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Molecular eco-systems biology: towards an understanding of community function

Nature Reviews Microbiology volume 6, pages 693–699 (2008)Cite this article

Abstract

Systems-biology approaches, which are driven by genome sequencing and high-throughput functional genomics data, are revolutionizing single-cell-organism biology. With the advent of various high-throughput techniques that aim to characterize complete microbial ecosystems (metagenomics, meta-transcriptomics and meta-metabolomics), we propose that the time is ripe to consider molecular systems biology at the ecosystem level (eco-systems biology). Here, we discuss the necessary data types that are required to unite molecular microbiology and ecology to develop an understanding of community function and discuss the potential shortcomings of these approaches.

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Figure 1: Systems biology: from proteins to environments.
Figure 2: From metagenomes to ecosystem functioning: influencing factors and hidden dependencies.
Figure 3: Visualizing complex environmental patterns.

References

  1. Bork, P. Is there biological research beyond Systems Biology? A comparative analysis of terms. Mol. Syst. Biol. 1, 2005.0012 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Joyce, A. R. & Palsson, B. O. The model organism as a system: integrating 'omics' data sets. Nature Rev. Mol. Cell Biol. 7, 198–210 (2006).

    Article  CAS  Google Scholar 

  3. Kitano, H. Systems biology: a brief overview. Science 295, 1662–1664 (2002).

    Article  CAS  PubMed  Google Scholar 

  4. McMahon, K. D., Martin, H. G. & Hugenholtz, P. Integrating ecology into biotechnology. Curr. Opin. Biotechnol. 18, 287–292 (2007).

    Article  CAS  PubMed  Google Scholar 

  5. Azam, F. & Worden, A. Z. Oceanography. Microbes, molecules, and marine ecosystems. Science 303, 1622–1624 (2004).

    Article  CAS  PubMed  Google Scholar 

  6. Bork, P. & Serrano, L. Towards cellular systems in 4D. Cell 121, 507–509 (2005).

    Article  CAS  PubMed  Google Scholar 

  7. Palsson, B. Two-dimensional annotation of genomes. Nature Biotechnol. 22, 1218–1219 (2004).

    Article  CAS  Google Scholar 

  8. Harrington, E. D. et al. Quantitative assessment of protein function prediction from metagenomics shotgun sequences. Proc. Natl Acad. Sci. USA 104, 13913–13918 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Raes, J., Harrington, E. D., Singh, A. H. & Bork, P. Protein function space: viewing the limits or limited by our view? Curr. Opin. Struct. Biol. 17, 362–369 (2007).

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  11. Lu, Y. & Conrad, R. In situ stable isotope probing of methanogenic archaea in the rice rhizosphere. Science 309, 1088–1090 (2005).

    Article  CAS  PubMed  Google Scholar 

  12. Whiteley, A. S., Manefield, M. & Lueders, T. Unlocking the 'microbial black box' using RNA-based stable isotope probing technologies. Curr. Opin. Biotechnol. 17, 67–71 (2006).

    Article  CAS  PubMed  Google Scholar 

  13. O'Donnell, A. G., Young, I. M., Rushton, S. P., Shirley, M. D. & Crawford, J. W. Visualization, modelling and prediction in soil microbiology. Nature Rev. Microbiol. 5, 689–699 (2007).

    Article  CAS  Google Scholar 

  14. Adamczyk, J. et al. The isotope array, a new tool that employs substrate-mediated labeling of rRNA for determination of microbial community structure and function. Appl. Environ. Microbiol. 69, 6875–6887 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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).

    Article  CAS  PubMed  Google Scholar 

  16. Kuypers, M. M. & Jorgensen, B. B. The future of single-cell environmental microbiology. Environ. Microbiol. 9, 6–7 (2007).

    Article  PubMed  Google Scholar 

  17. Neufeld, J. D. & Murrell, J. C. Witnessing the last supper of uncultivated microbial cells with Raman–FISH. ISME J. 1, 269–270 (2007).

    Article  PubMed  Google Scholar 

  18. Handelsman, J. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68, 669–685 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Beja, O. et al. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289, 1902–1906 (2000).

    Article  CAS  PubMed  Google Scholar 

  20. Ottesen, E. A., Hong, J. W., Quake, S. R. & Leadbetter, J. R. Microfluidic digital PCR enables multigene analysis of individual environmental bacteria. Science 314, 1464–1467 (2006).

    Article  CAS  PubMed  Google Scholar 

  21. Stepanauskas, R. & Sieracki, M. E. Matching phylogeny and metabolism in the uncultured marine bacteria, one cell at a time. Proc. Natl Acad. Sci. USA 104, 9052–9057 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lau, S. C. & Liu, W. T. Recent advances in molecular techniques for the detection of phylogenetic markers and functional genes in microbial communities. FEMS Microbiol. Lett. 275, 183–190 (2007).

    Article  CAS  PubMed  Google Scholar 

  23. Eisen, J. A. Environmental shotgun sequencing: its potential and challenges for studying the hidden world of microbes. PLoS Biol. 5, e82 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Tringe, S. G. & Rubin, E. M. Metagenomics: DNA sequencing of environmental samples. Nature Rev. Genet. 6, 805–814 (2005).

    Article  CAS  PubMed  Google Scholar 

  25. Tringe, S. G. et al. Comparative metagenomics of microbial communities. Science 308, 554–557 (2005).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  28. Liolios, K., Tavernarakis, N., Hugenholtz, P. & Kyrpides, N. C. The Genomes On Line Database (GOLD) v.2: a monitor of genome projects worldwide. Nucleic Acids Res. 34, D332–D334 (2006).

    Article  CAS  PubMed  Google Scholar 

  29. Raes, J., Foerstner, K. U. & Bork, P. Get the most out of your metagenome: computational analysis of environmental sequence data. Curr. Opin. Microbiol. 10, 490–498 (2007).

    Article  CAS  PubMed  Google Scholar 

  30. Raes, J., Korbel, J. O., Lercher, M. J., von Mering, C. & Bork, P. Prediction of effective genome size in metagenomic samples. Genome Biol. 8, R10 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Angly, F. et al. PHACCS, an online tool for estimating the structure and diversity of uncultured viral communities using metagenomic information. BMC Bioinformatics 6, 41 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. O'Toole, G., Kaplan, H. B. & Kolter, R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54, 49–79 (2000).

    Article  CAS  PubMed  Google Scholar 

  33. Bassler, B. L. & Losick, R. Bacterially speaking. Cell 125, 237–246 (2006).

    Article  CAS  PubMed  Google Scholar 

  34. Keller, L. & Surette, M. G. Communication in bacteria: an ecological and evolutionary perspective. Nature Rev. Microbiol. 4, 249–258 (2006).

    Article  CAS  Google Scholar 

  35. Martiny, J. B. et al. Microbial biogeography: putting microorganisms on the map. Nature Rev. Microbiol. 4, 102–112 (2006).

    Article  CAS  Google Scholar 

  36. Shapiro, J. A. Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52, 81–104 (1998).

    Article  CAS  PubMed  Google Scholar 

  37. Schink, B. Synergistic interactions in the microbial world. Antonie Van Leeuwenhoek 81, 257–261 (2002).

    Article  CAS  PubMed  Google Scholar 

  38. Woyke, T. et al. Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443, 950–955 (2006).

    Article  CAS  PubMed  Google Scholar 

  39. McCutcheon, J. P. & Moran, N. A. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc. Natl Acad. Sci. USA 104, 19392–19397 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Wu, D. et al. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 4, e188 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Stolyar, S. et al. Metabolic modeling of a mutualistic microbial community. Mol. Syst. Biol. 3, 92 (2007).

    Article  PubMed  PubMed Central  CAS  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  CAS  PubMed  PubMed Central  Google Scholar 

  43. Giovannoni, S. & Stingl, U. The importance of culturing bacterioplankton in the 'omics' age. Nature Rev. Microbiol. 5, 820–826 (2007).

    Article  CAS  Google Scholar 

  44. Zhang, K. et al. Sequencing genomes from single cells by polymerase cloning. Nature Biotechnol. 24, 680–686 (2006).

    Article  CAS  Google Scholar 

  45. Steward, G. F. & Rappe, M. S. What's the 'meta' with metagenomics? ISME J. 1, 100–102 (2007).

    Article  PubMed  Google Scholar 

  46. Hutchison, C. A. & Venter, J. C. Single-cell genomics. Nature Biotechnol. 24, 657–658 (2006).

    Article  CAS  Google Scholar 

  47. Dethlefsen, L. & Relman, D. A. The importance of individuals and scale: moving towards single cell microbiology. Environ. Microbiol. 9, 8–10 (2007).

    Article  PubMed  Google Scholar 

  48. Marcy, Y. et al. Dissecting biological “dark matter” with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc. Natl Acad. Sci. USA 104, 11889–11894 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Ochman, H. Single-cell genomics. Environ. Microbiol. 9, 7 (2007).

    Article  PubMed  Google Scholar 

  50. Battin, T. J. et al. Microbial landscapes: new paths to biofilm research. Nature Rev. Microbiol. 5, 76–81 (2007).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  52. Pepperkok, R. & Ellenberg, J. High-throughput fluorescence microscopy for systems biology. Nature Rev. Mol. Cell Biol. 7, 690–696 (2006).

    Article  CAS  Google Scholar 

  53. Gotelli, N. J. & McCabe, D. J. Species co-occurrence: a meta-analysis of JM Diamond's assembly rules model. Ecology 83, 2091–2096 (2002).

    Article  Google Scholar 

  54. Horner-Devine, M. C. et al. A comparison of taxon co-occurrence patterns for macro- and microorganisms. Ecology 88, 1345–1353 (2007).

    Article  PubMed  Google Scholar 

  55. Fuhrman, J. A. et al. Annually reoccurring bacterial communities are predictable from ocean conditions. Proc. Natl Acad. Sci. USA 103, 13104–13109 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Follows, M. J., Dutkiewicz, S., Grant, S. & Chisholm, S. W. Emergent biogeography of microbial communities in a model ocean. Science 315, 1843–1846 (2007).

    Article  CAS  PubMed  Google Scholar 

  57. Wingreen, N. S. & Levin, S. A. Cooperation among microorganisms. PLoS Biol. 4, e299 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Bailly, J. et al. Soil eukaryotic functional diversity, a metatranscriptomic approach. ISME J. 1, 632–642 (2007).

    Article  CAS  PubMed  Google Scholar 

  59. Lo, I. et al. Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446, 537–541 (2007).

    Article  CAS  PubMed  Google Scholar 

  60. Ram, R. J. Community proteomics of a natural microbial biofilm. Science 308, 1915–1920 (2005).

    Article  CAS  PubMed  Google Scholar 

  61. Kuhn, M., Campillos, M., von Mering, C., Jensen, L. J. & Bork P. STITCH: interaction networks of chemicals and proteins. Nucleic Acids Res. 36, D684–D688 (2008).

    Article  CAS  PubMed  Google Scholar 

  62. West, S. A., Griffin, A. S., Gardner, A. & Diggle, S. P. Social evolution theory for microorganisms. Nature Rev. Microbiol. 4, 597–607 (2006).

    Article  CAS  Google Scholar 

  63. Bell, T. Larger islands house more bacterial taxa. Science 308,1884 (2005).

    Article  CAS  PubMed  Google Scholar 

  64. Green, J. L. Spatial scaling of microbial eukaryote diversity. Nature 432, 747–750 (2004).

    Article  CAS  PubMed  Google Scholar 

  65. Horner-Devine, M. C., Lage, M., Hughes, J. B. & Bohannan, B. J. A taxa-area relationship for bacteria. Nature 432, 750–753 (2004).

    Article  CAS  PubMed  Google Scholar 

  66. Palmer, C., Bik, E. M., Digiulio, D. B., Relman, D. A. & Brown, P. O. Development of the human infant intestinal microbiota. PLoS Biol. 5, e177 (2007).

    PubMed  PubMed Central  Google Scholar 

  67. Thompson, J. R. Genotypic diversity within a natural coastal bacterioplankton population. Science 307, 1311–1313 (2005).

    Article  CAS  PubMed  Google Scholar 

  68. Lozupone, C. A. & Knight, R. Global patterns in bacterial diversity. Proc. Natl Acad. Sci. USA 104, 11436–11440 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Torsvik, V. & Ovreas, L. Microbial diversity and function in soil: from genes to ecosystems. Curr. Opin. Microbiol. 5, 240–245 (2002).

    Article  CAS  PubMed  Google Scholar 

  70. DeLong, E. F. et al. Community genomics among stratified microbial assemblages in the ocean's interior. Science 311, 496–503 (2006).

    Article  CAS  PubMed  Google Scholar 

  71. Kunin, V. et al. Millimeter-scale genetic gradients and community-level molecular convergence in a hypersaline microbial mat. Mol. Syst. Biol. 4, 198 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Seymour, J. R., Mitchell, J. G., Pearson, L. & Waters, R. L. Heterogeneity in bacterioplankton abundance from 4.5 millimetre resolution sampling. Aquat. Microb. Ecol. 22, 143–153 (2000).

    Article  Google Scholar 

  73. He, Z. et al. GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J. 1, 67–77 (2007).

    Article  CAS  PubMed  Google Scholar 

  74. Moisander, P. H. Application of a nifH oligonucleotide microarray for profiling diversity of N2-fixing microorganisms in marine microbial mats. Environ. Microbiol. 8, 1721–1735 (2006).

    Article  CAS  PubMed  Google Scholar 

  75. Palmer, C. Rapid quantitative profiling of complex microbial populations. Nucleic Acids Res. 34, e5 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Polz, M. F., Bertilsson, S., Acinas, S. G. & Hunt, D. A(r)Ray of hope in analysis of the function and diversity of microbial communities. Biol. Bull. 204, 196–199 (2003).

    Article  CAS  PubMed  Google Scholar 

  77. Rich, V. I., Konstantinidis, K. & Delong, E. F. Design and testing of 'genome-proxy' microarrays to profile marine microbial communities. Environ. Microbiol. 10, 506–521 (2008).

    Article  CAS  PubMed  Google Scholar 

  78. Gentry, T. J., Wickham, G. S., Schadt, C. W., He, Z. & Zhou, J. Microarray applications in microbial ecology research. Microb. Ecol. 52, 159–175 (2006).

    Article  CAS  PubMed  Google Scholar 

  79. Wold, B. & Myers, R. M. Sequence census methods for functional genomics. Nature Methods 5, 19–21 (2008).

    Article  CAS  PubMed  Google Scholar 

  80. Committee on metagenomics: challenges and functional applications. The New Science of Metagenomics: Revealing the Secrets of our Microbial Planet (The National Academies, Washington DC, 2007).

  81. Field, D. et al. The minimum information about a genome sequence (MIGS) specification. Nature Biotechnol. 26, 541–547 (2008).

    Article  CAS  Google Scholar 

  82. Markowitz, V. M. et al. An experimental metagenome data management and analysis system. Bioinformatics 22, e359–e367 (2006).

    Article  CAS  PubMed  Google Scholar 

  83. Seshadri, R., Kravitz, S. A., Smarr, L., Gilna, P. & Frazier, M. CAMERA: a community resource for metagenomics. PLoS Biol. 5, e75 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Kanehisa, M. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res. 34, D354–D357 (2006).

    Article  CAS  PubMed  Google Scholar 

  85. Letunic, I., Yamada, T., Kanehisa, M. & Bork, P. iPath: interactive exploration of biochemical pathways and networks. Trends Biochem. Sci. 33, 101–103 (2008).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank L. Jensen, A. Singh and other members of the Bork group for valuable comments. The author's research is funded by the FP7 programme (grant number HEALTH-F4-2007-201,052).

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  1. Jeroen Raes and Peer Bork are at the European Molecular Biology Laboratory, Meyerhofstrasse 1, D-69117 Heidelberg, Germany. raes@embl.de bork@embl.de,

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Raes, J., Bork, P. Molecular eco-systems biology: towards an understanding of community function. Nat Rev Microbiol 6, 693–699 (2008). https://doi.org/10.1038/nrmicro1935

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