Chance and necessity in the evolution of minimal metabolic networks

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.

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

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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.

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Correspondence to Laurence D. Hurst.

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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)

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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

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