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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References
Bork, P. Is there biological research beyond Systems Biology? A comparative analysis of terms. Mol. Syst. Biol. 1, 2005.0012 (2005).
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).
Kitano, H. Systems biology: a brief overview. Science 295, 1662–1664 (2002).
McMahon, K. D., Martin, H. G. & Hugenholtz, P. Integrating ecology into biotechnology. Curr. Opin. Biotechnol. 18, 287–292 (2007).
Azam, F. & Worden, A. Z. Oceanography. Microbes, molecules, and marine ecosystems. Science 303, 1622–1624 (2004).
Bork, P. & Serrano, L. Towards cellular systems in 4D. Cell 121, 507–509 (2005).
Palsson, B. Two-dimensional annotation of genomes. Nature Biotechnol. 22, 1218–1219 (2004).
Harrington, E. D. et al. Quantitative assessment of protein function prediction from metagenomics shotgun sequences. Proc. Natl Acad. Sci. USA 104, 13913–13918 (2007).
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).
Pace, N. R. A molecular view of microbial diversity and the biosphere. Science 276, 734–740 (1997).
Lu, Y. & Conrad, R. In situ stable isotope probing of methanogenic archaea in the rice rhizosphere. Science 309, 1088–1090 (2005).
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).
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).
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).
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).
Kuypers, M. M. & Jorgensen, B. B. The future of single-cell environmental microbiology. Environ. Microbiol. 9, 6–7 (2007).
Neufeld, J. D. & Murrell, J. C. Witnessing the last supper of uncultivated microbial cells with Raman–FISH. ISME J. 1, 269–270 (2007).
Handelsman, J. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68, 669–685 (2004).
Beja, O. et al. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289, 1902–1906 (2000).
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).
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).
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).
Eisen, J. A. Environmental shotgun sequencing: its potential and challenges for studying the hidden world of microbes. PLoS Biol. 5, e82 (2007).
Tringe, S. G. & Rubin, E. M. Metagenomics: DNA sequencing of environmental samples. Nature Rev. Genet. 6, 805–814 (2005).
Tringe, S. G. et al. Comparative metagenomics of microbial communities. Science 308, 554–557 (2005).
Tyson, G. W. et al. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37–43 (2004).
Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004).
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).
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).
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).
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).
O'Toole, G., Kaplan, H. B. & Kolter, R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54, 49–79 (2000).
Bassler, B. L. & Losick, R. Bacterially speaking. Cell 125, 237–246 (2006).
Keller, L. & Surette, M. G. Communication in bacteria: an ecological and evolutionary perspective. Nature Rev. Microbiol. 4, 249–258 (2006).
Martiny, J. B. et al. Microbial biogeography: putting microorganisms on the map. Nature Rev. Microbiol. 4, 102–112 (2006).
Shapiro, J. A. Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52, 81–104 (1998).
Schink, B. Synergistic interactions in the microbial world. Antonie Van Leeuwenhoek 81, 257–261 (2002).
Woyke, T. et al. Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443, 950–955 (2006).
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).
Wu, D. et al. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 4, e188 (2006).
Stolyar, S. et al. Metabolic modeling of a mutualistic microbial community. Mol. Syst. Biol. 3, 92 (2007).
Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol. 5, e77 (2007).
Giovannoni, S. & Stingl, U. The importance of culturing bacterioplankton in the 'omics' age. Nature Rev. Microbiol. 5, 820–826 (2007).
Zhang, K. et al. Sequencing genomes from single cells by polymerase cloning. Nature Biotechnol. 24, 680–686 (2006).
Steward, G. F. & Rappe, M. S. What's the 'meta' with metagenomics? ISME J. 1, 100–102 (2007).
Hutchison, C. A. & Venter, J. C. Single-cell genomics. Nature Biotechnol. 24, 657–658 (2006).
Dethlefsen, L. & Relman, D. A. The importance of individuals and scale: moving towards single cell microbiology. Environ. Microbiol. 9, 8–10 (2007).
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).
Ochman, H. Single-cell genomics. Environ. Microbiol. 9, 7 (2007).
Battin, T. J. et al. Microbial landscapes: new paths to biofilm research. Nature Rev. Microbiol. 5, 76–81 (2007).
Boetius, A. et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623–626 (2000).
Pepperkok, R. & Ellenberg, J. High-throughput fluorescence microscopy for systems biology. Nature Rev. Mol. Cell Biol. 7, 690–696 (2006).
Gotelli, N. J. & McCabe, D. J. Species co-occurrence: a meta-analysis of JM Diamond's assembly rules model. Ecology 83, 2091–2096 (2002).
Horner-Devine, M. C. et al. A comparison of taxon co-occurrence patterns for macro- and microorganisms. Ecology 88, 1345–1353 (2007).
Fuhrman, J. A. et al. Annually reoccurring bacterial communities are predictable from ocean conditions. Proc. Natl Acad. Sci. USA 103, 13104–13109 (2006).
Follows, M. J., Dutkiewicz, S., Grant, S. & Chisholm, S. W. Emergent biogeography of microbial communities in a model ocean. Science 315, 1843–1846 (2007).
Wingreen, N. S. & Levin, S. A. Cooperation among microorganisms. PLoS Biol. 4, e299 (2006).
Bailly, J. et al. Soil eukaryotic functional diversity, a metatranscriptomic approach. ISME J. 1, 632–642 (2007).
Lo, I. et al. Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446, 537–541 (2007).
Ram, R. J. Community proteomics of a natural microbial biofilm. Science 308, 1915–1920 (2005).
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).
West, S. A., Griffin, A. S., Gardner, A. & Diggle, S. P. Social evolution theory for microorganisms. Nature Rev. Microbiol. 4, 597–607 (2006).
Bell, T. Larger islands house more bacterial taxa. Science 308,1884 (2005).
Green, J. L. Spatial scaling of microbial eukaryote diversity. Nature 432, 747–750 (2004).
Horner-Devine, M. C., Lage, M., Hughes, J. B. & Bohannan, B. J. A taxa-area relationship for bacteria. Nature 432, 750–753 (2004).
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).
Thompson, J. R. Genotypic diversity within a natural coastal bacterioplankton population. Science 307, 1311–1313 (2005).
Lozupone, C. A. & Knight, R. Global patterns in bacterial diversity. Proc. Natl Acad. Sci. USA 104, 11436–11440 (2007).
Torsvik, V. & Ovreas, L. Microbial diversity and function in soil: from genes to ecosystems. Curr. Opin. Microbiol. 5, 240–245 (2002).
DeLong, E. F. et al. Community genomics among stratified microbial assemblages in the ocean's interior. Science 311, 496–503 (2006).
Kunin, V. et al. Millimeter-scale genetic gradients and community-level molecular convergence in a hypersaline microbial mat. Mol. Syst. Biol. 4, 198 (2008).
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).
He, Z. et al. GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J. 1, 67–77 (2007).
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).
Palmer, C. Rapid quantitative profiling of complex microbial populations. Nucleic Acids Res. 34, e5 (2006).
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).
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).
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).
Wold, B. & Myers, R. M. Sequence census methods for functional genomics. Nature Methods 5, 19–21 (2008).
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).
Field, D. et al. The minimum information about a genome sequence (MIGS) specification. Nature Biotechnol. 26, 541–547 (2008).
Markowitz, V. M. et al. An experimental metagenome data management and analysis system. Bioinformatics 22, e359–e367 (2006).
Seshadri, R., Kravitz, S. A., Smarr, L., Gilna, P. & Frazier, M. CAMERA: a community resource for metagenomics. PLoS Biol. 5, e75 (2007).
Kanehisa, M. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res. 34, D354–D357 (2006).
Letunic, I., Yamada, T., Kanehisa, M. & Bork, P. iPath: interactive exploration of biochemical pathways and networks. Trends Biochem. Sci. 33, 101–103 (2008).
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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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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DOI: https://doi.org/10.1038/nrmicro1935
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