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Evolution of organismal stoichiometry in a long-term experiment with Escherichia coli.

ABSTRACT: Organismal stoichiometry refers to the relative proportion of chemical elements in the biomass of organisms, and it can have important effects on ecological interactions from population to ecosystem scales. Although stoichiometry has been studied extensively from an ecological perspective, much less is known about the rates and directions of evolutionary changes in elemental composition. We measured carbon, nitrogen and phosphorus content of 12 Escherichia coli populations that evolved under controlled carbon-limited, serial-transfer conditions for 50?000 generations. The bacteria evolved higher relative nitrogen and phosphorus content, consistent with selection for increased use of the more abundant elements. Total carbon assimilated also increased, indicating more efficient use of the limiting element. We also measured stoichiometry in one population repeatedly through time. Stoichiometry changed more rapidly in early generations than later on, similar to the trajectory seen for competitive fitness. Altogether, our study shows that stoichiometry evolved over long time periods, and that it did so in a predictable direction, given the carbon-limited environment.

SUBMITTER: Turner CB

PROVIDER: S-EPMC5541568 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

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Evolution of organismal stoichiometry in a long-term experiment with <i>Escherichia coli</i>.

Turner Caroline B CB Wade Brian D BD Meyer Justin R JR Sommerfeld Brooke A BA Lenski Richard E RE

Royal Society open science 20170719 7

Organismal stoichiometry refers to the relative proportion of chemical elements in the biomass of organisms, and it can have important effects on ecological interactions from population to ecosystem scales. Although stoichiometry has been studied extensively from an ecological perspective, much less is known about the rates and directions of evolutionary changes in elemental composition. We measured carbon, nitrogen and phosphorus content of 12 <i>Escherichia coli</i> populations that evolved un ...[more]

PMID: 28791173

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Project description:UNLABELLED:Large-scale rearrangements may be important in evolution because they can alter chromosome organization and gene expression in ways not possible through point mutations. In a long-term evolution experiment, twelve Escherichia coli populations have been propagated in a glucose-limited environment for over 25 years. We used whole-genome mapping (optical mapping) combined with genome sequencing and PCR analysis to identify the large-scale chromosomal rearrangements in clones from each population after 40,000 generations. A total of 110 rearrangement events were detected, including 82 deletions, 19 inversions, and 9 duplications, with lineages having between 5 and 20 events. In three populations, successive rearrangements impacted particular regions. In five populations, rearrangements affected over a third of the chromosome. Most rearrangements involved recombination between insertion sequence (IS) elements, illustrating their importance in mediating genome plasticity. Two lines of evidence suggest that at least some of these rearrangements conferred higher fitness. First, parallel changes were observed across the independent populations, with ~65% of the rearrangements affecting the same loci in at least two populations. For example, the ribose-utilization operon and the manB-cpsG region were deleted in 12 and 10 populations, respectively, suggesting positive selection, and this inference was previously confirmed for the former case. Second, optical maps from clones sampled over time from one population showed that most rearrangements occurred early in the experiment, when fitness was increasing most rapidly. However, some rearrangements likely occur at high frequency and may have simply hitchhiked to fixation. In any case, large-scale rearrangements clearly influenced genomic evolution in these populations. IMPORTANCE:Bacterial chromosomes are dynamic structures shaped by long histories of evolution. Among genomic changes, large-scale DNA rearrangements can have important effects on the presence, order, and expression of genes. Whole-genome sequencing that relies on short DNA reads cannot identify all large-scale rearrangements. Therefore, deciphering changes in the overall organization of genomes requires alternative methods, such as optical mapping. We analyzed the longest-running microbial evolution experiment (more than 25 years of evolution in the laboratory) by optical mapping, genome sequencing, and PCR analyses. We found multiple large genome rearrangements in all 12 independently evolving populations. In most cases, it is unclear whether these changes were beneficial themselves or, alternatively, hitchhiked to fixation with other beneficial mutations. In any case, many genome rearrangements accumulated over decades of evolution, providing these populations with genetic plasticity reminiscent of that observed in some pathogenic bacteria.

Dataset Information

Evolution of organismal stoichiometry in a long-term experiment with Escherichia coli.

Publications

Evolution of organismal stoichiometry in a long-term experiment with <i>Escherichia coli</i>.

Similar Datasets

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