Key Points
-
Genomic analyses of microbial communities can reveal the metabolic potential of uncultivated microorganisms.
-
Community genomics emphasizes the analysis of natural coexisting species populations through cultivation-independent environmental genome sequencing. The approach enables post-genomic functional assays to be carried out to understand the ecology and evolution of microbial consortia.
-
It possible to reconstruct near-complete, and possibly complete, genome sequences directly from environmental samples. However, heterogeneity in gene content and sequence identity, and genomic rearrangements in strain populations presents a fundamental challenge in reconstructing species genomes from mixed communities. Resolution of strain-level genomic heterogeneity is a fundamental goal of community genomic analysis. Comparative genome assembly that uses a sequenced strain as an assembly scaffold is a rapid and efficient method for analysis of the corresponding environmental population.
-
Comparative genomics of DNA sequences from members of strain populations can reveal the extent to which individuals are representative of their associated populations, the form of genomic heterogeneity, and the importance of processes such as lateral gene transfer and recombination in genome evolution over relatively short timescales.
-
Genomic data from communities can enable analyses of metabolic activity using gene-expression-array-based and proteomic methods. Analyses that evaluate gene expression have the potential to reveal the extent to which metabolic functions are partitioned among community members and how this changes as communities establish and develop.
-
To understand the processes of adaptation and evolution, it is important to find ways in which genome and environmental change can be placed on the same timescale.
Abstract
It is possible to reconstruct near-complete, and possibly complete, genomes of the dominant members of microbial communities from DNA that is extracted directly from the environment. Genome sequences from environmental samples capture the aggregate characteristics of the strain population from which they were derived. Comparison of the sequence data within and among natural populations can reveal the evolutionary processes that lead to genome diversification and speciation. Community genomic datasets can also enable subsequent gene expression and proteomic studies to determine how resources are invested and functions are distributed among community members. Ultimately, genomics can reveal how individual species and strains contribute to the net activity of the community.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Torsvik, V., Gokoyr, J. & Daae, F. L. High diversity in DNA of soil bacteria. Appl. Environ. Microbiol. 56, 782–787 (1990).
Ammann, R. R., Ludwig, W. & Schleifer, K. H. Phlyogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59, 143–169 (1995).
Handelsman, J. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68, 669–685 (2004).
Cowan, D. A. et al. Metagenomics, gene discovery, and the ideal biocatalyst. Biochem. Soc. Trans. 32, 298–302 (2004).
Riesenfeld, C. S., Schloss, P. D. & Handelsman, J. Metagenomics: genomic analysis of microbial communities. Annu. Rev. Genet. 38, 525–552 (2004).
Streit, W. R. & Schmitz, R. A. Metagenomics — the key to the uncultured microbes. Curr. Opin. Microbiol. 7, 492–498 (2004).
Eyers, L. et al. Environmental genomics: exploring the unmined richness of microbes to degrade xenobiotics. Appl. Microbiol. Biotechnol. 66, 123–130 (2004).
Handelsman, J. Sorting out metagenomes. Nature Biotechnol. 23, 38–39 (2005).
Tyson, G. W. et al. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37–43 (2004). This report describes the first near-complete reconstruction of uncultivated microbial genomes using shotgun sequencing of a natural microbial community.
Ram, R. J. et al. Community proteomics of a natural microbial biofilm. Science (in the press). This paper reports the first 'shotgun' proteomic investigation of a natural microbial community performed in conjunction with community genome sequence data from the same location.
Stein, J. L., Marsh, T. L., Wu, K. Y., Shizuya, H. & DeLong, E. F. Characterization of uncultivated prokaryotes: isolation and analysis of a 40-kilobase-pair genomic fragment from a planktonic marine archaeon. J. Bacteriol. 178, 591–599 (1996).
Beja, O. et al. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289, 1902–1906 (2000).
Quaiser, A. et al. First insight into the genome of an uncultivated crenarchaeote in soil. Env. Microbiol. 4, 603–611 (2002).
Liles, M. R., Manske, B. F., Bintrim, S. B., Handelsman, J. & Goodman, R. M. A census of rRNA genes and linked genomic sequences within a soil metagenomic library. Appl. Environ. Microbiol. 69, 2684–2691 (2003).
Treusch, A. H. et al. Characterization of large-insert DNA libraries from soil for environmental genomic studies of Archaea. Environ. Microbiol. 6, 970–980 (2004).
Horner-Devine, M. C., Carney, K. M. & Bohannan, B. J. M. An ecological perspective on bacterial biodiversity. Proc. Biol. Sci. 271, 113–122 (2003).
Kassen, R. The experimental evolution of specialists, generalists, and the maintenance of diversity. J. Evol. Biol. 15, 173–190 (2002).
Rosenzweig, M. L. Species Diversity in Space and Time (Cambridge University Press, Cambridge, 1995).
Shock, E. L., McCollom, T. & Schulte, M. D. Geochemical constraints on chemolithoautotrophic reactions in hydrothermal systems. Orig. Life Evol. Biosph. 25, 141–159 (1995).
Lorenz, P. & Schleper, C. Metagenome — a challenging source of enzyme discovery. J. Mol. Catalysis B: Enzymatics 19, 13–19 (2002).
Hoehler, T. M. & Alperin, M. J. in Microbial Growth on C1 Compounds (eds Lindstrom, M. E. & Tabita, F. R.) 326–333 (Kluwer Academic, Dordrecht, 1996).
Hallam, S. J. et al. Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 304, 1457–1462 (2004).
Huws, S. A., McBain, A. J. & Gilbert, P. Protozoan grazing and its impact upon population dynamics in biofilm communities. J. Appl. Microbiol. 98, 238–244 (2005).
Kiorboe, T., Tang, K., Grossart, H. P. & Ploug, H. Dynamics of microbial communities on marine snow aggregates: colonization, growth, detachment, and grazing mortality of attached bacteria. Appl. Environ. Microbiol. 69, 3036–3047 (2003).
Boenigk, J., Stadler, P., Wiedlroither, A. & Hahn, M. W. Strain-specific differences in the grazing sensitivities of closely related ultramicrobacteria affiliated with the Polynucleobacter cluster. Appl. Environ. Microbiol. 70, 5787–5793 (2004).
Thingstad, T. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 45, 1320–1328 (2000).
Wommack, K. E. & Colwell, R. R. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69–114 (2000).
Weinbauer, M. G. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28, 127–181 (2004).
Jiang, S. C. & Paul, J. H. Viral contribution to dissolved DNA in the marine environment as determined by differential centrifugation and kingdom probing. Appl. Environ. Microbiol. 61, 317–325 (1995).
Cheetham, B. & Katz, M. A role for bacteriophages in the evolution and transfer of bacterial virulence determinants. Mol. Microbiol. 18, 201–208 (1995).
Weinbauer, M. G. & Rassoulzadegan, F. Are viruses driving microbial diversification and diversity? Environ. Microbiol. 6, 1–11 (2004).
Konstantinidis, K. T. & Tiedje, J. M. Genomic insights that advance the species definition for prokaryotes. Proc. Natl Acad. Sci. USA 102, 2567–2572 (2005). This report provides a thorough comparative analysis of 70 microbial genomes that highlight the extent of genomic variability that exists within and between microbial species.
Konstantinidis, K. T. & Tiedje, J. M. Trends between gene content and genome size in prokaryotic species with larger genomes. Proc. Natl Acad. Sci. USA 101, 3160–3165 (2004).
Hughes, J. B., Hellmann, J. J., Ricketts, T. H. & Bohannan, B. J. M. Counting the uncountable: statistical approaches to estimating microbial diversity. Appl. Environ. Microbiol. 67, 4399–4406 (2001). This review describes and evaluates the utility of statistical approaches in assessing microbial diversity in natural communities.
Lander, E. S. & Waterman, M. S. Genomic mapping by fingerprinting random clones: a mathematical analysis. Genomics 2, 231–239 (1988).
Venter, J. C. et al. Environmental shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004).
Tamas, I. et al. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296, 2376–2379 (2002).
Nelson, K. E. et al. Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Res. 32, 2386–2395 (2004).
Bolotin, A. et al. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nature Biotechnol. 22, 1554–1558 (2004).
Deng, W. et al. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 184, 4601–4611 (2002).
Wu, M. et al. Phylogenomics of the reproductive parasite Wolbachia pipientis mMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2, e69 (2004).
Teeling, H., Waldmann, J., Lombardot, T., Bauer, M. & Glockner, F. O. TETRA: a web-service and stand-alone program for the analysis and comparison of tetranucleotide usage patterns in DNA sequence. BMC Bioinformatics 5, 163 (2004).
Tyson, G. W. et al. Genome-directed isolation of the key nitrogen fixer, Leptospirillum ferrodiazotrophum sp. nov., from an acidophilic microbial community. Appl. Environ. Microbiol. (in the press).
de Las Rivas, B., Marcobal, A. & Munoz, R. Allelic diversity and population structure in Oenococcus oeni as determined from sequence analysis of housekeeping genes. Appl. Environ. Microbiol. 70, 7210–7219 (2004).
Papke, R. T., Koenig, J. E., Rodriguez-Valera, F. & Doolittle, W. F. Frequent recombination in a saltern population of Halorubrum. Science 306, 1928–1929 (2004).
Vulic, M., Lenski, R. E. & Radman, M. Mutation, recombination, and incipient speciation of bacteria in the laboratory. Proc. Natl Acad. Sci. USA 96, 7348–7351 (1999).
Dennis, P., Edwards, E. A., Liss, S. N. & Fulthorpe, R. Monitoring gene expression in mixed microbial communities by using DNA microarrays. Appl. Environ. Microbiol. 69, 769–778 (2003).
Wu, L. et al. Development and evaluation of functional gene arrays for detection of selected genes in the environment. Appl. Environ. Microbiol. 67, 5780–5790 (2001).
Sebat, J. L., Colwell, F. S. & Crawford, R. L. Metagenomic profiling: microarray analysis of an environmental genomic library. Appl. Environ. Microbiol. 69, 4927–4934 (2003).
Aebersold, R. & Mann, M. Mass spectrometry-based proteomics. Nature 422, 198–207 (2003).
Schulze, W. X. et al. A proteomic fingerprint of dissolved organic carbon and of soil particles. Oecologia 142, 335–343 (2005).
Powell, M. J., Sutton, J. N., Del Castillo, C. E. & Timperman, A. T. Marine proteomics: generation of sequence tags for dissolved proteins in seawater using tandem mass spectrometry. Marine Chem. (in the press).
Habermann, B., Oegema, J., Sunyaev, S. & Shevchenko, A. The power and the limitations of cross-species protein identification by mass spectrometry-driven sequence similarity searches. Mol. Cell. Proteomics 3, 238–249 (2004).
Roberts, R. J., Karp, P., Kasif, S., Linn, S. & Buckley, M. R. An Experimental Approach to Genome Annotation. Critical Issues Colloquia Report, Washington DC, USA: American Academy of Microbiology (Jan 2005).
Curtis, T. P. & Sloan, W. T. Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology. Curr. Opin. Microbiol. 7, 221–226 (2004).
Schmeisser, C. et al. Metagenome survey of biofilms in drinking-water networks. Appl. Environ. Microbiol. 69, 7298–7309 (2003).
Tringe, S. G. et al. Comparative metagenomics of microbial communities. Science 308, 554–557 (2005).
Curtis, T. P., Sloan, W. & Scannell, J. Estimating prokaryotic diversity and its limits. Proc. Natl Acad. Sci. USA 99, 10494–10499 (2002).
Wallner, G., Fuchs, B., Spring, S., Beisker, W. & Amann, R. Flow sorting of microorganisms for molecular analysis. Appl. Enivron. Microbiol. 63, 4223–4231 (1997).
Pernthaler, A. & Amann, R. Simultaneous fluorescence in situ hybridization of mRNA and rRNA in environmental bacteria. Appl. Environ. Microbiol. 70, 5426–5433 (2004).
Zwirglmaier, K., Ludwig, W. & Schleifer, K. H. Recognition of individual genes in a single bacterial cell by fluorescence in situ hybridization — RING-FISH. Mol. Microbiol. 51, 89–96 (2004).
Lizardi P. M. et al. Mutation detection and single-molecule counting using isothermal rolling-circle amplification. Nature Genet. 19, 225–232 (1998).
Gadkar, V. & Rillig M. C. Application of Phi29 DNA polymerase mediated whole genome amplification on single spores of arbuscular mycorrhizal (AM) fungi. FEMS Microbiol. Lett. 242, 65–71 (2005).
Henke, J. M. & Bassler, B. L. Bacterial social engagements. Trends Cell Biol. 14, 648–656 (2004).
Kell, D. B. Metabolomics and systems biology: making sense of the soup. Curr. Opin. Microbiol. 7, 296–307 (2004).
Horner-Devine, M. C., Lage, M., Hughes, J. B. & Bohannan, B. J. M. A taxa–area relationship for bacteria. Nature 432, 750–753 (2004).
Jeltsch, A. Maintenance of species identity and controlling speciation of bacteria: a new function for restriction/modification systems? Gene 317, 13–16 (2003).
Nei, M. & Gojobori, T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3, 418–26 (1986).
Yang, Z. & Bielawski, J. P. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15, 496–502 (2000).
Liberles, D. A. & Wayne, M. L. Tracking adaptive evolutionary events in genomic sequences. Genome Biol. 3, 1018 (2002).
Wick, L. M., Qi, W., Lacher D. W. & Whittam, T. S. Evolution of genomic content in the stepwise emergence of Escherichia coli O157:H7. J. Bacteriol. 187, 1783–1791 (2005).
Ohnishi, M., Kurokawa, K. & Hayashi, T. Diversification of Escherichia coli genomes: are bacteriophages the major contributors? Trends Microbiol. 9, 481–485 (2001).
Scheibe, T. D., Chien, Y. J., & Radtke, J. S. Use of quantitative models to design microbial transport experiments in a sandy aquifer. Ground Water 39, 210–222 (2001).
Orphan, V. J., House, C. H., Hinrichs, K. -U., McKeegan, K. D. & DeLong, E. F. Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293, 484–487 (2001).
Radajewski, S. et al. Identification of active methylotroph populations in an acidic forest soil by stable-isotope probing. Microbiol. 148, 2331–2342 (2002).
Wellington, E. M., Berry, A. & Krsek, M. Resolving functional diversity in relation to microbial community structure in soil: exploiting genomics and stable isotope probing. Curr. Opin. Microbiol. 6, 295–301 (2003).
Ouverney, C. C. & Fuhrman, J. A. Combined microautoradiography-16S rRNA probe technique for determination of radioisotope uptake by specific microbial cell types in situ. Appl. Environ. Microbiol. 65, 1746–1752 (1999).
Druschel, G. K., Baker, B. J., Gihring, T. H. & Banfield, J. F. Acid mine drainage biogeochemistry at Iron Mountain, California. Geochem. Trans. 5, 13–32 (2004).
Baker, B. J. & Banfield, J. F. Microbial communities in acid mine drainage. FEMS Microbiol. Ecol. 44, 139–152 (2003).
Bond, P. L., Dreuschel, G. K. & Banfield, J. F. Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems. Appl. Environ. Microbiol. 66, 4962–4971 (2000).
Miller, D. N., Bryant, J. E., Madsen, E. L. & Ghiorse, W. C. Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl. Environ. Microbiol. 65, 4715–4724 (1999).
DeLong, E. F. Microbial population genomics and ecology. Curr. Opin. Microbiol. 5, 520–524 (2002).
Rondon, M. R., et al. Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl. Environ. Microbiol. 66, 2514–2547 (2000).
Acknowledgements
We thank G. W. Tyson and anonymous reviewers for helpful comments. Support for our work from the Department of Energy Microbial Genome Program, National Science Foundation (NSF) Biocomplexity Program, NASA Astrobiology Institute, and the NSF Postdoctoral Research Fellowship Program in Microbial Biology (E.E.A.) is gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Related links
Glossary
- CLONE LIBRARY
-
A collection of targeted DNA sequences, such as the 16S rRNA gene, most often derived from PCR amplification and subsequent cloning into a vector. Specifically, 16S rRNA gene clone libraries are often used in surveys of microbial diversity from environmental samples.
- CONSORTIUM
-
Physical association between cells of two or more types of microorganism. Such an association might be advantageous to at least one of the microorganisms.
- COVERAGE
-
The average number of times a nucleotide is represented by a high-quality base in the sequence data; full genome coverage is usually attained at 8–10X coverage.
- ABIOTIC
-
The non-living physical and chemical attributes of a system, which include pH, temperature, pressure, osmotic strength, and chemical composition.
- SYNTENY
-
Refers to the presence of two or more genes on the same chromosome. However, the term is often used to refer to the shared colinearity in orthologous gene content and gene order between genomes.
- SCAFFOLD
-
A genome fragment constructed by the ordering and orienting of sets of unlinked contigs generated from raw shotgun sequence data by using additional information (such as paired-end sequence information or homology data) to determine proper contig linkage and placement along the chromosome. Scaffolds can be comprised of multiple contigs.
- PANMICTIC
-
Characterized by a lack of restriction in genetic exchange within the population; all individuals within the species population are potential recombination partners.
Rights and permissions
About this article
Cite this article
Allen, E., Banfield, J. Community genomics in microbial ecology and evolution. Nat Rev Microbiol 3, 489–498 (2005). https://doi.org/10.1038/nrmicro1157
Issue Date:
DOI: https://doi.org/10.1038/nrmicro1157