Skip to main content

Reverse Ecology: From Systems to Environments and Back

  • Chapter
  • First Online:
Evolutionary Systems Biology

Part of the book series: Advances in Experimental Medicine and Biology ((volume 751))

Abstract

The structure of complex biological systems reflects not only their function but also the environments in which they evolved and are adapted to. Reverse Ecology—an emerging new frontier in Evolutionary Systems Biology—aims to extract this information and to obtain novel insights into an organism’s ecology. The Reverse Ecology framework facilitates the translation of high-throughput genomic data into large-scale ecological data, and has the potential to transform ecology into a high-throughput field. In this chapter, we describe some of the pioneering work in Reverse Ecology, demonstrating how system-level analysis of complex biological networks can be used to predict the natural habitats of poorly characterized microbial species, their interactions with other species, and universal patterns governing the adaptation of organisms to their environments. We further present several studies that applied Reverse Ecology to elucidate various aspects of microbial ecology, and lay out exciting future directions and potential future applications in biotechnology, biomedicine, and ecological engineering.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Ungerer MC, Johnson LC, Herman MA (2008) Ecological genomics: understanding gene and genome function in the natural environment. Heredity 100(2):178–183. doi:10.1038/sj.hdy.6800992

    Article  PubMed  CAS  Google Scholar 

  2. Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ (2004) Bmp4 and morphological variation of beaks in Darwin’s finches. Science 305:1462–1465. doi:10.1126/science.1098095

    Article  PubMed  CAS  Google Scholar 

  3. Abzhanov A, Kuo WP, Hartmann C, Grant BR, Grant PR, Tabin CJ (2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin’s finches. Nature 442: 563–567. doi:10.1038/nature04843

    Article  PubMed  CAS  Google Scholar 

  4. Ellison CE et al (2011) Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc Natl Acad Sci USA 108:2831–2836. doi:10.1073/pnas.1014971108

    Article  PubMed  CAS  Google Scholar 

  5. Borenstein E, Kupiec M, Feldman MW, Ruppin E (2008) Large-scale reconstruction and phylogenetic analysis of metabolic environments. Proc Natl Acad Sci USA 105:14482–14487. doi:10.1073/pnas.0806162105

    Article  PubMed  CAS  Google Scholar 

  6. Aho A, Hopcroft J, Ullman J (1974) The design and analysis of computer algorithms. Addison-Wesley, Reading, MA

    Google Scholar 

  7. Horowitz NH (1945) On the evolution of biochemical syntheses. Proc Natl Acad Sci USA 31:153

    Article  PubMed  CAS  Google Scholar 

  8. Ebenhöh O, Handorf T, Heinrich R (2004) Structural analysis of expanding metabolic networks. Genome Inform 15:35–45; International Conference on Genome Informatics

    Google Scholar 

  9. Kruse K, Ebenhöh O (2008) Comparing flux balance analysis to network expansion: producibility, sustainability and the scope of compounds. Genome Inform 20:91–101; International Conference on Genome Informatics

    Google Scholar 

  10. De Visser J et al (2003) Perspective: evolution and detection of genetic robustness. Evol, Int J Org Evol 57:1959–1972

    Article  Google Scholar 

  11. Freilich S et al (2010) Decoupling environment-dependent and independent genetic robustness across bacterial species. PLoS Comp Biol 6:e1000690. doi:10.1371/journal.pcbi.1000690

    Article  Google Scholar 

  12. Raymond J, Segrè D (2006) The effect of oxygen on biochemical networks and the evolution of complex life. Science 311:1764–1767. doi:10.1126/science.1118439

    Article  PubMed  CAS  Google Scholar 

  13. Dale C, Moran NA (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126(3):453–465. doi:10.1016/j.cell.2006.07.014

    Article  PubMed  CAS  Google Scholar 

  14. Borenstein E, Feldman MW (2009) Topological signatures of species interactions in metabolic networks. J Comput Biol 16:191–200. doi:10.1089/cmb.2008.06TT

    Article  PubMed  CAS  Google Scholar 

  15. Trosvik P et al (2010) Web of ecological interactions in an experimental gut microbiota. Environ Microbiol 12(10):2677–2687. doi:10.1111/j.1462-2920.2010.02236.x

    PubMed  CAS  Google Scholar 

  16. Freilich S et al (2009) Metabolic-network-driven analysis of bacterial ecological strategies. Genome Biol 10:R61. doi:10.1186/gb-2009-10-6-r61

    Article  PubMed  Google Scholar 

  17. Freilich S et al (2010) The large-scale organization of the bacterial network of ecological co-occurrence interactions. Nucleic Acids Res 38:3857–3868. doi:10.1093/nar/gkq118

    Article  PubMed  CAS  Google Scholar 

  18. Edwards JS, Palsson BO (2000) Metabolic flux balance analysis and the in silico analysis of Escherichia coli K-12 gene deletions. BMC Bioinformatics 1:1

    Article  PubMed  CAS  Google Scholar 

  19. Reed J, Palsson BØ (2003) Thirteen years of building constraint-based in silico models of Escherichia coli. J Bacteriol 185:2692–2699. doi:10.1128/JB.185.9.2692

    Article  PubMed  CAS  Google Scholar 

  20. Thiele I, Palsson BØ (2010) A protocol for generating a high-quality genome-scale metabolic reconstruction. Nat Protocol 5:93–121. doi:10.1038/nprot.2009.203

    Article  CAS  Google Scholar 

  21. Stolyar S et al (2007) Metabolic modeling of a mutualistic microbial community. Mol Syst Biol 3:92. doi:10.1038/msb4100131

    Article  PubMed  Google Scholar 

  22. Wintermute EH, Silver PA (2010) Emergent cooperation in microbial metabolism. Mol Syst Biol 6:407. doi:10.1038/msb.2010.66

    Article  PubMed  Google Scholar 

  23. Klitgord N, Segrè D (2010) Environments that induce synthetic microbial ecosystems. PLoS Comp Biol 6:e1001002. doi:10.1371/journal.pcbi.1001002

    Article  Google Scholar 

  24. Hartwell LH et al (1999) From molecular to modular cell biology. Nature 402:6761. doi:10.1038/35011540

    Article  Google Scholar 

  25. Parter M, Kashtan N, Alon U (2007) Environmental variability and modularity of bacterial metabolic networks. BMC Evol Biol 7:169. doi:10.1186/1471-2148-7-169

    Article  PubMed  Google Scholar 

  26. Kreimer A, Borenstein E, Gophna U, Ruppin E (2008) The evolution of modularity in bacterial metabolic networks. Proc Natl Acad Sci USA 105:6976–6981. doi:10.1073/pnas.0712149105

    Article  PubMed  CAS  Google Scholar 

  27. Kashtan N, Alon U (2005) Spontaneous evolution of modularity and network motifs. Proc Natl Acad Sci USA 102:13773–13778. doi:10.1073/pnas.0503610102

    Article  PubMed  CAS  Google Scholar 

  28. Kashtan N et al (2009) An analytically solvable model for rapid evolution of modular structure. PLoS Comp Biol 5:e1000355 doi:10.1371/journal.pcbi.1000355

    Article  Google Scholar 

  29. Soyer OS, Pfeiffer T (2010) Evolution under fluctuating environments explains observed robustness in metabolic networks. PLoS Comp Biol 6:8. doi:10.1371/journal.pcbi.1000907

    Article  Google Scholar 

  30. Ostrowski E, Ofria C, Lenski RE (2007) Ecological specialization and adaptive decay in digital organisms. Am Nat 169:E1–E20

    Article  PubMed  Google Scholar 

  31. Kyrpides NC (2009) Fifteen years of microbial genomics: meeting the challenges and fulfilling the dream. Nat Biotechnol 27:627–632

    Article  PubMed  CAS  Google Scholar 

  32. Chalmers NI, Palmer RJ, Cisar JO, Kolenbrander PE (2008) Characterization of a Streptococcus sp.-Veillonella sp. community micromanipulated from dental plaque. J Bacteriol 190:8145–8154. doi:10.1128/JB.00983-08

    Google Scholar 

  33. Shou W, Ram S, Vilar JMG (2007) Synthetic cooperation in engineered yeast populations. Proc Natl Acad Sci USA 104:1877–1882. doi:10.1073/pnas.0610575104

    Article  PubMed  CAS  Google Scholar 

  34. Torsvik V, Øvreås L, Thingstad TF (2002) Prokaryotic diversity-magnitude, dynamics, and controlling factors. Science 296:1064–1066. doi:10.1126/science.1071698

    Article  PubMed  CAS  Google Scholar 

  35. Schloss PD, Handelsman J (2005) Metagenomics for studying unculturable microorganisms: cutting the Gordian knot. Genome Biol 6:229

    Article  PubMed  Google Scholar 

  36. Schink B, Stams AJM (2006) Syntrophism among prokaryotes. In: Dworkin M et al (ed) The prokaryotes: an evolving electronic resource for the microbiological community, vol 2. Springer, New York

    Google Scholar 

  37. Little AEF, Robinson CJ, Peterson SB, Raffa KF, Handelsman J (2008) Rules of engagement: interspecies interactions that regulate microbial communities. Annu Rev Microbiol 62: 375–401

    Article  PubMed  CAS  Google Scholar 

  38. McInerney MJ, Sieber JR, Gunsalus RP (2009) Syntrophy in anaerobic global carbon cycles. Curr Opin Biotechnol 20:623–632

    Article  PubMed  CAS  Google Scholar 

  39. Douglas A (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Ann Rev Entomol 43:17–37

    Article  CAS  Google Scholar 

  40. Lodwig E, Poole P (2003) Metabolism of Rhizobium bacteroids. Crit Rev Plant Sci 22:37–78

    Article  CAS  Google Scholar 

  41. Turnbaugh PJ et al (2007) The human microbiome project. Nature 449:804–810. doi:10.1038/nature06244

    Article  PubMed  CAS  Google Scholar 

  42. Vartoukian SR, Palmer RM, Wade WG (2010) Strategies for culture of ‘unculturable’ bacteria. FEMS Microbiol Lett 309(1):1–7. doi:10.1111/j.1574-6968.2010.02000.x

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  44. Gordon JI, Klaenhammer TR (2011) A rendezvous with our microbes. Proc Natl Acad Sci USA 108 Suppl 1:4513–4515. doi:10.1073/pnas.1101958108

    Article  PubMed  CAS  Google Scholar 

  45. Lederberg J (2000) Infectious history. Science 288:287–293. doi:10.1126/science. 288.5464.287

    Article  PubMed  CAS  Google Scholar 

  46. Greenblum S, Turnbaugh PJ, Borenstein E (2012). Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc Natl Acad Sci USA 109:594–599. doi:10.1073/pnas.1116053109

    Article  PubMed  CAS  Google Scholar 

  47. Khalil AS, Collins JJ (2010) Synthetic biology: applications come of age. Nat Rev Genet 11(5):367–379. doi:10.1038/nrg2775

    Article  PubMed  CAS  Google Scholar 

  48. Janga SC, Babu MM (2008) Network-based approaches for linking metabolism with environment. Genome Biol 9:239. doi:10.1186/gb-2008-9-11-239

    Article  PubMed  Google Scholar 

  49. Röling WFM, Ferrer M, Golyshin PN (2010) Systems approaches to microbial communities and their functioning. Curr Opin Biotechnol 21:532–538. doi:10.1016/j.copbio.2010.06.007

    Article  PubMed  Google Scholar 

  50. Brenner K, You L, Arnold FH (2008) Engineering microbial consortia: a new frontier in synthetic biology. Trends Biotechnol 26(9):483–489. doi:10.1016/j.tibtech.2008.05.004

    Article  PubMed  CAS  Google Scholar 

  51. Hansen EE et al (2011) Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii, studied in twins. Proc Natl Acad Sci USA 108 Suppl 1: 4599–4606. doi:10.1073/pnas.1000071108

    Article  PubMed  CAS  Google Scholar 

  52. Khoruts A et al (2010). Changes in the composition of the human fecal microbiome after bacteriotherapy for recurrent Clostridium difficile-associated diarrhea. J Clin Gastroenterol 44(5):354–360

    PubMed  Google Scholar 

  53. Rosenblueth A, Wiener N (1945) The role of models in science. Phil Sci 12:316–321

    Article  Google Scholar 

  54. Henry CS et al (2010) High-throughput generation, optimization and analysis of genome-scale metabolic models. Nat Biotechnol 28:969–974

    Article  Google Scholar 

  55. Mahowald MA et al (2009) Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc Natl Acad Sci USA 106:5859–5864. doi:10.1073/pnas.0901529106

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elhanan Borenstein .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Levy, R., Borenstein, E. (2012). Reverse Ecology: From Systems to Environments and Back. In: Soyer, O. (eds) Evolutionary Systems Biology. Advances in Experimental Medicine and Biology, vol 751. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-3567-9_15

Download citation

Publish with us

Policies and ethics