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Evolution of a cross-feeding interaction following a key innovation in a long-term evolution experiment with Escherichia coli.

ABSTRACT: The evolution of a novel trait can profoundly change an organism's effects on its environment, which can in turn affect the further evolution of that organism and any coexisting organisms. We examine these effects and feedbacks following the evolution of a novel function in the Long-Term Evolution Experiment (LTEE) with Escherichia coli. A characteristic feature of E. coli is its inability to grow aerobically on citrate (Cit^-). Nonetheless, a Cit⁺ variant with this capacity evolved in one LTEE population after 31 000 generations. The Cit⁺ clade then coexisted stably with another clade that retained the ancestral Cit^- phenotype. This coexistence was shaped by the evolution of a cross-feeding relationship based on C₄-dicarboxylic acids, particularly succinate, fumarate, and malate, that the Cit⁺ variants release into the medium. Both the Cit^- and Cit⁺ cells evolved to grow on these excreted resources. The evolution of aerobic growth on citrate thus led to a transition from an ecosystem based on a single limiting resource, glucose, to one with at least five resources that were either shared or partitioned between the two coexisting clades. Our findings show that evolutionary novelties can change environmental conditions in ways that facilitate diversity by altering ecosystem structure and the evolutionary trajectories of coexisting lineages.

SUBMITTER: Turner CB

PROVIDER: S-EPMC10482366 | biostudies-literature | 2023 Aug

REPOSITORIES: biostudies-literature

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Evolution of a cross-feeding interaction following a key innovation in a long-term evolution experiment with Escherichia coli.

Turner Caroline B CB Blount Zachary D ZD Mitchell Daniel H DH Lenski Richard E RE

Microbiology (Reading, England) 20230801 8

The evolution of a novel trait can profoundly change an organism's effects on its environment, which can in turn affect the further evolution of that organism and any coexisting organisms. We examine these effects and feedbacks following the evolution of a novel function in the Long-Term Evolution Experiment (LTEE) with Escherichia coli. A characteristic feature of E. coli is its inability to grow aerobically on citrate (Cit-). Nonetheless, a Cit+ variant with ...[more]

PMID: 37650867

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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 a cross-feeding interaction following a key innovation in a long-term evolution experiment with Escherichia coli.

Publications

Evolution of a cross-feeding interaction following a key innovation in a long-term evolution experiment with <i>Escherichia coli</i>.

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