Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Opinion
  • Published:

The ecological coherence of high bacterial taxonomic ranks

Abstract

The species is a fundamental unit of biological organization, but its relevance for Bacteria and Archaea is still hotly debated. Even more controversial is whether the deeper branches of the ribosomal RNA-derived phylogenetic tree, such as the phyla, have ecological importance. Here, we discuss the ecological coherence of high bacterial taxa in the light of genome analyses and present examples of niche differentiation between deeply diverging groups in terrestrial and aquatic systems. The ecological relevance of high bacterial taxa has implications for bacterial taxonomy, evolution and ecology.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Habitat–phylotype associations for the Alphaproteobacteria.
Figure 2: Niche differentiation at the phylum and class levels.
Figure 3: Microbial succession at the order level in the human small-bowel lumen.
Figure 4: Habitat–phylotype associations.

Similar content being viewed by others

References

  1. Achtman, M. & Wagner, M. Microbial diversity and the genetic nature of microbial species. Nature Rev. Microbiol. 6, 431–440 (2008).

    Article  CAS  Google Scholar 

  2. Gans, J., Wolinsky, M. & Dunbar, J. Computational improvements reveal great microbial diversity and high metal toxicity in soil. Science 309, 1387–1390 (2005).

    Article  CAS  PubMed  Google Scholar 

  3. Byappanahalli, M. N., Whitman, R. L., Shively, D. A., Sadowsky, M. J. & Ishii, S. Population structure, persistence, and seasonality of autochthonous Escherichia coli in temperate, coastal forest soil from a Great Lakes watershed. Environ. Microbiol. 8, 504–513 (2006).

    Article  CAS  PubMed  Google Scholar 

  4. Ishii, S., Ksoll, W. B., Hicks, R. E. & Sadowsky, M. J. Presence and growth of naturalized Escherichia coli in temperate soils from Lake Superior watersheds. Appl. Environ. Microbiol. 72, 612–621 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Gevers, D. et al. Re-evaluating prokaryotic species. Nature Rev. Microbiol. 3, 733–739 (2005).

    Article  CAS  Google Scholar 

  6. Prosser, J. I. et al. The role of ecological theory in microbial ecology. Nature Rev. Microbiol. 5, 384–392 (2007).

    Article  CAS  Google Scholar 

  7. Fraser, C., Alm, E. J., Polz, M. F., Spratt, B. G. & Hanage, W. P. The bacterial species challenge: making sense of genetic and ecological diversity. Science 323, 741–746 (2009).

    Article  CAS  PubMed  Google Scholar 

  8. Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: proposal for the domain Archaea, Bacteria and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Doolittle, W. F. The practice of classification and the theory of evolution, and what the demise of Charles Darwin's tree of life hypothesis mean for both of them. Phil. Trans. R. Soc. Lond. B 364, 2221–2228 (2009).

    Article  Google Scholar 

  10. Guidot, A. et al. Genetic structure and phylogeny of the plant pathogen Ralstonia solanacearum inferred from gene distribution analysis. J. Bacteriol. 189, 377–387 (2007).

    Article  CAS  PubMed  Google Scholar 

  11. Aparicio, S. et al. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297, 1301–1310 (2002).

    Article  CAS  PubMed  Google Scholar 

  12. Johnson, Z. I. et al. Niche partioning among Procholoroccus ecotypes along ocean-scale environmental gradients. Science 311, 1737–1740 (2006).

    Article  CAS  PubMed  Google Scholar 

  13. Hunt, D. E. et al. Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320, 1081–1085 (2008).

    Article  CAS  PubMed  Google Scholar 

  14. Brown, J. R. & Doolittle, W. F. Archaea and the prokaryote-to-eukaryote transition. Microbiol. Mol. Biol. Rev. 61, 456–502 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Doolittle, W. F. Phylogenetic classification and the universal tree. Science 284, 2124–2128 (1999).

    Article  CAS  PubMed  Google Scholar 

  16. Gogarten, J. P., Doolittle, W. F. & Lawrence, J. G. Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol. 19, 2226–2238 (2002).

    Article  CAS  PubMed  Google Scholar 

  17. Kurland, C. G., Canback, B. & Berg, O. G. Horizontal gene transfer: a critical view. Proc. Natl Acad. Sci. USA 19, 9658–9662 (2003).

    Article  Google Scholar 

  18. Fierer, N., Bradford, M. A. & Jackson, R. B. Toward an ecological classification of soil bacteria. Ecology 88, 1354–1364 (2007).

    Article  PubMed  Google Scholar 

  19. Philippot, L. et al. Spatial patterns of bacterial taxa in nature reflect ecological traits of deep branches of the 16S rRNA bacterial tree. Environ. Microbiol. 11, 1518–1526 (2009).

    Article  PubMed  Google Scholar 

  20. Wu, D. et al. A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462, 1056–1060 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Eisen, J. A. & Fraser, C. M. Phylogenomics: Intersection of evolution and genomics. Science 300, 1706–1707 (2003).

    Article  CAS  PubMed  Google Scholar 

  22. Sicheritz-Ponten, T. & Andersson, S. G. E. A phylogenomic approach to microbial evolution. Nucleic Acids Res. 29, 545–552 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Snel, B., Bork, P. & Huynen, M. A. Genome phylogeny based on gene content. Nature Genet. 21, 108–110 (1999).

    Article  CAS  PubMed  Google Scholar 

  24. Dutilh, B. E., Snel, B., Ettema, T. J. G. & Huynen, M. A. Signature genes as a phylogenomic tool. Mol. Biol. Evol. 25, 1659–1667 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Mulkidjanian, A. Y. et al. The cyanobacterial genome core and the origin of photosynthesis. Proc. Natl Acad. Sci. USA 103, 13126–13131 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Gao, B., Paramanathan, R. & Gupta, R. S. Signature proteins that are distinctive characteristics of Actinobacteria and their subgroups. Antonie Van Leeuwenhoek 90, 69–91 (2006).

    Article  CAS  PubMed  Google Scholar 

  27. Gupta, R. & Lorenzini, E. Phylogeny and molecular signatures (conserved proteins and indels) that are specific for the Bacteroidetes and Chlorobi species. BMC Evol. Biol. 7, 71 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Koonin, E. G. & Wolf, Y. I. Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res. 36, 6688–6719 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ettema, J. G. & Andersson, S. G. E. The α-proteobacteria: the Darwin finches of the bacterial world. Biol. Lett. 5, 429–432 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Boussau, B., Karlberg, E. O., Frank, A. C., Legault, B. A. & Andersson, S. G. E. Computational inference of scenarios for α-proteobacterial genome evolution. Proc. Natl Acad. Sci. USA 101, 9722–9727 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Williams, K. P., Sobral, B. W. & Dickerman, A. W. A robust species tree for the Alphaproteobacteria. J. Bacteriol. 189, 4578–4586 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Smit, E. et al. Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl. Environ. Microbiol. 67, 2284–2291 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Cruz-Martinez, K. et al. Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland. ISME J. 3, 738–744 (2009).

    Article  CAS  PubMed  Google Scholar 

  34. Thomson, B. C. et al. Vegetation affects the relative abundances of dominant soil bacterial taxa and soil respiration rates in an upland grassland soil. Microb. Ecol. 59, 335–343 (2009).

    Article  PubMed  Google Scholar 

  35. Lauber, C. L., Hamady, M., Knight, R. & Fierer, N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 75, 5111–5120 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Wallenstein, M. D., McMahon, S. & Schimel, J. Bacterial and fungal community structure in Arctic tundra tussock and shrub soils. FEMS Microbiol. Ecol. 59, 428–435 (2007).

    Article  CAS  PubMed  Google Scholar 

  37. Jones, R. T. et al. A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J. 3, 442–453 (2009).

    Article  CAS  PubMed  Google Scholar 

  38. Männistö, M. K., Tiirola, M. & Häggblom, M. Bacterial communities in Arctic fjelds of Finnish Lapland are stable but highly pH-dependent. FEMS Microbiol. Ecol. 59, 452–465 (2007).

    Article  PubMed  Google Scholar 

  39. Hartman, W. H., Richardson, C. J., Vilgalys, R. & Bruland, G. L. Environmental and anthropogenic controls over bacterial communities in wetland soils. Proc. Natl Acad. Sci. USA 105, 17842–17847 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ward, N. L. et al. Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl. Environ. Microbiol. 75, 2046–2056 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Morris, R. M. et al. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420, 806–810 (2002).

    Article  CAS  PubMed  Google Scholar 

  42. Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol. 5, e77 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Danon, M., Franke-Whittle, I. H., Insam, H., Chen, Y. & Hadar, Y. Molecular analysis of bacterial community succession during prolonged compost curing. FEMS Microbiol. Ecol. 65, 133–144 (2008).

    Article  CAS  PubMed  Google Scholar 

  44. Fulthorpe, R. R., Roesch, L. F. W., Riva, A. & Triplett, E. W. Distantly sampled soils carry few species in common. ISME J. 2, 901–910 (2008).

    Article  CAS  PubMed  Google Scholar 

  45. Hackl, E., Zechmeister-Boltenstern, S., Bodrossy, L. & Sessitsch, A. Comparison of diversities and compositions of bacterial populations inhabiting natural forest soils. Appl. Environ. Microbiol. 70, 5057–5065 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Pointing, S. B. et al. Highly specialized microbial diversity in hyper-arid polar desert. Proc. Natl Acad. Sci. USA 106, 19964–19969 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Buckley, D. H. & Schmidt, T. M. The structure of microbial communities in soil and the lasting impact of cultivation. Microb. Ecol. 42, 11–21 (2001).

    CAS  PubMed  Google Scholar 

  48. Nemergut, D. R. et al. The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environ. Microbiol. 10, 3093–3105 (2008).

    Article  CAS  PubMed  Google Scholar 

  49. Jangid, K. et al. Relative impacts of land-use, management intensity and fertilization upon soil microbial community structure in agricultural systems. Soil Biol. Biochem. 40, 2843–2853 (2008).

    Article  CAS  Google Scholar 

  50. Mou, X. Z., Sun, S. L., Edwards, R. A., Hodson, R. E. & Moran, M. A. Bacterial carbon processing by generalist species in the coastal ocean. Nature 451, 708–711 (2008).

    Article  CAS  PubMed  Google Scholar 

  51. Goffredi, S. K. & Orphan, V. J. Bacterial community shifts in taxa and diversity in response to localized organic loading in the deep sea. Environ. Microbiol. 12, 344–363 (2010).

    Article  CAS  PubMed  Google Scholar 

  52. Mering, C.v. et al. Quantitative phylogenetic assessment of microbial communities in diverse environments. Science 315, 1126–1130 (2007).

    Article  Google Scholar 

  53. Glockner, F. O., Fuchs, B. M. & Amann, R. Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl. Environ. Microbiol. 65, 3721–3726 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Zwart, G., Crump, B. C., Agterveld, M., Hagen, F. & Han, S. K. Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat. Microb. Ecol. 28, 141–155 (2002).

    Article  Google Scholar 

  55. Bouvier, T. C. & del Giorgio, P. A. Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol. Oceanogr. 47, 453–470 (2002).

    Article  CAS  Google Scholar 

  56. Steger, K., Jarvis, A., Vasara, T., Romantschuk, M. & Sundh, I. Effects of differing temperature management on development of Actinobacteria populations during composting. Res. Microbiol. 158, 617–624 (2007).

    Article  CAS  PubMed  Google Scholar 

  57. Hartman, A. L. et al. Human gut microbiome adopts an alternative state following small bowel transplantation. Proc. Natl Acad. Sci. USA 106, 17187–17192 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Gilbert, J. A. et al. The seasonal structure of microbial communities in the Western English Channel. Environ. Microbiol. 11, 3132–3139 (2009).

    Article  CAS  PubMed  Google Scholar 

  59. Chauhan, A., Cherrier, J. & Williams, H. N. Impact of sideways and bottom-up control factors on bacterial community succession over a tidal cycle. Proc. Natl Acad. Sci. USA 106, 4301–4306 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Vogel, T. M. et al. TerraGenome: a consortium for the sequencing of a soil metagenome. Nature Rev. Microbiol. 7, 252 (2009).

    Article  CAS  Google Scholar 

  61. Cohan, F. M. & Perry, E. B. A systematics for discovering the fundamental units of bacterial diversity. Curr. Microbiol. 17, R373–R386 (2007).

    CAS  Google Scholar 

  62. Konstantinidis, K. T. & Tiedje, J. M. Genomic insights that advance the species definition for prokaryotes. Proc. Natl Acad. Sci. USA 102, 2567–2572 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Ward, D. M. et al. Genomics, environmental genomics and the issue of microbial species. Heredity 100, 207–219 (2008).

    Article  CAS  PubMed  Google Scholar 

  64. Cohan, F. M. & Koeppel, A. F. The origins of ecological diversity in prokaryotes. Curr. Biol. 18, R1024–R1034 (2008).

    Article  CAS  PubMed  Google Scholar 

  65. Baldauf, S. L. The tree of life is a tree (more or less). Trends Ecol. Evol. 17, 450–451 (2002).

    Article  Google Scholar 

  66. Valentine, J. W. On the Origin of Phyla (University of Chicago Press, Chicago, 2004).

    Google Scholar 

  67. Mayr, E. This is Biology: the Science of the Living World (Harvard University Press, Cambridge, USA, 1997).

    Google Scholar 

  68. Trosvik, P., Stenseth, N. C. & Rudi, K. Convergent temporal dynamics of the human infant gut microbiota. ISME J. 3, 151–158 (2009).

    Google Scholar 

  69. Loreau, M. et al. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804–808 (2001).

    Article  CAS  PubMed  Google Scholar 

  70. Ley, R. E., Turnbaugh, P. J., Klein, S. & Gordon, J. I. Microbial ecology: Human gut microbes associated with obesity. Nature 444, 1022–1023 (2006).

    CAS  PubMed  Google Scholar 

  71. Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031 (2006).

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

L.P. gratefully acknowledges the Environment and Agronomy research division and the International Relations Department of the Institut National de la Recherche Agronomique, France, and the Department of Microbiology of the Swedish University of Agricultural Sciences in Uppsala for supporting and hosting his sabbatical in Sweden. T.J.B. was supported by the Lake Ecosystems Response to Environmental Change (LEREC) programme (which is funded by the Swedish Research Council Formas) while at the University of Uppsala. S.H. is supported by the Swedish Research Council and the Swedish Research Council Formas, which finance the Uppsala Monitoring Centre, and S.G.E.A. is supported by the Swedish Research Council, the Göran Gustafsson Foundation, the Swedish Foundation for Strategic Research and the Knut and Alice Wallenberg Foundation. J.P. acknowledges support from the Royal Society of Edinburgh, and W.B.W. from the US Department of Agriculture and the US National Science Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laurent Philippot.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

DATABASES

Entrez Genome Project

Escherichia coli

Ralstonia solanacearum

Takifugu rubripes

FURTHER INFORMATION

Laurent Philippot's homepage

GEBA

NCBI Microbial Genomes

Genomes OnLine

JCVI Comprehensive Microbial Resource

Glossary

Biogeography

The distribution of organisms over space and time, including where they live, at what abundance, and why; these data offer insights into the mechanisms that generate and maintain diversity.

Clade

A phylogenetically coherent bacterial group.

Deep sequencing

High-throughput sequencing designed to maximize the amount of sequence information that can be gained from an environmental sample, the ultimate aim being exhaustive sequencing.

High taxonomic level

A taxonomic level from genus to phylum.

Horizontal gene transfer

The acquisition of a new DNA fragment from another organism.

Ileostomy

A surgical opening between the abdominal wall and the ileum (small intestine).

Lineage

A group of taxa that are related by descent from a common ancestor.

Niche

The particular set of resources and environmental conditions that an individual species exploits.

Phylogeny

The inferred evolutionary relationships among a group of organisms (most often inferred on the basis of molecular data).

Phylotype

A taxon-neutral term referring to an organism with a unique genetic make-up according to its evolutionary relationship to other organisms.

Species

A generally accepted species definition has yet to be established for microorganisms. For the purposes of taxonomy, an ad hoc definition on the basis of DNA hybridization is widely used. This definition is based on degrees of relatedness, without an underlying biological principle.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Philippot, L., Andersson, S., Battin, T. et al. The ecological coherence of high bacterial taxonomic ranks. Nat Rev Microbiol 8, 523–529 (2010). https://doi.org/10.1038/nrmicro2367

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro2367

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing