Article | Published:

Community structure and metabolism through reconstruction of microbial genomes from the environment

Nature volume 428, pages 3743 (04 March 2004) | Download Citation

Subjects

Abstract

Microbial communities are vital in the functioning of all ecosystems; however, most microorganisms are uncultivated, and their roles in natural systems are unclear. Here, using random shotgun sequencing of DNA from a natural acidophilic biofilm, we report reconstruction of near-complete genomes of Leptospirillum group II and Ferroplasma type II, and partial recovery of three other genomes. This was possible because the biofilm was dominated by a small number of species populations and the frequency of genomic rearrangements and gene insertions or deletions was relatively low. Because each sequence read came from a different individual, we could determine that single-nucleotide polymorphisms are the predominant form of heterogeneity at the strain level. The Leptospirillum group II genome had remarkably few nucleotide polymorphisms, despite the existence of low-abundance variants. The Ferroplasma type II genome seems to be a composite from three ancestral strains that have undergone homologous recombination to form a large population of mosaic genomes. Analysis of the gene complement for each organism revealed the pathways for carbon and nitrogen fixation and energy generation, and provided insights into survival strategies in an extreme environment.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    Bacterial evolution. Microbiol. Rev. 51, 221–271 (1987)

  2. 2.

    & Comparative genomics of archaea: how much have we learned in six years, and what's next? Genome Biol. 4, 115.1–115.16 (2003)

  3. 3.

    & Complete genome sequences of cellular life forms: glimpses of theoretical evolutionary genomics. Curr. Opin. Genet. Dev. 6, 757–762 (1996)

  4. 4.

    , & Phylogenetic identification and in-situ detection of individual microbial-cells without cultivation. Microbiol. Rev. 59, 143–169 (1995)

  5. 5.

    A molecular view of microbial diversity and the biosphere. Science 276, 734–740 (1997)

  6. 6.

    Exploring prokaryotic diversity in the genomic era. Genome Biol. 3, reviews0003.1–0003.8. (2002)

  7. 7.

    et al. Construction and analysis of bacterial artificial chromosome libraries from a marine microbial assemblage. Environ. Microbiol. 2, 516–529 (2000)

  8. 8.

    et al. Comparative genomic analysis of archaeal genotypic variants in a single population and in two different oceanic provinces. Appl. Environ. Microbiol. 68, 335–345 (2002)

  9. 9.

    et al. Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl. Environ. Microbiol. 66, 2541–2547 (2000)

  10. 10.

    , & Prokaryotic diversity—magnitude, dynamics, and controlling factors. Science 296, 1064–1066 (2002)

  11. 11.

    & Acidic mine drainage rate-determining step. Science 167, 1121–1127 (1970)

  12. 12.

    , & Seasonal variations in microbial populations and environmental conditions in an extreme acid mine drainage environment. Appl. Environ. Microbiol. 65, 3627–3632 (1999)

  13. 13.

    , & Phylogeny of microorganisms populating a thick, subaerial, predominantly lithotrophic biofilm at an extreme acid mine drainage site. Appl. Environ. Microbiol. 66, 3842–3849 (2000)

  14. 14.

    , & Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems. Appl. Environ. Microbiol. 66, 4962–4971 (2000)

  15. 15.

    & Microbial communities in acid mine drainage. FEMS Microbiol. Ecol. 44, 139–152 (2003)

  16. 16.

    et al. Geochemical and biological aspects of sulfide mineral dissolution: lessons from Iron Mountain, California. Chem. Geol. 169, 383–397 (2000)

  17. 17.

    & Microbial formation and degradation of minerals. Adv. Appl. Microbiol. 6, 153–206 (1964)

  18. 18.

    & Design and performance of rRNA targeted oligonucleotide probes for in situ detection and phylogenetic identification of microorganisms inhabiting acid mine drainage environments. Microb. Ecol. 41, 149–161 (2001)

  19. 19.

    & Molecular relationship between two groups of the genus Leptospirillum and the finding that Leptospirillum ferriphilum sp nov dominates South African commercial biooxidation tanks that operate at 40 °C. Appl. Environ. Microbiol. 68, 838–845 (2002)

  20. 20.

    , , , & The value of complete microbial genome sequencing (you get what you pay for). J. Bacteriol. 184, 6403–6405 (2002)

  21. 21.

    & On the high value of low standards. J. Bacteriol. 184, 6406–6409 (2002)

  22. 22.

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

  23. 23.

    , , , & Genomic organization analysis of acidophilic chemolithotropic bacteria using pulse field gel electrophoretic techniques. Biochimie 80, 911–921 (1998)

  24. 24.

    et al. Capturing whole-genome characteristics in short sequences using a naive Bayesian classifier. Genome Res. 11, 1404–1409 (2001)

  25. 25.

    et al. Informatics for unveiling hidden genome signatures. Genome Res. 13, 693–702 (2003)

  26. 26.

    , & The relative contributions of recombination and point mutation to the diversification of bacterial clones. Curr. Opin. Microbiol. 4, 602–606 (2001)

  27. 27.

    , , & Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in enterobacteria. Proc. Natl Acad. Sci. USA 94, 9763–9767 (1997)

  28. 28.

    & Explaining the excess of rare species in natural species abundance distributions. Nature 422, 714–716 (2003)

  29. 29.

    A test of the unified neutral theory of biodiversity. Nature 422, 881–885 (2003)

  30. 30.

    A dynamical model of communities and a new species-abundance distribution. Biol. Bull. 198, 152–165 (2000)

  31. 31.

    et al. The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum. Nature 407, 508–513 (2000)

  32. 32.

    & Gene function analysis in environmental isolates: The nif regulon of the strict iron oxidizing bacterium Leptospirillum ferrooxidans. Proc. Natl Acad. Sci. USA 100, 7883–7888 (2003)

  33. 33.

    , , & Respiratory components in acidophilic bacteria that respire on iron. Geomicrobiol. J. 10, 173–192 (1992)

  34. 34.

    & Respiratory enzymes of Thiobacillus ferrooxidans—kinetic-properties of an acid-stable irron-rusticyanin oxidoreductase. Biochemistry 33, 9220–9228 (1994)

  35. 35.

    & Molecular aspects of the electron transfer system which participates in the oxidation of ferrous ion by Thiobacillus ferrooxidans. FEMS Microbiol. Rev. 17, 401–413 (1995)

  36. 36.

    , , & Characterization of an operon encoding two c-type cytochromes, an aa(3)-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020. Appl. Environ. Microbiol. 65, 4781–4787 (1999)

  37. 37.

    , & The Bradyrhizobium japonicum fixGHIS genes are required for the formation of the high-affinity cbb(3)-type cytochrome oxidase. Arch. Microbiol. 165, 297–305 (1996)

  38. 38.

    , & Cytochrome cbb(3) oxidase and bacterial microaerobic metabolism. Biochem. Soc. Trans. 30, 653–658 (2002)

  39. 39.

    & Respiratory protection of nitrogenase activity in Azotobacter vinelandii—roles of the terminal oxidases. Biosci. Rep. 17, 303–317 (1997)

  40. 40.

    , & The archaeal respiratory supercomplex SoxM from S. acidocaldarius combines features of quinole and cytochrome c oxidases. Biol. Chem. 383, 1791–1799 (2002)

  41. 41.

    , , , & Chemotaxis of Leptospirillum ferrooxidans and other acidophilic chemolithotrophs—comparison with the Escherichia coli chemosensory system. FEMS Microbiol. Lett. 96, 37–42 (1992)

  42. 42.

    et al. Tetraether-linked membrane monolayers in Ferroplasma spp.: a key to survival in acid. Extremophiles (submitted)

Download references

Acknowledgements

This research was funded by the US Department of Energy Microbial Genomics Program and the National Science Foundation Biocomplexity Program. We would like to thank M. Power, W. Getz, R. Blake, J. Handlesman, B. Baker, I. Lo, J. Flanagan, D. Dodds and R. Carver for their contributions to this work. We also thank C. Detter and members of his laboratory at JGI for help with library construction, and T. Arman (Iron Mountain Mines) and R. Sugarek (EPA) for access to the Richmond mine.

Author information

Affiliations

  1. Department of Environmental Science, Policy and Management, University of California, Berkeley, California 94720, USA

    • Gene W. Tyson
    • , Philip Hugenholtz
    • , Eric E. Allen
    • , Rachna J. Ram
    •  & Jillian F. Banfield
  2. Department of Earth and Planetary Sciences, University of California, Berkeley, California 94720, USA

    • Jillian F. Banfield
  3. Department of Physics, University of California, Berkeley, California 94720, USA

    • Jarrod Chapman
    •  & Daniel S. Rokhsar
  4. Joint Genome Institute, Walnut Creek, California 94598, USA

    • Jarrod Chapman
    • , Paul M. Richardson
    • , Victor V. Solovyev
    • , Edward M. Rubin
    •  & Daniel S. Rokhsar

Authors

  1. Search for Gene W. Tyson in:

  2. Search for Jarrod Chapman in:

  3. Search for Philip Hugenholtz in:

  4. Search for Eric E. Allen in:

  5. Search for Rachna J. Ram in:

  6. Search for Paul M. Richardson in:

  7. Search for Victor V. Solovyev in:

  8. Search for Edward M. Rubin in:

  9. Search for Daniel S. Rokhsar in:

  10. Search for Jillian F. Banfield in:

Competing interests

The authors declare that they have no competing financial interests.

Corresponding author

Correspondence to Jillian F. Banfield.

Supplementary information

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature02340

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.