Endospore

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An endospore stain of the cell Bacillus subtilis showing endospores as green and the vegetative cell as red Bacillus subtilis Spore.jpg
An endospore stain of the cell Bacillus subtilis showing endospores as green and the vegetative cell as red
Phase-bright endospores of Paenibacillus alvei imaged with phase-contrast microscopy Paenibacillus alvei endospore microscope image.tif
Phase-bright endospores of Paenibacillus alvei imaged with phase-contrast microscopy

An endospore is a dormant, tough, and non-reproductive structure produced by some bacteria in the phylum Bacillota. [1] [2] The name "endospore" is suggestive of a spore or seed-like form (endo means 'within'), but it is not a true spore (i.e., not an offspring). It is a stripped-down, dormant form to which the bacterium can reduce itself. Endospore formation is usually triggered by a lack of nutrients, and usually occurs in gram-positive bacteria. In endospore formation, the bacterium divides within its cell wall, and one side then engulfs the other. [3] Endospores enable bacteria to lie dormant for extended periods, even centuries. There are many reports of spores remaining viable over 10,000 years, and revival of spores millions of years old has been claimed. There is one report of viable spores of Bacillus marismortui in salt crystals approximately 25 million years old. [4] [5] When the environment becomes more favorable, the endospore can reactivate itself into a vegetative state. Most types of bacteria cannot change to the endospore form. Examples of bacterial species that can form endospores include Bacillus cereus , Bacillus anthracis , Bacillus thuringiensis , Clostridium botulinum , and Clostridium tetani . [6] Endospore formation is not found among Archaea . [7]

Contents

The endospore consists of the bacterium's DNA, ribosomes and large amounts of dipicolinic acid. Dipicolinic acid is a spore-specific chemical that appears to help in the ability for endospores to maintain dormancy. This chemical accounts for up to 10% of the spore's dry weight. [3]

Endospores can survive without nutrients. They are resistant to ultraviolet radiation, desiccation, high temperature, extreme freezing and chemical disinfectants. Thermo-resistant endospores were first hypothesized by Ferdinand Cohn after studying Bacillus subtilis growth on cheese after boiling the cheese. His notion of spores being the reproductive mechanism for the growth was a large blow to the previous suggestions of spontaneous generation. Astrophysicist Steinn Sigurdsson said "There are viable bacterial spores that have been found that are 40 million years old on Earth—and we know they're very hardened to radiation." [8] Common antibacterial agents that work by destroying vegetative cell walls do not affect endospores. Endospores are commonly found in soil and water, where they may survive for long periods of time. A variety of different microorganisms form "spores" or "cysts", but the endospores of low G+C gram-positive bacteria are by far the most resistant to harsh conditions. [3]

Some classes of bacteria can turn into exospores, also known as microbial cysts, instead of endospores. Exospores and endospores are two kinds of "hibernating" or dormant stages seen in some classes of microorganisms.

Formation of an endospore through the process of sporulation. Endospore Formation.png
Formation of an endospore through the process of sporulation.

Life cycle of bacteria

The bacterial life cycle does not necessarily include sporulation. Sporulation is usually triggered by adverse environmental conditions, so as to help the survival of the bacterium. Endospores exhibit no signs of life and can thus be described as cryptobiotic. Endospores retain viability indefinitely and they can germinate into vegetative cells under the appropriate conditions. Endospores have survived thousands of years until environmental stimuli trigger germination. They have been characterized as the most durable cells produced in nature. [9]

Structure

Variations in endospore morphology: (1, 4) central endospore; (2, 3, 5) terminal endospore; (6) lateral endospore Bakterien Sporen.png
Variations in endospore morphology: (1, 4) central endospore; (2, 3, 5) terminal endospore; (6) lateral endospore

Bacteria produce a single endospore internally. The spore is sometimes surrounded by a thin covering known as the exosporium, which overlies the spore coat. The spore coat, which acts like a sieve that excludes large toxic molecules like lysozyme, is resistant to many toxic molecules and may also contain enzymes that are involved in germination. In Bacillus subtilus endospores, the spore coat is estimated to contain more than 70 coat proteins, which are organized into an inner and an outer coat layer. [10] The X-ray diffraction pattern of purified B. subtilis endospores indicates the presence of a component with a regular periodic structure, which Kadota and Iijima speculated might be formed from a keratin-like protein. [11] However, after further studies this group concluded that the structure of the spore coat protein was different from keratin. [12] When the B. subtilis genome was sequenced, no ortholog of human keratin was detected. [13] The cortex lies beneath the spore coat and consists of peptidoglycan. The core wall lies beneath the cortex and surrounds the protoplast or core of the endospore. The core contains the spore chromosomal DNA which is encased in chromatin-like proteins known as SASPs (small acid-soluble spore proteins), that protect the spore DNA from UV radiation and heat. The core also contains normal cell structures, such as ribosomes and other enzymes, but is not metabolically active.

Up to 20% of the dry weight of the endospore consists of calcium dipicolinate within the core, which is thought to stabilize the DNA. Dipicolinic acid could be responsible for the heat resistance of the spore, and calcium may aid in resistance to heat and oxidizing agents. However, mutants resistant to heat but lacking dipicolinic acid have been isolated, suggesting other mechanisms contributing to heat resistance are also at work. [14] Small acid-soluble proteins (SASPs) are found in endospores. These proteins tightly bind and condense the DNA, and are in part responsible for resistance to UV light and DNA-damaging chemicals. [3]

Visualising endospores under light microscopy can be difficult due to the impermeability of the endospore wall to dyes and stains. While the rest of a bacterial cell may stain, the endospore is left colourless. To combat this, a special stain technique called a Moeller stain is used. That allows the endospore to show up as red, while the rest of the cell stains blue. Another staining technique for endospores is the Schaeffer-Fulton stain, which stains endospores green and bacterial bodies red. The arrangement of spore layers is as follows:

Location

The position of the endospore differs among bacterial species and is useful in identification. The main types within the cell are terminal, subterminal, and centrally placed endospores. Terminal endospores are seen at the poles of cells, whereas central endospores are more or less in the middle. Subterminal endospores are those between these two extremes, usually seen far enough towards the poles but close enough to the center so as not to be considered either terminal or central. Lateral endospores are seen occasionally.

Examples of bacteria having terminal endospores include Clostridium tetani , the pathogen that causes the disease tetanus. Bacteria having a centrally placed endospore include Bacillus cereus . Sometimes the endospore can be so large the cell can be distended around the endospore. This is typical of Clostridium tetani.

Formation and destruction

Endospore formation and cycle Sporulation.png
Endospore formation and cycle

Under conditions of starvation, especially the lack of carbon and nitrogen sources, a single endospore forms within some of the bacteria through a process called sporulation. [15]

When a bacterium detects environmental conditions are becoming unfavourable it may start the process of endosporulation, which takes about eight hours. The DNA is replicated and a membrane wall known as a spore septum begins to form between it and the rest of the cell. The plasma membrane of the cell surrounds this wall and pinches off to leave a double membrane around the DNA, and the developing structure is now known as a forespore. Calcium dipicolinate, the calcium salt of dipicolinic acid, is incorporated into the forespore during this time. The dipicolinic acid helps stabilize the proteins and DNA in the endospore. [16] : 141  Next the peptidoglycan cortex forms between the two layers and the bacterium adds a spore coat to the outside of the forespore. In the final stages of endospore formation the newly forming endospore is dehydrated and allowed to mature before being released from the mother cell. [3] The cortex is what makes the endospore so resistant to temperature. The cortex contains an inner membrane known as the core. The inner membrane that surrounds this core leads to the endospore's resistance against UV light and harsh chemicals that would normally destroy microbes. [3] Sporulation is now complete, and the mature endospore will be released when the surrounding vegetative cell is degraded.

Endospores are resistant to most agents that would normally kill the vegetative cells they formed from. Unlike persister cells, endospores are the result of a morphological differentiation process triggered by nutrient limitation (starvation) in the environment; endosporulation is initiated by quorum sensing within the "starving" population. [16] : 141 Most disinfectants such as household cleaning products, alcohols, quaternary ammonium compounds and detergents have little effect on endospores. However, sterilant alkylating agents such as ethylene oxide (ETO), and 10% bleach are effective against endospores. To kill most anthrax spores, standard household bleach (with 10% sodium hypochlorite) must be in contact with the spores for at least several minutes; a very small proportion of spores can survive longer than 10 minutes in such a solution. [17] Higher concentrations of bleach are not more effective, and can cause some types of bacteria to aggregate and thus survive.

While significantly resistant to heat and radiation, endospores can be destroyed by burning or by autoclaving at a temperature exceeding the boiling point of water, 100 °C. Endospores are able to survive at 100 °C for hours, although the larger the number of hours the fewer that will survive. An indirect way to destroy them is to place them in an environment that reactivates them to their vegetative state. They will germinate within a day or two with the right environmental conditions, and then the vegetative cells, not as hardy as endospores, can be straightforwardly destroyed. This indirect method is called Tyndallization. It was the usual method for a while in the late 19th century before the introduction of inexpensive autoclaves. Prolonged exposure to ionising radiation, such as x-rays and gamma rays, will also kill most endospores.

The endospores of certain types of (typically non-pathogenic) bacteria, such as Geobacillus stearothermophilus , are used as probes to verify that an autoclaved item has been rendered truly sterile: a small capsule containing the spores is put into the autoclave with the items; after the cycle the content of the capsule is cultured to check if anything will grow from it. If nothing will grow, then the spores were destroyed and the sterilization was successful. [18]

In hospitals, endospores on delicate invasive instruments such as endoscopes are killed by low-temperature, and non-corrosive, ethylene oxide sterilizers. Ethylene oxide is the only low-temperature sterilant to stop outbreaks on these instruments. [19] In contrast, "high level disinfection" does not kill endospores but is used for instruments such as a colonoscope that do not enter sterile bodily cavities. This latter method uses only warm water, enzymes, and detergents.

Bacterial endospores are resistant to antibiotics, most disinfectants, and physical agents such as radiation, boiling, and drying. The impermeability of the spore coat is thought to be responsible for the endospore's resistance to chemicals. The heat resistance of endospores is due to a variety of factors:

Reactivation

Reactivation of the endospore occurs when conditions are more favourable and involves activation, germination, and outgrowth. Even if an endospore is located in plentiful nutrients, it may fail to germinate unless activation has taken place. This may be triggered by heating the endospore. Germination involves the dormant endospore starting metabolic activity and thus breaking hibernation. It is commonly characterised by rupture or absorption of the spore coat, swelling of the endospore, an increase in metabolic activity, and loss of resistance to environmental stress.

Outgrowth follows germination and involves the core of the endospore manufacturing new chemical components and exiting the old spore coat to develop into a fully functional vegetative bacterial cell, which can divide to produce more cells.

Endospores possess five times more sulfur than vegetative cells. This excess sulfur is concentrated in spore coats as an amino acid, cysteine. It is believed that the macromolecule accountable for maintaining the dormant state has a protein coat rich in cystine, stabilized by S-S linkages. A reduction in these linkages has the potential to change the tertiary structure, causing the protein to unfold. This conformational change in the protein is thought to be responsible for exposing active enzymatic sites necessary for endospore germination. [20]

Endospores can stay dormant for a very long time. For instance, endospores were found in the tombs of the Egyptian pharaohs. When placed in appropriate medium, under appropriate conditions, they were able to be reactivated. In 1995, Raul Cano of California Polytechnic State University found bacterial spores in the gut of a fossilized bee trapped in amber from a tree in the Dominican Republic. The bee fossilized in amber was dated to being about 25 million years old. The spores germinated when the amber was cracked open and the material from the gut of the bee was extracted and placed in nutrient medium. After the spores were analyzed by microscopy, it was determined that the cells were very similar to Lysinibacillus sphaericus which is found in bees in the Dominican Republic today. [16]

Importance

As a simplified model for cellular differentiation, the molecular details of endospore formation have been extensively studied, specifically in the model organism Bacillus subtilis . These studies have contributed much to our understanding of the regulation of gene expression, transcription factors, and the sigma factor subunits of RNA polymerase.

Endospores of the bacterium Bacillus anthracis were used in the 2001 anthrax attacks. The powder found in contaminated postal letters consisted of anthrax endospores. This intentional distribution led to 22 known cases of anthrax (11 inhalation and 11 cutaneous). The case fatality rate among those patients with inhalation anthrax was 45% (5/11). The six other individuals with inhalation anthrax and all the individuals with cutaneous anthrax recovered. Had it not been for antibiotic therapy, many more might have been stricken. [16]

According to WHO veterinary documents, B. anthracis sporulates when it sees oxygen instead of the carbon dioxide present in mammal blood; this signals to the bacteria that it has reached the end of the animal, and an inactive dispersable morphology is useful.

Sporulation requires the presence of free oxygen. In the natural situation, this means the vegetative cycles occur within the low oxygen environment of the infected host and, within the host, the organism is exclusively in the vegetative form. Once outside the host, sporulation commences upon exposure to the air and the spore forms are essentially the exclusive phase in the environment. [21] [22]

Biotechnology

Bacillus subtilis spores are useful for the expression of recombinant proteins and in particular for the surface display of peptides and proteins as a tool for fundamental and applied research in the fields of microbiology, biotechnology and vaccination. [23]

Endospore-forming bacteria

Examples of endospore-forming bacteria include the genera:

Related Research Articles

<i>Bacillus</i> Genus of bacteria

Bacillus is a genus of Gram-positive, rod-shaped bacteria, a member of the phylum Bacillota, with 266 named species. The term is also used to describe the shape (rod) of other so-shaped bacteria; and the plural Bacilli is the name of the class of bacteria to which this genus belongs. Bacillus species can be either obligate aerobes which are dependent on oxygen, or facultative anaerobes which can survive in the absence of oxygen. Cultured Bacillus species test positive for the enzyme catalase if oxygen has been used or is present.

<span class="mw-page-title-main">Gram-positive bacteria</span> Bacteria that give a positive result in the Gram stain test

In bacteriology, gram-positive bacteria are bacteria that give a positive result in the Gram stain test, which is traditionally used to quickly classify bacteria into two broad categories according to their type of cell wall.

<i>Bacillus cereus</i> Species of bacterium

Bacillus cereus is a Gram-positive rod-shaped bacterium commonly found in soil, food, and marine sponges. The specific name, cereus, meaning "waxy" in Latin, refers to the appearance of colonies grown on blood agar. Some strains are harmful to humans and cause foodborne illness due to their spore-forming nature, while other strains can be beneficial as probiotics for animals, and even exhibit mutualism with certain plants. B. cereus bacteria may be aerobes or facultative anaerobes, and like other members of the genus Bacillus, can produce protective endospores. They have a wide range of virulence factors, including phospholipase C, cereulide, sphingomyelinase, metalloproteases, and cytotoxin K, many of which are regulated via quorum sensing. B. cereus strains exhibit flagellar motility.

Autolysins are endogenous lytic enzymes that break down the peptidoglycan components of biological cells which enables the separation of daughter cells following cell division. They are involved in cell growth, cell wall metabolism, cell division and separation, as well as peptidoglycan turnover and have similar functions to lysozymes.

<i>Clostridium</i> Genus of bacteria, which includes several human pathogens

Clostridium is a genus of anaerobic, Gram-positive bacteria. Species of Clostridium inhabit soils and the intestinal tracts of animals, including humans. This genus includes several significant human pathogens, including the causative agents of botulism and tetanus. It also formerly included an important cause of diarrhea, Clostridioides difficile, which was reclassified into the Clostridioides genus in 2016.

<i>Bacillus subtilis</i> Catalase-positive bacterium

Bacillus subtilis, known also as the hay bacillus or grass bacillus, is a gram-positive, catalase-positive bacterium, found in soil and the gastrointestinal tract of ruminants, humans and marine sponges. As a member of the genus Bacillus, B. subtilis is rod-shaped, and can form a tough, protective endospore, allowing it to tolerate extreme environmental conditions. B. subtilis has historically been classified as an obligate aerobe, though evidence exists that it is a facultative anaerobe. B. subtilis is considered the best studied Gram-positive bacterium and a model organism to study bacterial chromosome replication and cell differentiation. It is one of the bacterial champions in secreted enzyme production and used on an industrial scale by biotechnology companies.

<span class="mw-page-title-main">Lysogenic cycle</span> Process of virus reproduction

Lysogeny, or the lysogenic cycle, is one of two cycles of viral reproduction. Lysogeny is characterized by integration of the bacteriophage nucleic acid into the host bacterium's genome or formation of a circular replicon in the bacterial cytoplasm. In this condition the bacterium continues to live and reproduce normally, while the bacteriophage lies in a dormant state in the host cell. The genetic material of the bacteriophage, called a prophage, can be transmitted to daughter cells at each subsequent cell division, and later events can release it, causing proliferation of new phages via the lytic cycle.

A bacterium, despite its simplicity, contains a well-developed cell structure which is responsible for some of its unique biological structures and pathogenicity. Many structural features are unique to bacteria and are not found among archaea or eukaryotes. Because of the simplicity of bacteria relative to larger organisms and the ease with which they can be manipulated experimentally, the cell structure of bacteria has been well studied, revealing many biochemical principles that have been subsequently applied to other organisms.

<span class="mw-page-title-main">Bacteria</span> Domain of microorganisms

Bacteria are ubiquitous, mostly free-living organisms often consisting of one biological cell. They constitute a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria were among the first life forms to appear on Earth, and are present in most of its habitats. Bacteria inhabit the air, soil, water, acidic hot springs, radioactive waste, and the deep biosphere of Earth's crust. Bacteria play a vital role in many stages of the nutrient cycle by recycling nutrients and the fixation of nitrogen from the atmosphere. The nutrient cycle includes the decomposition of dead bodies; bacteria are responsible for the putrefaction stage in this process. In the biological communities surrounding hydrothermal vents and cold seeps, extremophile bacteria provide the nutrients needed to sustain life by converting dissolved compounds, such as hydrogen sulphide and methane, to energy. Bacteria also live in mutualistic, commensal and parasitic relationships with plants and animals. Most bacteria have not been characterised and there are many species that cannot be grown in the laboratory. The study of bacteria is known as bacteriology, a branch of microbiology.

Spore photoproduct lyase is a radical SAM enzyme that repairs DNA cross linking of thymine bases caused by UV-radiation. There are several types of thymine cross linking, but SPL specifically targets 5-thyminyl-5,6-dihydrothymine, which is also called spore photoproduct (SP). Spore photoproduct is the predominant type of thymine crosslinking in germinating endospores, which is why SPL is unique to organisms that produce endospores, such as Bacillus subtilis. Other types of thymine crosslinking, such as cyclobutane pyrimidine dimers (CPD) and pyrimidine (6-4) pyrimidone photoproducts (6-4PPs), are less commonly formed in endospores. These differences in DNA crosslinking are a function of differing DNA structure. Spore genomic DNA features many DNA binding proteins called small acid soluble proteins, which changes the DNA from the traditional B-form conformation to an A-form conformation. This difference in conformation is believed to be the reason why dormant spores predominantly accumulate SP in response to UV-radiation, rather than other forms of cross linking. Spores cannot repair cross-linking while dormant, instead the SPs are repaired during germination to allow the vegetative cell to function normally. When not repaired, spore photoproduct and other types of crosslinking can cause mutations by blocking transcription and replication past the point of the crosslinking. The repair mechanism utilizing spore photoproduct lyase is one of the reasons for the resilience of certain bacterial spores.

<i>Bacillus anthracis</i> Species of bacterium

Bacillus anthracis is a gram-positive and rod-shaped bacterium that causes anthrax, a deadly disease to livestock and, occasionally, to humans. It is the only permanent (obligate) pathogen within the genus Bacillus. Its infection is a type of zoonosis, as it is transmitted from animals to humans. It was discovered by a German physician Robert Koch in 1876, and became the first bacterium to be experimentally shown as a pathogen. The discovery was also the first scientific evidence for the germ theory of diseases.

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

Dipicolinic acid is a chemical compound which plays a role in the heat resistance of bacterial endospores. It is also used to prepare dipicolinato ligated lanthanide and transition metal complexes for ion chromatography.

<span class="mw-page-title-main">Sda protein domain</span>

In molecular biology, the protein domain Sda is short for suppressor of dnaA or otherwise known as sporulation inhibitor A. It is found only in bacteria. This protein domain is highly important to cell survival. When starved of nutrients, the cell is under extreme stress so undergoes a series of reactions to increase the chances of survival. One method is to form endospores which can withstand a large amount of environmental pressure. Sda protein domain is a checkpoint which prevents the formation of spores. The Sda domain affects cell signalling. It prevents the cell communicating the stress that it is under, which is crucial if the cell is to survive.

Sporulation in <i>Bacillus subtilis</i>

Bacillus subtilis is a rod-shaped, Gram-positive bacteria that is naturally found in soil and vegetation, and is known for its ability to form a small, tough, protective and metabolically dormant endospore. B. subtilis can divide symmetrically to make two daughter cells, or asymmetrically, producing a single endospore that is resistant to environmental factors such as heat, desiccation, radiation and chemical insult which can persist in the environment for long periods of time. The endospore is formed at times of nutritional stress, allowing the organism to persist in the environment until conditions become favourable. The process of endospore formation has profound morphological and physiological consequences: radical post-replicative remodelling of two progeny cells, accompanied eventually by cessation of metabolic activity in one daughter cell and death by lysis of the other.

Bacillus pumilus is a Gram-positive, aerobic, spore-forming bacillus commonly found in soil.

<span class="mw-page-title-main">Endospore staining</span> Technique used in bacteriology to identify the presence of endospores in a bacterial sample

Endospore staining is a technique used in bacteriology to identify the presence of endospores in a bacterial sample. Within bacteria, endospores are protective structures used to survive extreme conditions, including high temperatures making them highly resistant to chemicals. Endospores contain little or no ATP which indicates how dormant they can be. Endospores contain a tough outer coating made up of keratin which protects them from nucleic DNA as well as other adaptations. Endospores are able to regerminate into vegetative cells, which provides a protective nature that makes them difficult to stain using normal techniques such as simple staining and gram staining. Special techniques for endospore staining include the Schaeffer–Fulton stain and the Moeller stain.

<i>Clostridioides difficile</i> Species of bacteria

Clostridioides difficile is a bacterium known for causing serious diarrheal infections, and may also cause colon cancer. It is known also as C. difficile, or C. diff, and is a Gram-positive species of spore-forming bacteria. Clostridioides spp. are anaerobic, motile bacteria, ubiquitous in nature and especially prevalent in soil. Its vegetative cells are rod-shaped, pleomorphic, and occur in pairs or short chains. Under the microscope, they appear as long, irregular cells with a bulge at their terminal ends. Under Gram staining, C. difficile cells are Gram-positive and show optimum growth on blood agar at human body temperatures in the absence of oxygen. C. difficile is catalase- and superoxide dismutase-negative, and produces up to three types of toxins: enterotoxin A, cytotoxin B and Clostridioides difficile transferase. Under stress conditions, the bacteria produce spores that are able to tolerate extreme conditions that the active bacteria cannot tolerate.

The exosporium is the outer surface layer of mature spores. In plant spores it is also referred to as the exine. Some bacteria also produce endospores with an exosporium, of which the most commonly studied are Bacillus species, particularly Bacillus cereus and the anthrax-causing bacterium Bacillus anthracis. The exosporium is the portion of the spore that interacts with the environment or host organism, and may contain spore antigens. Exosporium proteins, such as Cot protein, are also discovered related to strains of B. anthracis and B.cereus. This Cot protein share similar sequences with other spore coat proteins, and their putative determinants are believed to include bxpC, lunA, exsA, etc.

The Bacillus Spore Morphogenesis and Germination Holin (BSH) Family is a family of proteins named after a holin in Bacillus subtilis described to be involved in spore morphogenesis and germination by Real et al (2005). The gene encoding this holin is ywcE. Mutants lacking this gene or its product have spores that exhibit outer coat defects. These spores lack the characteristic striatal pattern resulting in the failure of the outer coat to attach to the underlying inner coat. Finally, the mutant spores accumulate reduced amounts of dipicolinic acid. BSH proteins average about 90 amino acyl residues in length and exhibit 3 transmembrane segments (TMSs). A representative list of homologous proteins, found only in Bacillus species, is available in the Transporter Classification Database.

<span class="mw-page-title-main">5,6-Dihydro-5(α-thyminyl)thymine</span> Chemical compound

5,6-Dihydro-5(α-thyminyl)thymine is a DNA pyrimidine dimer photoproduct produced when DNA in bacterial spores is exposed to ultraviolet light. In bacteria, this DNA base dimer deforms the structure of DNA, so endospore forming bacteria have an enzyme called spore photoproduct lyase that repairs this damage.

References

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