4.5 Article

ASYMMETRIC, BIMODAL TRADE-OFFS DURING ADAPTATION OF METHYLOBACTERIUM TO DISTINCT GROWTH SUBSTRATES

Journal

EVOLUTION
Volume 63, Issue 11, Pages 2816-2830

Publisher

WILEY
DOI: 10.1111/j.1558-5646.2009.00757.x

Keywords

Experimental evolution; metabolism; methylotrophy; pleiotropy; specialization

Funding

  1. National Science Foundation [DBI-0301202, IOB-0612591]
  2. Clark/Cooke Fund
  3. Harvard University

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Trade-offs between selected and nonselected environments are often assumed to exist during adaptation. This phenomenon is prevalent in microbial metabolism, where many organisms have come to specialize on a narrow breadth of substrates. One well-studied example is methylotrophic bacteria that can use single-carbon (C-1) compounds as their sole source of carbon and energy, but generally use few, if any, multi-C compounds. Here, we use adaptation of experimental populations of the model methylotroph, Methylobacterium extorquens AM1, to C-1 (methanol) or multi-C (succinate) compounds to investigate specialization and trade-offs between these two metabolic lifestyles. We found a general trend toward trade-offs during adaptation to succinate, but this was neither universal nor showed a quantitative relationship with the extent of adaptation. After 1500 generations, succinate-evolved strains had a remarkably bimodal distribution of fitness values on methanol: either an improvement comparable to the strains adapted on methanol or the complete loss of the ability to grow on C-1 compounds. In contrast, adaptation to methanol resulted in no such trade-offs. Based on the substantial, asymmetric loss of C-1 growth during growth on succinate, we suggest that the long-term maintenance of C-1 metabolism across the genus Methylobacterium requires relatively frequent use of C-1 compounds to prevent rapid loss.

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