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Identifying microorganisms responsible for ecologically significant biogeochemical processes

Abstract

Throughout evolutionary time, and each day in every habitat throughout the globe, microorganisms have been responsible for maintaining the biosphere. Despite the crucial part that they play in the cycling of nutrients in habitats such as soils, sediments and waters, only rarely have the microorganisms actually responsible for key processes been identified. Obstacles that have traditionally impeded fundamental microbial ecology inquiries are now yielding to technical advancements that have important parallels in medical microbiology. The pace of new discoveries that document ecological processes and their causative agents will no doubt accelerate in the near future, and might assist in ecosystem management.

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Figure 1: Conceptual representation of the interactions between environmental science and microbial ecology.
Figure 2: Model for the generation and interpretation of environmental microbiological information, with emphasis on field relevance and ecological validation of data.

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References

  1. Beijerinck, M. W. Anhäufungsversuche mit Urembakteriën. Centralblatt f. Bakteriologie Part II, 7, 33–61 (1888). English translation in Milestones in Microbiology (ed. T. D. Brock) 234–237 (Prentice Hall Inc., New Jersey, 1961).

    Google Scholar 

  2. Winogradsky, S. Recherches physiologiques sur les sulfobactéries. Ann. Inst. Pasteur (Paris) 3, 49–60 (1889). English translation in Milestones in Microbiology (ed. T. D. Brock) 227–231 (Prentice Hall Inc., New Jersey, 1961).

    Google Scholar 

  3. Stumm, W. & Morgan, J. J. Aquatic Chemistry 3rd edn (Wiley and Sons, New York, 1996).

    Google Scholar 

  4. Atlas, R. M. & Bartha, R. Microbial Ecology 4th edn (Addison Wesley, New York, 1997).

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  6. Amann, R., Ludwig, W. & Schleifer, K. -H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59, 143–169 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Curtis, T. P., Sloan, W. T. & Scannell, J. W. Estimating prokaryotic diversity and its limits. Proc. Natl Acad. Sci. USA 99, 10494–10499 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Madsen, E. L. Epistemology of environmental microbiology. Environ. Sci. Technol. 32, 429–439 (1998).

    CAS  Google Scholar 

  9. Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: the unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Waksman, S. A. Principles of Soil Microbiology (Williams and Wilkins, Maryland, 1927).

    Google Scholar 

  11. Ehrlich, H. L. Geomicrobiology 4th edn (Marcel Dekker Inc., New York, 2002).

    Google Scholar 

  12. Waksman, S. A. Soil microbiology as a field of science. Science 102, 339–344 (1945).

    CAS  PubMed  Google Scholar 

  13. Winogradsky, S. Microbologie du Sol, Problèmes et Méthodes; Cinquante Ans de Recherches. Oeuvres Complètes. (Masson, Paris, 1949).

    Google Scholar 

  14. Torsvik, V., Ovreas, L. & Thingstad, T. F. Prokaryotic diversity — magnitude, dynamics, and controlling factors. Science 296, 1064–1066 (2002).

    CAS  PubMed  Google Scholar 

  15. Henis, Y. (ed) Survival and Dormancy of Microorganisms (John Wiley & Sons, New York, 1987).

    Google Scholar 

  16. Brock, T. D. in Ecology of Microbial Communities. (eds Fletcher, M., Gray, T. R. G. & Jones, J. G.) (Cambridge University Press, New York, 1987). Symp. Soc. Gen. Microbiol. 41, 1–17 (1987).

    Google Scholar 

  17. Antelmann, H., Scharf, C. & Hecker, M. Phosphate starvation-inducible proteins of Bacillus subtilis: proteomics and transcriptional analysis. J. Bacteriol. 182, 4478–4490 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Imlay, J. A. Pathways of oxidative damage. Annu. Rev. Microbiol. 57, 395–418 (2003).

    CAS  PubMed  Google Scholar 

  19. Miller, M. B. & Bassler, B. L. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55, 165–199 (2001).

    CAS  PubMed  Google Scholar 

  20. Venrick, E. L., Beers, J. R. & Heinbokel, J. F. Possible consequence of containing microplankton for physiological rate measurements. J. Exp. Mar. Biol. Ecol. 26, 55–76 (1977).

    CAS  Google Scholar 

  21. Vaulot, D., Marie, D. Olson, R. J. & Chisholm, S. W. Growth of Prochlorococcus, a photosynthetic prokaryote, in the equatorial Pacific Ocean. Science 268, 1480–1482 (1995).

    CAS  PubMed  Google Scholar 

  22. Beja, O., Spuduch, E. N., Spudich, J. L., Leclerc, M. & DeLong, E. F. Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789 (2001).

    CAS  PubMed  Google Scholar 

  23. Hugenholtz, P., Goebel, B. M. & Pace, N. R. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180, 4765–4774 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Tyson, G. W. et al. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37–43 (2004).

    CAS  PubMed  Google Scholar 

  25. van Wintzingerode, F. V., Gobel, J. B. & Stackebrandt, E. Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol. Rev. 21, 213–229 (1997).

    Google Scholar 

  26. Koch, R. Mittbeilungen aus dem Kaiserlichen Gesundheitsamte 2, 1–88 (1884). English translation in Milestones in Microbiology (ed. T. D. Brock) 116–118 (Prentice Hall Inc., New Jersey, 1961).

    Google Scholar 

  27. Falkow, S. Molecular Koch's postulates applied to bacterial pathogenicity — a personal recollection 15 years later. Nature Rev. Microbiol. 2, 67–72 (2004).

    CAS  Google Scholar 

  28. Brooks, G. F., Butel, J. S. & Morse, S. A. Medical Microbiology 23rd edn (McGraw–Hill, New York, 2004).

    Google Scholar 

  29. Sugden, A., Ash, C., Hanson, B. & Smith, J. Where do we go from here? Science 302, 1906 (2003).

    CAS  Google Scholar 

  30. Reysenbach, A. -L. & Shock, E. Merging genomes with geochemistry in hydrothermal ecosystems. Science 296, 1077–1082 (2002).

    CAS  PubMed  Google Scholar 

  31. van der Wielen, P. W. et al. The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 307, 121–123 (2005).

    CAS  PubMed  Google Scholar 

  32. D'Hondt, S. et al. Distributions of microbial activities in deep seafloor sediments. Science 306, 2216–2221 (2004).

    CAS  PubMed  Google Scholar 

  33. Jouzel, J. et al. More than 200 meters of lake ice above subglacial Lake Vostok, Antarctica. Science 286, 2138–2141 (1999).

    CAS  PubMed  Google Scholar 

  34. Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004).

    CAS  PubMed  Google Scholar 

  35. Hallam, S. J. et al. Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305, 1457–1462 (2004).

    CAS  PubMed  Google Scholar 

  36. Button, D. K., Schut, F., Quang, P., Martin, R. & Robertson, B. R. Viability and isolation of marine bacteria by dilution culture: theory, procedures, and initial results. Appl. Environ. Microbiol. 59, 881–891 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Rappe, M. S., Connon, S. A., Vergin, K. L. & Giovannoni, S. J. Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418, 630–633 (2002).

    CAS  PubMed  Google Scholar 

  38. Kaeberlein, T., Lewis, K. & Epstein, S. S. Isolating 'uncultivable' microorganisms in pure culture in a simulated natural environment. Science 296, 1127–1129 (2002).

    CAS  PubMed  Google Scholar 

  39. Rocap, G. et al. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424, 1042–1047 (2003).

    CAS  PubMed  Google Scholar 

  40. Church, M. et al. Abundance and distribution of planktonic Archaea and Bacteria in the waters west of the Antarctic Peninsula. Limnol. Oceanograph. 48, 1893–1902 (2003).

    Google Scholar 

  41. Felske, A., Wolterink, A., Van Lis, R., De Vos, W. M. & Akkermans, A. D. Response of a soil bacterial community to grassland succession as monitored by 16S rRNA levels of the predominant ribotypes. Appl. Environ. Microbiol. 66, 3998–4003 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Partensky, F., Hess, W. R. & Vaulot, D. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63, 106–127 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Ting, C. S., Rocap, G., King, J. & Chisholm, S. W. Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends Microbiol. 10, 134–142 (2002).

    CAS  PubMed  Google Scholar 

  44. Pichard, S. L. et al. Analysis of ribulose bisphosphate carboxylase gene expression in natural phytoplankton communities by group-specific gene probing. Marine Ecol. Prog. Ser. 149, 239–253 (1997).

    CAS  Google Scholar 

  45. Heemsbergen, D. A. Biodiversity effects on soil processes explained by interspecific functional dissimilarity. Science 306, 1019–1020 (2004).

    CAS  PubMed  Google Scholar 

  46. Jones, T. H. et al. Impacts of rising atmospheric carbon dioxide on model terrestrial ecosystems. Science 280, 441–443 (1998).

    CAS  PubMed  Google Scholar 

  47. Conrad, R. Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol. Rev. 60, 609–640 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Schink, B. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol. Mol. Biol. Rev. 61, 262–280 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Bull, I. D., Parekh, N. R., Hall, G. H., Ineson, P. & Evershed, R. P. Detection and classification of atmospheric methane oxidizing bacteria in soil. Nature 405, 175–178 (2000).

    CAS  PubMed  Google Scholar 

  50. Segers, R. Methane production and methane consumption: a review of processes underlying wetland methane fluxes. Biogeochemistry 41, 23–51 (1998).

    CAS  Google Scholar 

  51. Boetius, A. et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623–626 (2000).

    CAS  PubMed  Google Scholar 

  52. Boxall, A. B., Sinclair, C. J., Fenner, K., Kolpin, D. & Maund, S. J. When synthetic chemicals degrade in the environment. Environ. Sci. Technol. 38, 369A–375A (2004).

    Google Scholar 

  53. Alexander, M. Biodegradation and Bioremediation 2nd edn (Academic Press, San Diego, California, 1999).

    Google Scholar 

  54. Van Hamme, J. C., Singh, A. & Ward, O. P. Recent advances in petroleum microbiology. Microbiol. Mol. Biol. Rev. 67, 503–549 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Deeb, R. A. et al. MTBE and other oxygenates: environmental sources, analysis, occurrence, and treatment. Environ. Eng. Sci. 20, 433–447 (2003).

    CAS  Google Scholar 

  56. Spain, J. C., Hughes, J. B., & Knackmuss, H. -J. (eds) Biodegradation of Nitroaromatic Compounds and Explosives. (Lewis Publishers, Boca Raton, Florida, 2000).

    Google Scholar 

  57. Esteve-Núñez, A., Caballero, A. & Ramos, J. L. Biological degradation of 2,4,6-trinitrotoluene. Microbiol. Mol. Biol. Rev. 65, 335–352 (2001).

    PubMed  PubMed Central  Google Scholar 

  58. Ternes, T. A., Joss, A. & Seigrist, H. Scrutinizing personal care products. Environ. Sci. Technol. 38, 393A–399A (2004).

    Google Scholar 

  59. Maymo-Gatell, X., Chien, Y., Gossett, J. M. & Zinder, S. H. Isolation of a bacterium that reductively dechlorinates tetrachloroethene to ethene. Science 276, 1568–1571 (1997).

    CAS  PubMed  Google Scholar 

  60. Adrian, L., Szewzyk, U., Wecke, J. & Gorisch, H. Bacterial dehalorespiration with chlorinated benzenes. Nature 408, 580–583 (2000).

    CAS  PubMed  Google Scholar 

  61. Karl, D. et al. Dinitrogen fixation in the world's oceans. Biogeochem. 57–58, 47–98 (2002).

    Google Scholar 

  62. Stark, J. M. & Hart, S. C. High rates of nitrification and nitrate turnover in undisturbed coniferous forests. Nature 385, 61–64 (1997).

    CAS  Google Scholar 

  63. Kowalchuk, G. A. & Stephen, J. R. Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu. Rev. Microbiol. 55, 485–529 (2001).

    CAS  PubMed  Google Scholar 

  64. Dalsgaard, T., Canfield, D. E., Petersen, J., Thamdrup, B. & Acuna-Gonzalez, J. N2 production by the anammox reaction in the anoxic water column of Golfo Culce, Costa Rica. Nature 422, 606–608 (2003).

    CAS  PubMed  Google Scholar 

  65. van Niftrik, L. A. et al. The anammoxosome: an intracytoplasmic compartment in anammox bacteria. FEMS Microbiol. Lett. 233, 7–31 (2004).

    CAS  PubMed  Google Scholar 

  66. Zumft, W. G. Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61, 533–616 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. van Breemen, N. et al. Where did all the nitrogen go? Fate of nitrogen inputs to large watersheds in the northeastern U. S. A. Biogeochem. 57–58, 267–293 (2002).

    Google Scholar 

  68. Taylor, C. D. & Wirsen, C. O. Microbiology and ecology of filamentous sulfur formation. Science 277, 1483–1485 (1997).

    CAS  Google Scholar 

  69. Habicht, K. S. & Canfield, D. E. Sulphur isotope fractionation in modern microbial mats and the evolution of the sulphur cycle. Nature 25, 342–343 (1996).

    Google Scholar 

  70. Morel, F. M., Kraepiel, A. M. L. & Amyiot, M. The chemical cycle and bioaccumulation of mercury. Annu. Rev. Ecol. Systemat. 29, 543–566 (1998).

    Google Scholar 

  71. Baldi, F. in Metal Ions in Biological Systems: Mercury and its Effects on Environment and Biology (eds Sigel, A. & Sigel, H.) 213–257 (Marcel Dekker, New York, 1997).

    Google Scholar 

  72. Coates, J. D. & Achenbach, L. A. Microbial perchlorate reduction: rocket-fuelled metabolism. Nature Rev. Microbiol. 2, 569–580 (2004).

    CAS  Google Scholar 

  73. Lovley, D. R. Cleaning up with genomics: applying molecular biology to bioremediation. Nature Rev. Microbiol. 1, 35–44 (2003).

    CAS  Google Scholar 

  74. Oremland, R. S. & Stolz, F. J. The ecology of arsenic. Science 300, 939–944 (2003).

    CAS  PubMed  Google Scholar 

  75. Edwards, K. J., Bond, P. L., Gihrling, T. M. & Banfield, J. F. An archaeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 287, 1796–1799 (2000).

    CAS  PubMed  Google Scholar 

  76. Fred, E. B., Baldwin, I. L. & McCoy, E. Root Nodule Bacteria and Leguminous Plants. University of Wisconsin Studies in Science, No. 5. (University of Wisconsin, Madison, 1932).

    Google Scholar 

  77. Major, D. W. et al. Field demonstration of successful bioaugmentation to achieve dechlorination of tetrachloroethene to ethene. Environ. Sci. Technol. 36, 5106–5116 (2002).

    CAS  PubMed  Google Scholar 

  78. Brock, T. D. & Brock, M. L. Autoradiography as a tool in microbial ecology. Nature 209, 723–736 (1966).

    Google Scholar 

  79. Fliermans, C. B. & Schmidt, E. L. Autoradiography and immunofluorescence combined for autoecological study of single cell activity with Nitrobacter as a model system. Appl. Microbiol. 30, 676–684 (1975).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Ward, B. B. Combined autoradiography and immunofluorescence for estimation of single cell activity by ammonium-oxidizing bacteria. Limnol. Oceanogr. 29, 402–410 (1984).

    Google Scholar 

  81. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Lee, N. et al. Combination of fluorescent in situ hybridization and microautoradiography— a new tool for structure–function analyses in microbial ecology. Appl. Environ. Microbiol. 65, 1289–1297 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Nielsen, J. L., Christensen, D., Kloppenberg, M. & Nielsen, P. H. Quantification of cell-specific substrate uptake by probe-defined bacteria under in situ conditions by microautoradiography and fluorescence in situ hybridization. Environ. Microbiol. 5, 202–211 (2003).

    CAS  PubMed  Google Scholar 

  84. Pernthaler, A. & Amann, R. Simultaneous fluorescence in situ hybridization of mRNA and rRNA in environmental bacteria. Appl. Environ. Microbiol. 70, 5426–5433 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Hinrichs, K. -U., Hayes, J. M., Sylva, S. P., Brewer, P. G. & DeLong, E. F. Methane-consuming archaebacteria in marine sediments. Nature 398, 802–805 (1999).

    CAS  PubMed  Google Scholar 

  86. 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).

    CAS  PubMed  Google Scholar 

  87. Michaelis, W. et al. Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane. Science 297, 1013–1015 (2002).

    CAS  PubMed  Google Scholar 

  88. Boschker, H. T. S. et al. Direct linking of microbial populations to specific biogeochemical processes by 13C-labelling of biomarkers. Nature 392, 801–805 (1998).

    CAS  Google Scholar 

  89. Radajewski, S., Ineson, P., Parekh, N. R. & Murrell, J. C. Stable-isotope probing as a tool in microbial ecology. Nature 403, 646–649 (2000).

    CAS  PubMed  Google Scholar 

  90. Manefield, M., Whiteley, A. S., Griffiths, R. I. & Bailey, M. J. RNA stable isotope probing, a novel means of linking microbial community function to phylogeny. Appl. Environ. Microbiol. 68, 5367–5373 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Ginige, M. P. et al. Use of stable-isotope probing, full-cycle rRNA analysis, and fluorescence in situ hybridization-microautoradiography to study a methanol-fed denitrifying microbial community. Appl. Environ. Microbiol. 70, 588–596 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Jeon, C. -O. et al. Discovery of a novel bacterium, with distinctive dioxygenase, that is responsible for in situ biodegradation in a contaminated sediment. Proc. Natl Acad. Sci. USA 100, 13591–13596 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Capone, D. A., Zehr, J. P., Paerl, H., Bergman, B. & Carpenter, E. J. Trichodesmium, a globally significant marine cyanobacterium. Science 276, 1221–1229 (1997).

    CAS  Google Scholar 

  94. Paerl, H. W., Priscu, J. C. & Brawner, D. L. Immunochemical localization of nitrogenase in marine Trichodesmium aggregates: relationship to N2 fixation potential. Appl. Environ. Microbiol. 55, 2965–2975 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Montoya, J. P. et al. High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430, 1027–1031 (2004).

    CAS  PubMed  Google Scholar 

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Acknowledgements

Support was provided by the National Science Foundation and the National Institute of Environmental Health Sciences. The author is grateful to the Second Okazaki Biology Conference on Terra Microbiology and many colleagues, past and present, whose collaboration has enabled his own work and the development of views expressed here.

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Madsen, E. Identifying microorganisms responsible for ecologically significant biogeochemical processes. Nat Rev Microbiol 3, 439–446 (2005). https://doi.org/10.1038/nrmicro1151

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