Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Chance and necessity in the evolution of minimal metabolic networks

Nature volume 440, pages 667–670 (2006)Cite this article

Abstract

It is possible to infer aspects of an organism's lifestyle from its gene content1. Can the reverse also be done? Here we consider this issue by modelling evolution of the reduced genomes of endosymbiotic bacteria. The diversity of gene content in these bacteria may reflect both variation in selective forces and contingency-dependent loss of alternative pathways. Using an in silico representation of the metabolic network of Escherichia coli, we examine the role of contingency by repeatedly simulating the successive loss of genes while controlling for the environment. The minimal networks that result are variable in both gene content and number. Partially different metabolisms can thus evolve owing to contingency alone. The simulation outcomes do preserve a core metabolism, however, which is over-represented in strict intracellular bacteria. Moreover, differences between minimal networks based on lifestyle are predictable: by simulating their respective environmental conditions, we can model evolution of the gene content in Buchnera aphidicola and Wigglesworthia glossinidia with over 80% accuracy. We conclude that, at least for the particular cases considered here, gene content of an organism can be predicted with knowledge of its distant ancestors and its current lifestyle.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: General properties of evolved minimal networks.
Figure 2: Comparison of reaction content of simulated and Buchnera metabolic networks.

Similar content being viewed by others

References

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

    Article  ADS  CAS  PubMed  Google Scholar 

  2. Koonin, E. V. Comparative genomics, minimal gene-sets and the last universal common ancestor. Nature Rev. Microbiol. 1, 127–136 (2003)

    Article  CAS  Google Scholar 

  3. Reed, J. L., Vo, T. D., Schilling, C. H. & Palsson, B. O. An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR). Genome Biol. 4, R54 (2003)

    Article  PubMed  PubMed Central  Google Scholar 

  4. Price, N. D., Reed, J. L. & Palsson, B. O. Genome-scale models of microbial cells: evaluating the consequences of constraints. Nature Rev. Microbiol. 2, 886–897 (2004)

    Article  CAS  Google Scholar 

  5. Edwards, J. S. & Palsson, B. O. The Escherichia coli MG1655 in silico metabolic genotype: its definition, characteristics, and capabilities. Proc. Natl Acad. Sci. USA 97, 5528–5533 (2000)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  6. Gil, R., Latorre, A. & Moya, A. Bacterial endosymbionts of insects: insights from comparative genomics. Environ. Microbiol. 6, 1109–1122 (2004)

    Article  CAS  PubMed  Google Scholar 

  7. Klasson, L. & Andersson, S. G. Evolution of minimal-gene-sets in host-dependent bacteria. Trends Microbiol. 12, 37–43 (2004)

    Article  CAS  PubMed  Google Scholar 

  8. Burgard, A. P., Vaidyaraman, S. & Maranas, C. D. Minimal reaction sets for Escherichia coli metabolism under different growth requirements and uptake environments. Biotechnol. Prog. 17, 791–797 (2001)

    Article  CAS  PubMed  Google Scholar 

  9. Moran, N. A. & Mira, A. The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol. 2, research0054 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y. & Ishikawa, H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407, 81–86 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  11. van Ham, R. C. et al. Reductive genome evolution in Buchnera aphidicola. Proc. Natl Acad. Sci. USA 100, 581–586 (2003)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  12. Tamas, I. et al. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296, 2376–2379 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  13. Akman, L. et al. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nature Genet. 32, 402–407 (2002)

    Article  CAS  PubMed  Google Scholar 

  14. Nakabachi, A. & Ishikawa, H. Provision of riboflavin to the host aphid, Acyrthosiphon pisum, by endosymbiotic bacteria, Buchnera. J. Insect Physiol. 45, 1–6 (1999)

    Article  CAS  PubMed  Google Scholar 

  15. Baumann, P. et al. Genetics, physiology, and evolutionary relationships of the genus Buchnera—intracellular symbionts of aphids. Ann. Rev. Microbiol. 49, 55–94 (1995)

    Article  CAS  Google Scholar 

  16. Hanley, J. A. & McNeil, B. J. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143, 29–36 (1982)

    Article  CAS  PubMed  Google Scholar 

  17. Kumari, S., Tishel, R., Eisenbach, M. & Wolfe, A. J. Cloning, characterization, and functional expression of acs, the gene which encodes acetyl coenzyme A synthetase in Escherichia coli. J. Bacteriol. 177, 2878–2886 (1995)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Zientz, E., Dandekar, T. & Gross, R. Metabolic interdependence of obligate intracellular bacteria and their insect hosts. Microbiol. Mol. Biol. Rev. 68, 745–770 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Nogge, G. Significance of symbionts for the maintenance of an optimal nutritional state for successful reproduction in haematophagous arthropods. Parasitology 82, 101–104 (1981)

    Google Scholar 

  20. Cormen, T. H., Leiserson, C. E., Rivest, R. L. & Stein, C. Introduction to Algorithms (MIT Press, Cambridge, MA, 2001)

    MATH  Google Scholar 

  21. Burgard, A. P., Nikolaev, E. V., Schilling, C. H. & Maranas, C. D. Flux coupling analysis of genome-scale metabolic network reconstructions. Genome Res. 14, 301–312 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Travisano, M., Mongold, J. A., Bennett, A. F. & Lenski, R. E. Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267, 87–90 (1995)

    Article  ADS  CAS  PubMed  Google Scholar 

  23. Mushegian, A. R. & Koonin, E. V. A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc. Natl Acad. Sci. USA 93, 10268–10273 (1996)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gil, R., Silva, F. J., Pereto, J. & Moya, A. Determination of the core of a minimal bacterial gene set. Microbiol. Mol. Biol. Rev. 68, 518–537 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Westers, H. et al. Genome engineering reveals large dispensable regions in Bacillus subtilis. Mol. Biol. Evol. 20, 2076–2090 (2003)

    Article  CAS  PubMed  Google Scholar 

  26. Kolisnychenko, V. et al. Engineering a reduced Escherichia coli genome. Genome Res. 12, 640–647 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hutchison, C. A. et al. Global transposon mutagenesis and a minimal Mycoplasma genome. Science 286, 2165–2169 (1999)

    Article  CAS  PubMed  Google Scholar 

  28. Nilsson, A. I. et al. Bacterial genome size reduction by experimental evolution. Proc. Natl Acad. Sci. USA 102, 12112–12116 (2005)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  29. Oliver, S. G. From DNA sequence to biological function. Nature 379, 597–600 (1996)

    Article  ADS  CAS  PubMed  Google Scholar 

  30. Mira, A. & Moran, N. A. Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb. Ecol. 44, 137–143 (2002)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank C. von Mering for providing early access to the updated STRING database. C.P., B.P. and P.C. are supported by the Hungarian Scientific Research Fund (OTKA). C.P. is also supported by an EMBO Long-term Fellowship. B.P. is a Fellow of the Human Frontier Science Program. M.J.L. acknowledges financial support by the Deutsche Forschungsgemeinschaft. Work on systems biology in S.G.O.'s laboratory is supported by the Biotechnology and Biological Sciences Research Council.

Author information

Author notes

  1. Csaba Pál and Balázs Papp: *These authors contributed equally to this work

Authors and Affiliations

  1. European Molecular Biology Laboratory, Meyerhofstrasse 1, D-69012, Heidelberg, Germany

    Csaba Pál & Martin J. Lercher

  2. Department of Zoology, University of Oxford, OX1 3PS, Oxford, UK

    Csaba Pál

  3. Faculty of Life Sciences, The University of Manchester, Michael Smith Building, Oxford Road, M13 9PT, Manchester, UK

    Balázs Papp & Stephen G. Oliver

  4. Department of Biology & Biochemistry, University of Bath, Claverton Down, BA2 7AY, Bath, UK

    Martin J. Lercher & Laurence D. Hurst

  5. Biochemistry, University of Bath, Claverton Down

    Martin J. Lercher & Laurence D. Hurst

  6. Department of Medical Chemistry, Semmelweis University, PO Box 260, H-1444, Budapest, Hungary

    Péter Csermely

Authors
  1. Csaba Pál
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Balázs Papp
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin J. Lercher
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Péter Csermely
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stephen G. Oliver
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Laurence D. Hurst
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laurence D. Hurst.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file contains the Supplementary Methods and Supplementary Tables 1–12. (DOC 760 kb)

Supplementary Table 13

Metabolic gene content of endosymbionts and simulated minimal genomes. (PDF 129 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pál, C., Papp, B., Lercher, M. et al. Chance and necessity in the evolution of minimal metabolic networks. Nature 440, 667–670 (2006). https://doi.org/10.1038/nature04568

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04568

This article is cited by

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.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing