metabolism within the cell. Under low nutrient availability, the Pho regulon helps the cell survive and thrive despite a depletion of phosphate within the environment. When this occurs, phosphate starvation-inducible (psi) genes activate other proteins that aid in the transport of inorganic phosphate.

Niels Høiby is a Danish physician, professor and politician. He specialises in microbiology and was a pioneer in the study of biofilms and their role in conditions such as cystic fibrosis. He worked for many years as a department head at Denmark's largest hospital, the Rigshospitalet.

Diffusible signal factor (DSF) is found in several gram-negative bacteria and play a role in the formation of biofilms, motility, virulence, and antibiotic resistance. Xanthomonas campestris was the first bacteria known to have DSF. The synthesis of the DSF can be seen in rpfF and rpfB enzymes. An understanding of the DSF signaling mechanism could lead to further disease control.

References

  1. ↑ Vert M, Doi Y, Hellwich KH, Hess M, Hodge P, Kubisa P, et al. (2012). "Terminology for biorelated polymers and applications (IUPAC Recommendations 2012)". Pure and Applied Chemistry . 84 (2): 377–410. doi: 10.1351/PAC-REC-10-12-04 .
  2. 1 2 3 López D, Vlamakis H, Kolter R (July 2010). "Biofilms". Cold Spring Harbor Perspectives in Biology. 2 (7): a000398. doi:10.1101/cshperspect.a000398. PMC   2890205 . PMID   20519345.
  3. 1 2 3 4 5 Hall-Stoodley L, Costerton JW, Stoodley P (February 2004). "Bacterial biofilms: from the natural environment to infectious diseases". Nature Reviews. Microbiology. 2 (2): 95–108. doi:10.1038/nrmicro821. PMID   15040259. S2CID   9107205.
  4. 1 2 Aggarwal S, Stewart PS, Hozalski RM (January 2016). "Biofilm Cohesive Strength as a Basis for Biofilm Recalcitrance: Are Bacterial Biofilms Overdesigned?". Microbiology Insights. 8 (Suppl 2): 29–32. doi:10.4137/MBI.S31444. PMC   4718087 . PMID   26819559.
  5. 1 2 Watnick P, Kolter R (May 2000). "Biofilm, city of microbes". Journal of Bacteriology. 182 (10): 2675–9. doi:10.1128/jb.182.10.2675-2679.2000. PMC   101960 . PMID   10781532.
  6. ↑ "Building Codes for Bacterial Cities | Quanta Magazine". Quanta Magazine. Archived from the original on 26 July 2017. Retrieved 25 July 2017.
  7. 1 2 Lear G, Lewis GD, eds. (2012). Microbial Biofilms: Current Research and Applications. Caister Academic Press. ISBN   978-1-904455-96-7.
  8. 1 2 O'Toole GA, Kolter R (May 1998). "Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis". Molecular Microbiology. 28 (3): 449–61. doi: 10.1046/j.1365-2958.1998.00797.x . PMID   9632250. S2CID   43897816.
  9. ↑ O'Toole GA, Kolter R (October 1998). "Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development". Molecular Microbiology. 30 (2): 295–304. doi: 10.1046/j.1365-2958.1998.01062.x . PMID   9791175. S2CID   25140899.
  10. ↑ Karatan E, Watnick P (June 2009). "Signals, regulatory networks, and materials that build and break bacterial biofilms". Microbiology and Molecular Biology Reviews. 73 (2): 310–47. doi:10.1128/MMBR.00041-08. PMC   2698413 . PMID   19487730.
  11. ↑ Hoffman LR, D'Argenio DA, MacCoss MJ, Zhang Z, Jones RA, Miller SI (August 2005). "Aminoglycoside antibiotics induce bacterial biofilm formation". Nature. 436 (7054): 1171–5. Bibcode:2005Natur.436.1171H. doi:10.1038/nature03912. PMID   16121184. S2CID   4404961. (primary source)
  12. ↑ An D, Parsek MR (June 2007). "The promise and peril of transcriptional profiling in biofilm communities". Current Opinion in Microbiology. 10 (3): 292–6. doi:10.1016/j.mib.2007.05.011. PMID   17573234.
  13. 1 2 Momeni B (June 2018). "Division of Labor: How Microbes Split Their Responsibility". Current Biology. 28 (12): R697–R699. Bibcode:2018CBio...28.R697M. doi: 10.1016/j.cub.2018.05.024 . PMID   29920261. S2CID   49315067.
  14. ↑ Case C, Funke B, Tortora G. Microbiology An Introduction (tenth ed.).
  15. ↑ Briandet R, Herry J, Bellon-Fontaine M (August 2001). "Determination of the van der Waals, electron donor and electron acceptor surface tension components of static Gram-positive microbial biofilms". Colloids Surf B. 21 (4): 299–310. doi:10.1016/S0927-7765(00)00213-7. PMID   11397632.
  16. ↑ Takahashi H, Suda T, Tanaka Y, Kimura B (June 2010). "Cellular hydrophobicity of Listeria monocytogenes involves initial attachment and biofilm formation on the surface of polyvinyl chloride". Lett. Appl. Microbiol. 50 (6): 618–25. doi: 10.1111/j.1472-765X.2010.02842.x . PMID   20438621. S2CID   24880220.
  17. ↑ "7: Archaea". Biology LibreTexts. 6 February 2018. Archived from the original on 23 September 2020. Retrieved 10 August 2020.
  18. ↑ Madigan M (2019). Brock biology of microorganisms (Fifteenth, Global ed.). Pearson. p. 86. ISBN   978-1-292-23510-3.
  19. 1 2 Wang F, Cvirkaite-Krupovic V, Krupovic M, Egelman EH (June 2022). "Archaeal bundling pili of Pyrobaculum calidifontis reveal similarities between archaeal and bacterial biofilms". Proceedings of the National Academy of Sciences of the United States of America. 119 (26): e2207037119. Bibcode:2022PNAS..11907037W. doi: 10.1073/pnas.2207037119 . PMC   9245690 . PMID   35727984.
  20. ↑ "Golden Dome Cave" Archived 13 December 2022 at the Wayback Machine . National Park Service. November 6, 2021. Retrieved February 11, 2024.
  21. 1 2 3 Donlan RM (2002). "Biofilms: Microbial Life on Surfaces". Emerging Infectious Diseases. 8 (9): 881–890. doi:10.3201/eid0809.020063. PMC   2732559 . PMID   12194761.
  22. ↑ Li S, Liu SY, Chan SY, Chua SL (January 2022). "Biofilm matrix cloaks bacterial quorum sensing chemoattractants from predator detection". The ISME Journal. 16 (5): 1388–1396. Bibcode:2022ISMEJ..16.1388L. doi:10.1038/s41396-022-01190-2. PMC   9038794 . PMID   35034106.
  23. ↑ Ciofu O, Tolker-Nielsen T (2019). "Tolerance and Resistance of Pseudomonas aeruginosa Biofilms to Antimicrobial Agents-How P. aeruginosa Can Escape Antibiotics". Frontiers in Microbiology. 10: 913. doi: 10.3389/fmicb.2019.00913 . PMC   6509751 . PMID   31130925.
  24. ↑ Sakuragi Y, Kolter R (July 2007). "Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa". Journal of Bacteriology. 189 (14): 5383–6. doi: 10.1128/JB.00137-07 . PMC   1951888 . PMID   17496081.
  25. 1 2 Rapacka-Zdonczyk A, Wozniak A, Nakonieczna J, Grinholc M (February 2021). "Development of Antimicrobial Phototreatment Tolerance: Why the Methodology Matters". International Journal of Molecular Sciences. 22 (4). MDPI AG: 2224. doi: 10.3390/ijms22042224 . PMC   7926562 . PMID   33672375. CC-BY icon.svg Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License Archived 16 October 2017 at the Wayback Machine .
  26. ↑ Hall CW, Mah TF (May 2017). "Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria". FEMS Microbiology Reviews. 41 (3). Oxford University Press (OUP): 276–301. doi: 10.1093/femsre/fux010 . PMID   28369412.
  27. ↑ O'Toole G, Kaplan HB, Kolter R (2000). "Biofilm formation as microbial development". Annual Review of Microbiology. 54: 49–79. doi: 10.1146/annurev.micro.54.1.49 . PMID   11018124.
  28. 1 2 Monroe D (November 2007). "Looking for chinks in the armor of bacterial biofilms". PLOS Biology. 5 (11): e307. doi: 10.1371/journal.pbio.0050307 . PMC   2071939 . PMID   18001153.
  29. ↑ Kaplan JB, Ragunath C, Ramasubbu N, Fine DH (August 2003). "Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous beta-hexosaminidase activity". Journal of Bacteriology. 185 (16): 4693–8. doi:10.1128/JB.185.16.4693-4698.2003. PMC   166467 . PMID   12896987.
  30. ↑ Izano EA, Amarante MA, Kher WB, Kaplan JB (January 2008). "Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms". Applied and Environmental Microbiology. 74 (2): 470–6. Bibcode:2008ApEnM..74..470I. doi:10.1128/AEM.02073-07. PMC   2223269 . PMID   18039822.
  31. ↑ Kaplan JB, Ragunath C, Velliyagounder K, Fine DH, Ramasubbu N (July 2004). "Enzymatic detachment of Staphylococcus epidermidis biofilms". Antimicrobial Agents and Chemotherapy. 48 (7): 2633–6. doi:10.1128/AAC.48.7.2633-2636.2004. PMC   434209 . PMID   15215120.
  32. ↑ Xavier JB, Picioreanu C, Rani SA, van Loosdrecht MC, Stewart PS (December 2005). "Biofilm-control strategies based on enzymic disruption of the extracellular polymeric substance matrix--a modelling study". Microbiology. 151 (Pt 12): 3817–32. doi: 10.1099/mic.0.28165-0 . PMID   16339929.
  33. ↑ Davies DG, Marques CN (March 2009). "A fatty acid messenger is responsible for inducing dispersion in microbial biofilms". Journal of Bacteriology. 191 (5): 1393–403. doi:10.1128/JB.01214-08. PMC   2648214 . PMID   19074399.
  34. ↑ Barraud N, Hassett DJ, Hwang SH, Rice SA, Kjelleberg S, Webb JS (2006). "Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa". Journal of Bacteriology. 188 (21): 7344–7353. doi:10.1128/jb.00779-06. PMC   1636254 . PMID   17050922.
  35. ↑ Barraud N, Storey MV, Moore ZP, Webb JS, Rice SA, Kjelleberg S (2009). "Nitric oxide-mediated dispersal in single- and multi-species biofilms of clinically and industrially relevant microorganisms". Microbial Biotechnology. 2 (3): 370–378. doi:10.1111/j.1751-7915.2009.00098.x. PMC   3815757 . PMID   21261931.
  36. ↑ "Dispersal of Biofilm in Cystic Fibrosis using Low Dose Nitric Oxide". University of Southampton. Archived from the original on 8 December 2013. Retrieved 20 January 2012.
  37. 1 2 Chua SL, Liu Y, Yam JK, Tolker-Nielsen T, Kjelleberg S, Givskov M, et al. (2014). "Dispersed cells represent a distinct stage in the transition from bacterial biofilm to planktonic lifestyles". Nature Communications. 5: 4462. Bibcode:2014NatCo...5.4462C. doi: 10.1038/ncomms5462 . PMID   25042103.
  38. ↑ Chua SL, Hultqvist LD, Yuan M, Rybtke M, Nielsen TE, Givskov M, et al. (August 2015). "In vitro and in vivo generation and characterization of Pseudomonas aeruginosa biofilm-dispersed cells via c-di-GMP manipulation". Nat Protoc. 10 (8): 1165–80. doi:10.1038/nprot.2015.067. hdl: 10356/84100 . PMID   26158442. S2CID   20235088.
  39. 1 2 Ma Y, Deng Y, Hua H, Khoo BL, Chua SL (August 2023). "Distinct bacterial population dynamics and disease dissemination after biofilm dispersal and disassembly". The ISME Journal. 17 (8): 1290–1302. Bibcode:2023ISMEJ..17.1290M. doi:10.1038/s41396-023-01446-5. PMC   10356768 . PMID   37270584.
  40. ↑ Nadell CD, Xavier JB, Foster KR (January 2009). "The sociobiology of biofilms". FEMS Microbiology Reviews. 33 (1): 206–24. doi: 10.1111/j.1574-6976.2008.00150.x . PMID   19067751.
  41. 1 2 3 4 Rybtke M, Hultqvist LD, Givskov M, Tolker-Nielsen T (November 2015). "Pseudomonas aeruginosa Biofilm Infections: Community Structure, Antimicrobial Tolerance and Immune Response". Journal of Molecular Biology. 427 (23): 3628–45. doi:10.1016/j.jmb.2015.08.016. PMID   26319792.
  42. ↑ Danese PN, Pratt LA, Kolter R (June 2000). "Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture". Journal of Bacteriology. 182 (12): 3593–6. doi:10.1128/jb.182.12.3593-3596.2000. PMC   101973 . PMID   10852895.
  43. ↑ Branda SS, Chu F, Kearns DB, Losick R, Kolter R (February 2006). "A major protein component of the Bacillus subtilis biofilm matrix". Molecular Microbiology. 59 (4): 1229–38. doi: 10.1111/j.1365-2958.2005.05020.x . PMID   16430696. S2CID   3041295.
  44. ↑ Choong FX, Bäck M, Fahlén S, Johansson LB, Melican K, Rhen M, et al. (23 November 2016). "Salmonella biofilms using luminescent oligothiophenes". npj Biofilms and Microbiomes. 2: 16024. doi:10.1038/npjbiofilms.2016.24. PMC   5515270 . PMID   28721253.
  45. ↑ Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S (August 2016). "Biofilms: an emergent form of bacterial life". Nature Reviews. Microbiology. 14 (9): 563–75. doi:10.1038/nrmicro.2016.94. PMID   27510863. S2CID   4384131.
  46. ↑ Stoodley P, Debeer D, Lewandowski Z (August 1994). "Liquid flow in biofilm systems". Applied and Environmental Microbiology. 60 (8): 2711–6. Bibcode:1994ApEnM..60.2711S. doi:10.1128/aem.60.8.2711-2716.1994. PMC   201713 . PMID   16349345.
  47. ↑ Vlamakis H, Aguilar C, Losick R, Kolter R (April 2008). "Control of cell fate by the formation of an architecturally complex bacterial community". Genes & Development. 22 (7): 945–53. doi:10.1101/gad.1645008. PMC   2279205 . PMID   18381896.
  48. ↑ Stewart PS, Costerton JW (July 2001). "Antibiotic resistance of bacteria in biofilms". Lancet. 358 (9276): 135–8. doi:10.1016/S0140-6736(01)05321-1. PMID   11463434. S2CID   46125592.
  49. ↑ Pandey R, Mishra SK, Shrestha A (2021). "Characterisation of ESKAPE Pathogens with Special Reference to Multidrug Resistance and Biofilm Production in a Nepalese Hospital". Infect Drug Resist. 14: 2201–2212. doi: 10.2147/IDR.S306688 . PMC   8214009 . PMID   34163185.
  50. 1 2 3 4 5 6 Del Pozo JL, Rouse MS, Patel R (September 2008). "Bioelectric effect and bacterial biofilms. A systematic review". The International Journal of Artificial Organs. 31 (9): 786–795. doi:10.1177/039139880803100906. PMC   3910516 . PMID   18924090.
  51. 1 2 Chimileski S, Franklin MJ, Papke RT (August 2014). "Biofilms formed by the archaeon Haloferax volcanii exhibit cellular differentiation and social motility, and facilitate horizontal gene transfer". BMC Biology. 12: 65. doi: 10.1186/s12915-014-0065-5 . PMC   4180959 . PMID   25124934.
  52. ↑ Molin S, Tolker-Nielsen T (June 2003). "Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure". Current Opinion in Biotechnology. 14 (3): 255–61. doi:10.1016/S0958-1669(03)00036-3. PMID   12849777.
  53. ↑ Jakubovics NS, Shields RC, Rajarajan N, Burgess JG (December 2013). "Life after death: the critical role of extracellular DNA in microbial biofilms". Letters in Applied Microbiology. 57 (6): 467–75. doi: 10.1111/lam.12134 . PMID   23848166. S2CID   206168952.
  54. ↑ Spoering AL, Lewis K (December 2001). "Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials". Journal of Bacteriology. 183 (23): 6746–51. doi:10.1128/JB.183.23.6746-6751.2001. PMC   95513 . PMID   11698361.
  55. ↑ "Introduction to Biofilms: Desirable and undesirable impacts of biofilm". Archived from the original on 22 June 2008. (primary source)
  56. ↑ Andersen PC, Brodbeck BV, Oden S, Shriner A, Leite B (September 2007). "Influence of xylem fluid chemistry on planktonic growth, biofilm formation and aggregation of Xylella fastidiosa". FEMS Microbiology Letters. 274 (2): 210–7. doi: 10.1111/j.1574-6968.2007.00827.x . PMID   17610515.
  57. ↑ "Biological wastewater treatment processes; secondary treatment". Staffordshire University. Archived from the original on 18 April 2011. Retrieved 13 December 2019.
  58. ↑ Centre for Affordable Water and Sanitation Technology, Biosand Filter Manual: Design, Construction, & Installation," July 2007.
  59. ↑ "Slow Sand Filtration" (PDF). Tech Brief. 14. Morgantown, WV: National Drinking Water Clearinghouse (U.S.). June 2000. Archived from the original (PDF) on 6 April 2016.
  60. ↑ Kloepper JW (1988). "Plant Growth-Promoting Rhizobacteria on Canola (Rapeseed)". Plant Disease. 72 (1): 42. doi:10.1094/pd-72-0042. ISSN   0191-2917.
  61. 1 2 3 4 Nihorimbere V, Cawoy H, Seyer A, Brunelle A, Thonart P, Ongena M (January 2012). "Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499". FEMS Microbiology Ecology. 79 (1): 176–91. Bibcode:2012FEMME..79..176N. doi: 10.1111/j.1574-6941.2011.01208.x . PMID   22029651.
  62. ↑ Choudhary DK, Johri BN (September 2009). "Interactions of Bacillus spp. and plants—with special reference to induced systemic resistance (ISR)". Microbiological Research. 164 (5): 493–513. doi: 10.1016/j.micres.2008.08.007 . PMID   18845426.
  63. 1 2 van Loon LC (5 June 2007). "Plant responses to plant growth-promoting rhizobacteria". European Journal of Plant Pathology. 119 (3): 243–254. Bibcode:2007EJPP..119..243V. doi: 10.1007/s10658-007-9165-1 . ISSN   0929-1873.
  64. 1 2 3 4 5 Van Wees SC, Van der Ent S, Pieterse CM (August 2008). "Plant immune responses triggered by beneficial microbes". Current Opinion in Plant Biology. 11 (4): 443–8. Bibcode:2008COPB...11..443V. doi:10.1016/j.pbi.2008.05.005. hdl: 1874/30010 . PMID   18585955. S2CID   25880745.
  65. ↑ Holguin G, Bashan Y (December 1996). "Nitrogen-fixation by Azospirillum brasilense Cd is promoted when co-cultured with a mangrove rhizosphere bacterium (Staphylococcus sp.)". Soil Biology and Biochemistry. 28 (12): 1651–1660. Bibcode:1996SBiBi..28.1651H. doi:10.1016/s0038-0717(96)00251-9. ISSN   0038-0717.
  66. ↑ Babalola OO (November 2010). "Beneficial bacteria of agricultural importance". Biotechnology Letters. 32 (11): 1559–70. doi:10.1007/s10529-010-0347-0. PMID   20635120. S2CID   13518392.
  67. ↑ Bakker PA, Pieterse CM, van Loon LC (February 2007). "Induced Systemic Resistance by Fluorescent Pseudomonas spp". Phytopathology. 97 (2): 239–43. doi: 10.1094/phyto-97-2-0239 . PMID   18944381.
  68. ↑ Bent E (2006). "Induced Systemic Resistance Mediated by Plant Growth-Promoting Rhizobacteria (PGPR) and Fungi (PGPF)". Multigenic and Induced Systemic Resistance in Plants. Springer US. pp. 225–258. doi:10.1007/0-387-23266-4_10. ISBN   978-0-387-23265-2.
  69. ↑ Lynch JM, Brimecombe MJ, De Leij FA (21 August 2001), "Rhizosphere", eLS, John Wiley & Sons, Ltd, doi:10.1038/npg.els.0000403, ISBN   0-470-01617-5
  70. ↑ Randal Bollinger R, Barbas AS, Bush EL, Lin SS, Parker W (December 2007). "Biofilms in the large bowel suggest an apparent function of the human vermiform appendix". Journal of Theoretical Biology. 249 (4): 826–31. Bibcode:2007JThBi.249..826R. doi:10.1016/j.jtbi.2007.08.032. PMID   17936308.
  71. ↑ Buret AG, Motta JP, Allain T, Ferraz J, Wallace JL (January 2019). "Pathobiont release from dysbiotic gut microbiota biofilms in intestinal inflammatory diseases: a role for iron?". Journal of Biomedical Science. 26 (1): 1. doi: 10.1186/s12929-018-0495-4 . PMC   6317250 . PMID   30602371.
  72. ↑ Characklis WG, Nevimons MJ, Picologlou BF (1981). "Influence of Fouling Biofilms on Heat Transfer". Heat Transfer Engineering. 3 (1): 23–37. Bibcode:1981HTrEn...3...23C. doi:10.1080/01457638108939572. Archived from the original on 19 August 2022. Retrieved 19 December 2022.
  73. ↑ Schwermer CU, Lavik G, Abed RM, Dunsmore B, Ferdelman TG, Stoodley P, et al. (May 2008). "Impact of nitrate on the structure and function of bacterial biofilm communities in pipelines used for injection of seawater into oil fields". Applied and Environmental Microbiology. 74 (9): 2841–51. Bibcode:2008ApEnM..74.2841S. doi:10.1128/AEM.02027-07. PMC   2394879 . PMID   18344353.
  74. ↑ Chandki R, Banthia P, Banthia R (April 2011). "Biofilms: A microbial home". Journal of Indian Society of Periodontology. 15 (2): 111–4. doi: 10.4103/0972-124X.84377 . PMC   3183659 . PMID   21976832.
  75. ↑ Augustin M, Chifiriuc CB, Lazăr V, Stănescu R, Burlibașa M, Ispas DC (December 2010). "Microbial biofilms in dental medicine in reference to implanto-prostethic rehabilitation". Revista de Chirurgie Oro-maxilo-facială și Implantologie (in Romanian). 1 (1): 9–13. ISSN   2069-3850. 8. Retrieved 3 June 2012.[ permanent dead link ](webpage has a translation button)
  76. ↑ Marquis RE (September 1995). "Oxygen metabolism, oxidative stress and acid-base physiology of dental plaque biofilms". Journal of Industrial Microbiology. 15 (3): 198–207. doi: 10.1007/bf01569826 . PMID   8519478. S2CID   19959528.
  77. 1 2 3 Lemos JA, Abranches J, Burne RA (January 2005). "Responses of cariogenic streptococci to environmental stresses" (PDF). Current Issues in Molecular Biology. 7 (1): 95–107. PMID   15580782. Archived from the original (PDF) on 7 April 2014. Retrieved 3 April 2014.
  78. ↑ Tamm C, Hodes ME, Chargaff E (March 1952). "The formation apurinic acid from the desoxyribonucleic acid of calf thymus". The Journal of Biological Chemistry. 195 (1): 49–63. doi: 10.1016/S0021-9258(19)50874-2 . PMID   14938354.
  79. ↑ Freese EB (April 1961). "Transitions and transversions induced by depurinating agents". Proceedings of the National Academy of Sciences of the United States of America. 47 (4): 540–5. Bibcode:1961PNAS...47..540B. doi: 10.1073/pnas.47.4.540 . PMC   221484 . PMID   13701660.
  80. 1 2 Pennwell, "Toothbrush technology, dentifrices and dental biofilm removal." Dental Academy of CE Accessed 12 January 2022
  81. ↑ Fejerskov O (2015). Pathology of dental caries. In: Dental caries: the disease and its clinical management. Oxford (UK): Wiley Blackwell. pp. 7–9. ISBN   978-1-4051-3889-5.
  82. 1 2 Li YH, Lau PC, Lee JH, Ellen RP, Cvitkovitch DG (February 2001). "Natural genetic transformation of Streptococcus mutans growing in biofilms". J. Bacteriol. 183 (3): 897–908. doi:10.1128/JB.183.3.897-908.2001. PMC   94956 . PMID   11208787.
  83. ↑ Senadheera D, Cvitkovitch DG (2008). "Quorum Sensing and Biofilm Formation by Streptococcus mutans". Bacterial Signal Transduction: Networks and Drug Targets. Advances in Experimental Medicine and Biology. Vol. 631. pp.  178–88. doi:10.1007/978-0-387-78885-2_12. ISBN   978-0-387-78884-5. PMID   18792689.
  84. 1 2 Michod RE, Bernstein H, Nedelcu AM (May 2008). "Adaptive value of sex in microbial pathogens". Infect. Genet. Evol. 8 (3): 267–85. Bibcode:2008InfGE...8..267M. doi:10.1016/j.meegid.2008.01.002. PMID   18295550. http://www.hummingbirds.arizona.edu/Faculty/Michod/Downloads/IGE%20review%20sex.pdf Archived 11 May 2020 at the Wayback Machine
  85. ↑ Atkinson S, Goldstone RJ, Joshua GW, Chang CY, Patrick HL, Cámara M, et al. (January 2011). "Biofilm development on Caenorhabditis elegans by Yersinia is facilitated by quorum sensing-dependent repression of type III secretion". PLOS Pathogens. 7 (1): e1001250. doi: 10.1371/journal.ppat.1001250 . PMC   3017118 . PMID   21253572.
  86. ↑ Chan SY, Liu SY, Seng Z, Chua SL (September 2020). "Biofilm matrix disrupts nematode motility and predatory behavior". The ISME Journal. 15 (1): 260–269. doi:10.1038/s41396-020-00779-9. PMC   7852553 . PMID   32958848.
  87. ↑ Li S, Liu SY, Chan SY, Chua SL (May 2022). "Biofilm matrix cloaks bacterial quorum sensing chemoattractants from predator detection". The ISME Journal. 16 (5): 1388–1396. Bibcode:2022ISMEJ..16.1388L. doi:10.1038/s41396-022-01190-2. PMC   9038794 . PMID   35034106.
  88. ↑ Abee T, Kovács AT, Kuipers OP, van der Veen S (April 2011). "Biofilm formation and dispersal in Gram-positive bacteria" (PDF). Current Opinion in Biotechnology. 22 (2): 172–9. doi:10.1016/j.copbio.2010.10.016. hdl: 11370/999da2a4-d509-471b-bab5-085dac6ff681 . PMID   21109420. S2CID   22024410. Archived (PDF) from the original on 23 July 2018. Retrieved 21 December 2018.
  89. ↑ Rossi F, De Philippis R (April 2015). "Role of cyanobacterial exopolysaccharides in phototrophic biofilms and in complex microbial mats". Life. 5 (2): 1218–38. Bibcode:2015Life....5.1218R. doi: 10.3390/life5021218 . PMC   4500136 . PMID   25837843.
  90. 1 2 Danhorn T, Fuqua C (2007). "Biofilm formation by plant-associated bacteria". Annual Review of Microbiology. 61: 401–22. doi:10.1146/annurev.micro.61.080706.093316. PMID   17506679.
  91. 1 2 Joubert LM, Wolfaardt GM, Botha A (August 2006). "Microbial exopolymers link predator and prey in a model yeast biofilm system". Microb. Ecol. 52 (2): 187–97. Bibcode:2006MicEc..52..187J. doi:10.1007/s00248-006-9063-7. PMID   16897306. S2CID   20431229.
  92. 1 2 Van Colen C, Underwood GC, Serôdio J, Paterson DM (2014). "Ecology of intertidal microbial biofilms: Mechanisms, patterns and future research needs". Journal of Sea Research. 92: 2–5. Bibcode:2014JSR....92....2V. doi:10.1016/j.seares.2014.07.003.
  93. 1 2 Aslam SN, Cresswell-Maynard T, Thomas DN, Underwood GJ (December 2012). "Production and Characterization of the Intra- and Extracellular Carbohydrates and Polymeric Substances (EPS) of Three Sea-Ice Diatom Species, and Evidence for a Cryoprotective Role for EPS". J. Phycol. 48 (6): 1494–509. Bibcode:2012JPcgy..48.1494A. doi: 10.1111/jpy.12004 . PMID   27009999. S2CID   9226690.
  94. ↑ "Research on microbial biofilms (PA-03-047)". NIH, National Heart, Lung, and Blood Institute. 20 December 2002. Archived from the original on 10 December 2006. Retrieved 12 October 2006.
  95. ↑ Rogers A (2008). Molecular Oral Microbiology. Caister Academic Press. pp. 88–91. ISBN   978-1-904455-24-0.
  96. ↑ Imamura Y, Chandra J, Mukherjee PK, Lattif AA, Szczotka-Flynn LB, Pearlman E, et al. (January 2008). "Fusarium and Candida albicans biofilms on soft contact lenses: model development, influence of lens type, and susceptibility to lens care solutions". Antimicrobial Agents and Chemotherapy. 52 (1): 171–82. doi:10.1128/AAC.00387-07. PMC   2223913 . PMID   17999966.
  97. ↑ Capoor MN, Ruzicka F, Schmitz JE, James GA, Machackova T, Jancalek R, et al. (3 April 2017). "Propionibacterium acnes biofilm is present in intervertebral discs of patients undergoing microdiscectomy". PLOS ONE. 12 (4): e0174518. Bibcode:2017PLoSO..1274518C. doi: 10.1371/journal.pone.0174518 . PMC   5378350 . PMID   28369127.
  98. ↑ Lewis K (April 2001). "Riddle of biofilm resistance". Antimicrobial Agents and Chemotherapy. 45 (4): 999–1007. doi:10.1128/AAC.45.4.999-1007.2001. PMC   90417 . PMID   11257008.
  99. ↑ Parsek MR, Singh PK (2003). "Bacterial biofilms: an emerging link to disease pathogenesis". Annual Review of Microbiology. 57: 677–701. doi:10.1146/annurev.micro.57.030502.090720. PMID   14527295.
  100. 1 2 Agarwal A, Mooney M, Agarwal AG, Jayaswal D, Saakyan G, Goel V, et al. (2020). "High Prevalence of Biofilms on Retrieved Implants from Aseptic Pseudarthrosis Cases". Spine Surgery and Related Research. 5 (2): 104–108. doi: 10.22603/ssrr.2020-0147 . PMC   8026210 . PMID   33842718.
  101. 1 2 Curran N (20 November 2020). "New study first to visually capture biofilm architecture in retrieved implants from live patients". Spinal News International. Archived from the original on 23 November 2020. Retrieved 24 November 2020.
  102. ↑ "biofilm". 22 December 2020. Archived from the original on 22 January 2021. Retrieved 22 December 2020.
  103. ↑ Davis SC, Ricotti C, Cazzaniga A, Welsh E, Eaglstein WH, Mertz PM (2008). "Microscopic and physiologic evidence for biofilm-associated wound colonization in vivo". Wound Repair and Regeneration. 16 (1): 23–9. doi:10.1111/j.1524-475X.2007.00303.x. PMID   18211576. S2CID   205669081.
  104. ↑ Vyas KS, Wong LK (January 2016). "Detection of Biofilm in Wounds as an Early Indicator for Risk for Tissue Infection and Wound Chronicity". Annals of Plastic Surgery. 76 (1): 127–31. doi:10.1097/SAP.0000000000000440. PMID   25774966. S2CID   42078581.
  105. ↑ Sanclement J, Webster P, Thomas J, Ramadan H (2005). "Bacterial biofilms in surgical specimens of patients with chronic rhinosinusitis". The Laryngoscope. 115 (4): 578–82. doi:10.1097/01.mlg.0000161346.30752.18. PMID   15805862. S2CID   25830188.
  106. ↑ Sanderson AR, Leid JG, Hunsaker D (July 2006). "Bacterial biofilms on the sinus mucosa of human subjects with chronic rhinosinusitis". The Laryngoscope. 116 (7): 1121–6. doi: 10.1097/01.mlg.0000221954.05467.54 . PMID   16826045. S2CID   24785016.
  107. ↑ Leevy WM, Gammon ST, Jiang H, Johnson JR, Maxwell DJ, Jackson EN, et al. (December 2006). "Optical imaging of bacterial infection in living mice using a fluorescent near-infrared molecular probe". Journal of the American Chemical Society. 128 (51): 16476–7. doi:10.1021/ja0665592. PMC   2531239 . PMID   17177377.
  108. ↑ Kaplan JB, Izano EA, Gopal P, Karwacki MT, Kim S, Bose JL, et al. (2012). "Low levels of β-lactam antibiotics induce extracellular DNA release and biofilm formation in Staphylococcus aureus". mBio. 3 (4): e00198-12. doi:10.1128/mBio.00198-12. PMC   3419523 . PMID   22851659.
  109. ↑ Ibrahim AM (2015). The tragedy of the commons and prisoner's dilemma may improve our realization of the theory of life and provide us with advanced therapeutic ways (Report). doi:10.13140/RG.2.1.2327.9842.
  110. ↑ Ciofu O, Tolker-Nielsen T, Jensen PØ, Wang H, Høiby N (May 2015). "Antimicrobial resistance, respiratory tract infections and role of biofilms in lung infections in cystic fibrosis patients". Advanced Drug Delivery Reviews. 85: 7–23. doi:10.1016/j.addr.2014.11.017. PMID   25477303.
  111. ↑ Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (February 2002). "Extracellular DNA required for bacterial biofilm formation". Science. 295 (5559): 1487. doi:10.1126/science.295.5559.1487. PMID   11859186.
  112. ↑ Sen CK, Gordillo GM, Roy S, Kirsner R, Lambert L, Hunt TK, et al. (November 2009). "Human skin wounds: a major and snowballing threat to public health and the economy". Wound Repair and Regeneration. 17 (6): 763–771. doi:10.1111/j.1524-475X.2009.00543.x. PMC   2810192 . PMID   19903300.
  113. ↑ Singh PK, Parsek MR, Greenberg EP, Welsh MJ (May 2002). "A component of innate immunity prevents bacterial biofilm development". Nature. 417 (6888): 552–555. Bibcode:2002Natur.417..552S. doi:10.1038/417552a. PMID   12037568. S2CID   4423528.
  114. ↑ Oggioni MR, Trappetti C, Kadioglu A, Cassone M, Iannelli F, Ricci S, et al. (September 2006). "Switch from planktonic to sessile life: a major event in pneumococcal pathogenesis". Molecular Microbiology. 61 (5): 1196–210. doi:10.1111/j.1365-2958.2006.05310.x. PMC   1618759 . PMID   16925554.
  115. ↑ Wei H, Håvarstein LS (August 2012). "Fratricide is essential for efficient gene transfer between pneumococci in biofilms". Appl. Environ. Microbiol. 78 (16): 5897–905. Bibcode:2012ApEnM..78.5897W. doi:10.1128/AEM.01343-12. PMC   3406168 . PMID   22706053.
  116. ↑ Kalsy M, Tonk M, Hardt M, Dobrindt U, Zdybicka-Barabas A, Cytrynska M, et al. (2020). "The insect antimicrobial peptide cecropin A disrupts uropathogenic Escherichia coli biofilms". npj Biofilms and Microbiomes. 6 (1): 6. doi: 10.1038/s41522-020-0116-3 . PMC   7016129 . PMID   32051417.
  117. ↑ Sturbelle RT, de Avila LF, Roos TB, Borchardt JL, da Conceição R, Dellagostin OA, et al. (November 2015). "The role of quorum sensing in Escherichia coli (ETEC) virulence factors". Veterinary Microbiology. 180 (3–4): 245–252. doi:10.1016/j.vetmic.2015.08.015. PMID   26386492.
  118. ↑ Vogeleer P, Tremblay YD, Mafu AA, Jacques M, Harel J (2014). "Life on the outside: role of biofilms in environmental persistence of Shiga-toxin producing Escherichia coli". Frontiers in Microbiology. 5: 317. doi: 10.3389/fmicb.2014.00317 . PMC   4076661 . PMID   25071733.
  119. ↑ Danese PN, Pratt LA, Kolter R (June 2000). "Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture". Journal of Bacteriology. 182 (12): 3593–3596. doi:10.1128/JB.182.12.3593-3596.2000. PMC   101973 . PMID   10852895.
  120. ↑ Niranjan V, Malini A (June 2014). "Antimicrobial resistance pattern in Escherichia coli causing urinary tract infection among inpatients". The Indian Journal of Medical Research. 139 (6): 945–948. PMC   4165009 . PMID   25109731.
  121. ↑ Reisner A, Maierl M, Jörger M, Krause R, Berger D, Haid A, et al. (March 2014). "Type 1 fimbriae contribute to catheter-associated urinary tract infections caused by Escherichia coli". Journal of Bacteriology. 196 (5): 931–939. doi:10.1128/JB.00985-13. PMC   3957706 . PMID   24336940.
  122. ↑ Kobayashi SD, Malachowa N, Whitney AR, Braughton KR, Gardner DJ, Long D, et al. (September 2011). "Comparative analysis of USA300 virulence determinants in a rabbit model of skin and soft tissue infection". The Journal of Infectious Diseases. 204 (6): 937–941. doi:10.1093/infdis/jir441. PMC   3156927 . PMID   21849291.
  123. ↑ Kitur K, Parker D, Nieto P, Ahn DS, Cohen TS, Chung S, et al. (April 2015). "Toxin-induced necroptosis is a major mechanism of Staphylococcus aureus lung damage". PLOS Pathogens. 11 (4): e1004820. doi: 10.1371/journal.ppat.1004820 . PMC   4399879 . PMID   25880560.
  124. ↑ Thurlow LR, Hanke ML, Fritz T, Angle A, Aldrich A, Williams SH, et al. (June 2011). "Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo". Journal of Immunology. 186 (11): 6585–6596. doi:10.4049/jimmunol.1002794. PMC   3110737 . PMID   21525381.
  125. ↑ Craft KM, Nguyen JM, Berg LJ, Townsend SD (August 2019). "Methicillin-resistant Staphylococcus aureus (MRSA): antibiotic-resistance and the biofilm phenotype". MedChemComm. 10 (8): 1231–1241. doi:10.1039/c9md00044e. PMC   6748282 . PMID   31534648.
  126. ↑ Rice SA, Koh KS, Queck SY, Labbate M, Lam KW, Kjelleberg S (2005). "Biofilm Formation and Sloughing in Serratia marcescens Are Controlled by Quorum Sensing and Nutrient Cues". Journal of Bacteriology. 187 (10): 3477–3485. doi:10.1128/JB.187.10.3477-3485.2005. PMC   1111991 . PMID   15866935.
  127. ↑ Sethupathy S, Sathiyamoorthi E, Kim Y, Lee J, Lee J (2020). "Antibiofilm and Antivirulence Properties of Indoles Against Serratia marcescens". Frontiers in Microbiology. 11. doi: 10.3389/fmicb.2020.584812 . PMC   7662412 . PMID   33193228.
  128. ↑ Lazar V (December 2011). "Quorum sensing in biofilms—how to destroy the bacterial citadels or their cohesion/power?". Anaerobe. 17 (6): 280–5. doi:10.1016/j.anaerobe.2011.03.023. PMID   21497662.
  129. ↑ Bjarnsholt T, Jensen PØ, Moser C, Høiby N (2011). Biofilm infections. New York: Springer. ISBN   978-1-4419-6083-2. OCLC   682907381.
  130. 1 2 3 4 Bryers JD (May 2008). "Medical biofilms". Biotechnology and Bioengineering. 100 (1): 1–18. doi:10.1002/bit.21838. PMC   2706312 . PMID   18366134.
  131. ↑ Auler ME, Morreira D, Rodrigues FF, Abr Ao MS, Margarido PF, Matsumoto FE, et al. (February 2010). "Biofilm formation on intrauterine devices in patients with recurrent vulvovaginal candidiasis". Medical Mycology. 48 (1): 211–6. doi: 10.3109/13693780902856626 . PMID   20055746.
  132. ↑ Vuotto C, Longo F, Balice MP, Donelli G, Varaldo PE (September 2014). "Antibiotic Resistance Related to Biofilm Formation in Klebsiella pneumoniae". Pathogens. 3 (3): 743–758. doi: 10.3390/pathogens3030743 . PMC   4243439 . PMID   25438022.
  133. ↑ Santos-Lopez A, Marshall CW, Scribner MR, Snyder DJ, Cooper VS (September 2019). "Evolutionary pathways to antibiotic resistance are dependent upon environmental structure and bacterial lifestyle". eLife. 8: e47612. doi: 10.7554/eLife.47612 . PMC   6814407 . PMID   31516122.
  134. ↑ Pai L, Patil S, Liu S, Wen F (2023). "A growing battlefield in the war against biofilm-induced antimicrobial resistance: insights from reviews on antibiotic resistance". Front Cell Infect Microbiol. 13: 1327069. doi: 10.3389/fcimb.2023.1327069 . PMC   10770264 . PMID   38188636.
  135. 1 2 Kim YW, Subramanian S, Gerasopoulos K, Ben-Yoav H, Wu HC, Quan D, et al. (2015). "Effect of electrical energy on the efficacy of biofilm treatment using the bioelectric effect". npj Biofilms and Microbiomes. 1: 15016. doi:10.1038/npjbiofilms.2015.16. PMC   5515217 . PMID   28721233.
  136. ↑ Martins dos Santos VA, Yakimov MM, Timmis KN, Golyshin PN (2008). "Genomic Insights into Oil Biodegradation in Marine Systems". In Díaz E (ed.). Microbial Biodegradation: Genomics and Molecular Biology. Horizon Scientific Press. pp.  1971. ISBN   978-1-904455-17-2.
  137. ↑ Wang VB, Chua SL, Cai Z, Sivakumar K, Zhang Q, Kjelleberg S, et al. (March 2014). "A stable synergistic microbial consortium for simultaneous azo dye removal and bioelectricity generation". Bioresource Technology. 155: 71–76. Bibcode:2014BiTec.155...71W. doi:10.1016/j.biortech.2013.12.078. PMID   24434696.
  138. ↑ Wang VB, Chua SL, Cao B, Seviour T, Nesatyy VJ, Marsili E, et al. (2013). "Engineering PQS biosynthesis pathway for enhancement of bioelectricity production in pseudomonas aeruginosa microbial fuel cells". PLOS ONE. 8 (5): e63129. Bibcode:2013PLoSO...863129W. doi: 10.1371/journal.pone.0063129 . PMC   3659106 . PMID   23700414.
  139. ↑ Vera M, Schippers A, Sand W (September 2013). "Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation—part A". Appl. Microbiol. Biotechnol. 97 (17): 7529–41. doi:10.1007/s00253-013-4954-2. PMID   23720034. S2CID   17677624.
  140. ↑ Chan SY, Wong MW, Kwan BT, Fang JK, Chua SL (12 October 2022). "Microbial–Enzymatic Combinatorial Approach to Capture and Release Microplastics". Environmental Science & Technology Letters. 9 (11): 975–982. Bibcode:2022EnSTL...9..975C. doi:10.1021/acs.estlett.2c00558. ISSN   2328-8930. S2CID   252892619.
  141. ↑ Liu SY, Leung MM, Fang JK, Chua SL (15 January 2021). "Engineering a microbial 'trap and release' mechanism for microplastics removal". Chemical Engineering Journal. 404: 127079. Bibcode:2021ChEnJ.40427079L. doi:10.1016/j.cej.2020.127079. hdl: 10397/88307 . ISSN   1385-8947. S2CID   224972583.
  142. 1 2 3 4 5 6 7 8 9 Srey S, Jahid ID, Ha SD (June 2013). "Biofilm formation in food industries: A food safety concern". Food Control. 31 (2): 572–585. doi:10.1016/j.foodcont.2012.12.001. ISSN   0956-7135.
  143. ↑ T. Tarver, "Biofilms: A Threat to Food Safety – IFT.org", Ift.org, 2016.
  144. 1 2 3 4 Kumar CG, Anand SK (June 1998). "Significance of microbial biofilms in food industry: a review". International Journal of Food Microbiology. 42 (1–2): 9–27. doi:10.1016/s0168-1605(98)00060-9. PMID   9706794.
  145. ↑ Kwok TY, Ma Y, Chua SL (April 2022). "Biofilm dispersal induced by mechanical cutting leads to heightened foodborne pathogen dissemination". Food Microbiology. 102: 103914. doi:10.1016/j.fm.2021.103914. hdl: 10397/100037 . PMID   34809940. S2CID   244234814.
  146. 1 2 3 4 Mizan F (2015). "Microbial biofilms in seafood: A food-hygiene challenge". Food Microbiology. 49: 41–55. doi:10.1016/j.fm.2015.01.009. PMID   25846914.
  147. ↑ De Araujo LV, Abreu F, Lins U, Santa Anna LM, Nitschke M, Freire DM (January 2011). "Rhamnolipid and surfactin inhibit Listeria monocytogenes adhesion". Food Research International. 44 (1): 481–488. doi:10.1016/j.foodres.2010.09.002.
  148. ↑ Wang X, Yao X, Zhu Z, Tang T, Dai K, Sadovskaya I, et al. (July 2009). "Effect of berberine on Staphylococcus epidermidis biofilm formation". International Journal of Antimicrobial Agents. 34 (1): 60–6. doi:10.1016/j.ijantimicag.2008.10.033. PMID   19157797.
  149. ↑ Carvalho DB, Fox EG, Santos DG, Sousa JS, Freire DM, Nogueira FC, et al. (July 2019). "Fire Ant Venom Alkaloids Inhibit Biofilm Formation". Toxins. 11 (7): 420. doi: 10.3390/toxins11070420 . PMC   6669452 . PMID   31323790.
  150. ↑ Braithwaite RA, McEvoy LA (2004). "Marine biofouling on fish farms and its remediation". Advances in Marine Biology. 47: 215–252. doi:10.1016/S0065-2881(04)47003-5. ISBN   978-0-12-026148-2. PMID   15596168.
  151. ↑ Qian PY, Lau SC, Dahms HU, Dobretsov S, Harder T (2007). "Marine biofilms as mediators of colonization by marine macroorganisms: implications for antifouling and aquaculture". Marine Biotechnology. 9 (4): 399–410. Bibcode:2007MarBt...9..399Q. doi:10.1007/s10126-007-9001-9. PMID   17497196. S2CID   7614961.
  152. ↑ Cai W, De La Fuente L, Arias CR (September 2013). "Biofilm formation by the fish pathogen Flavobacterium columnare: development and parameters affecting surface attachment". Applied and Environmental Microbiology. 79 (18): 5633–42. Bibcode:2013ApEnM..79.5633C. doi:10.1128/AEM.01192-13. PMC   3754160 . PMID   23851087.
  153. ↑ King RK, Flick Jr GJ, Pierson D, Smith SA, Boardman GD, Coale Jr CW (2004). "Identification of bacterial pathogens in biofilms of recirculating aquaculture systems". Journal of Aquatic Food Product Technology. 13 (1): 125–133. Bibcode:2004JAFPT..13a.125K. doi:10.1300/j030v13n01_11. S2CID   83791439.
  154. ↑ Bourne DG, Høj L, Webster NS, Swan J, Hall MR (2006). "Biofilm development within a larval rearing tank of the tropical rock lobster, Panulirus ornatus". Aquaculture. 260 (1–4): 27–38. Bibcode:2006Aquac.260...27B. doi:10.1016/j.aquaculture.2006.06.023.
  155. ↑ Wietz M, Hall MR, Høj L (July 2009). "Effects of seawater ozonation on biofilm development in aquaculture tanks". Systematic and Applied Microbiology. 32 (4): 266–77. Bibcode:2009SyApM..32..266W. doi:10.1016/j.syapm.2009.04.001. PMID   19446976.
  156. ↑ Liu YS, Deng Y, Chen CK, Khoo BL, Chua SL (June 2022). "Rapid detection of microorganisms in a fish infection microfluidics platform". Journal of Hazardous Materials. 431: 128572. Bibcode:2022JHzM..43128572L. doi:10.1016/j.jhazmat.2022.128572. PMID   35278965. S2CID   247136872.
  157. ↑ Karunasagar I, Pai R, Malathi G (1994). "Mass mortality of Penaeus monodon larvae due to antibiotic-resistant Vibrio harveyi infection". Aquaculture. 128 (3–4): 203–209. Bibcode:1994Aquac.128..203K. doi:10.1016/0044-8486(94)90309-3.
  158. ↑ Lawrence JR, Korber DR, Hoyle BD, Costerton JW, Caldwell DE (October 1991). "Optical sectioning of microbial biofilms". Journal of Bacteriology. 173 (20): 6558–67. doi:10.1128/jb.173.20.6558-6567.1991. PMC   208993 . PMID   1917879.
  159. ↑ Cooksey K, Wigglesworth-Cooksey B (1995). "Adhesion of bacteria and diatoms to surfaces in the sea: a review". Aquatic Microbial Ecology. 9 (1): 87–96. doi: 10.3354/ame009087 .
  160. ↑ Fanning S, Mitchell AP (2012). "Fungal Biofilms". PLOS Pathog. 8 (4): e1002585. doi: 10.1371/journal.ppat.1002585 . PMC   3320593 . PMID   22496639.
  161. ↑ Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA (September 2001). "Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance". J. Bacteriol. 183 (18): 5385–94. doi:10.1128/jb.183.18.5385-5394.2001. PMC   95423 . PMID   11514524.
  162. ↑ Burmølle M, Kjøller A, Sørenses S (2012). Lear G, Gavin L, Lewis G (eds.). Microbial Biofilms: Current Research and Applications. Horizon Scientific Press. pp. 61–71. ISBN   978-1-904455-96-7.
  163. ↑ Steele DJ, Franklin DJ, Underwood GJ (September 2014). "Protection of cells from salinity stress by extracellular polymeric substances in diatom biofilms". Biofouling. 30 (8): 987–98. Bibcode:2014Biofo..30..987S. doi:10.1080/08927014.2014.960859. PMC   4706044 . PMID   25268215.
  164. ↑ Windler M, Leinweber K, Bartulos CR, Philipp B, Kroth PG (April 2015). "Biofilm and capsule formation of the diatom Achnanthidium minutissimum are affected by a bacterium". J. Phycol. 51 (2): 343–55. Bibcode:2015JPcgy..51..343W. doi:10.1111/jpy.12280. PMID   26986529. S2CID   1446573.
  165. ↑ Buhmann M, Kroth PG, Schleheck D (February 2012). "Photoautotrophic-heterotrophic biofilm communities: a laboratory incubator designed for growing axenic diatoms and bacteria in defined mixed-species biofilms". Environ Microbiol Rep. 4 (1): 133–40. Bibcode:2012EnvMR...4..133B. doi:10.1111/j.1758-2229.2011.00315.x. PMID   23757240.
  166. ↑ Thomas CM, Nielsen KM (September 2005). "Mechanisms of, and barriers to, horizontal gene transfer between bacteria". Nature Reviews. Microbiology. 3 (9): 711–721. doi:10.1038/nrmicro1234. PMID   16138099. S2CID   1231127.
  167. 1 2 3 4 5 6 7 8 9 Luo A, Wang F, Sun D, Liu X, Xin B (2022). "Formation, Development, and Cross-Species Interactions in Biofilms". Frontiers in Microbiology. 12: 757327. doi: 10.3389/fmicb.2021.757327 . PMC   8764401 . PMID   35058893.
  168. ↑ Patkowski JB, Dahlberg T, Amin H, Gahlot DK, Vijayrajratnam S, Vogel JP, et al. (April 2023). "The F-pilus biomechanical adaptability accelerates conjugative dissemination of antimicrobial resistance and biofilm formation". Nature Communications. 14 (1): 1879. doi:10.1038/s41467-023-37600-y. PMC   10076315 . PMID   37019921.
  169. ↑ Thomas VC, Hancock LE (September 2009). "Suicide and fratricide in bacterial biofilms". The International Journal of Artificial Organs. 32 (9): 537–544. doi:10.1177/039139880903200902. PMID   19851979. S2CID   201969291.
  170. 1 2 3 4 5 6 7 8 9 10 Abe K, Nomura N, Suzuki S (May 2020). "Biofilms: hot spots of horizontal gene transfer (HGT) in aquatic environments, with a focus on a new HGT mechanism". FEMS Microbiology Ecology. 96 (5). doi:10.1093/femsec/fiaa031. PMC   7189800 . PMID   32109282.
  171. ↑ Chimileski S, Franklin MJ, Papke RT (August 2014). "Biofilms formed by the archaeon Haloferax volcanii exhibit cellular differentiation and social motility, and facilitate horizontal gene transfer". BMC Biology. 12 (1): 65. doi: 10.1186/s12915-014-0065-5 . PMC   4180959 . PMID   25124934.
  172. ↑ Azeredo J, Azevedo NF, Briandet R, Cerca N, Coenye T, Costa AR, et al. (May 2017). "Critical review on biofilm methods". Critical Reviews in Microbiology. 43 (3): 313–351. doi: 10.1080/1040841X.2016.1208146 . hdl: 1822/45004 . PMID   27868469. S2CID   3991858.

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