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Kinnersley, M.

Publications and source records attributed to Kinnersley, M..

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Fitness and productivity increase with ecotypic diversity among E. coli evolved in a simple, constant environment

Community productivity often correlates with diversity. In the microbial world this phenomenon can sometimes be explained by highly-specific metabolic interactions that include cross-feeding and syntrophy. Such interactions help account for the astonishing variety of microbial life, and drive many of the biogeochemical cycles without which life as we know it could not exist. While it is difficult to recapitulate experimentally how these interactions evolved among multiple taxa, we can explore in the laboratory how they arise within one. These experiments provide insight into how different bacterial ecotypes evolve and from these, possibly new species. We have previously shown that in a simple, constant environment a single clone of E. coli can give rise to a consortium of genetically-and physiologically-differentiated strains, in effect, a set of ecotypes, that coexist by cross-feeding. We marked these different ecotypes and their shared ancestor by integrating fluorescent protein into their genomes. We then used flow cytometry to show that each strain by itself is more fit than the shared ancestor, that pairs of evolved strains are fitter still, and that the entire consortium is fittest of all. We further demonstrate that the rank order of fitness values agrees with estimates of yield, indicating that an experimentally evolved consortium more efficiently converts resources to offspring than its ancestor or any member acting in isolation.\n\nImportanceIn the microbial world, diversity and productivity of communities and consortia often correlate positively. However, it is challenging to tease apart a consortium whose members have co-evolved, and connect estimates of their fitness and the fitness of their ancestor(s) with estimates of productivity. Such analyses are prerequisite to understanding the evolutionary origins of all biological communities. Here we dissect an E. coli consortium that evolved in the laboratory and show that cooperative interactions are favored under continuous glucose limitation because a partnership of ecotypes is better able to scavenge all available resources and more efficiently convert those resources to offspring than any single individual. Such interactions may be a prelude to a special form of syntrophy, and are likely to be key determinants of microbial community structure in nature, including those having clinical significance, such as chronic infections.

microbiology

Evolutionary dynamics of de novo mutations and mutant lineages arising in a simple, constant environment

A large, asexual population founded by a single clone evolves into a population teeming with many, whether or not its environment is structured, and whether or not resource levels are constant or fluctuating. The maintenance of genetic complexity in such populations has been attributed to balancing selection, or to either clonal interference or clonal reinforcement, arising from antagonistic or synergistic interactions, respectively. To distinguish among these possibilities, to identify targets of selection and establish when and how often they are hit, as well as to gain insight into how de novo mutations interact, we carried out 300-500 generation glucose-limited chemostat experiments founded by an E. coli mutator. To discover all de novo mutations reaching [≥]1% frequency, we performed whole-genome, whole-population sequencing at [~]1000X-coverage every 50 generations. To establish linkage relationships among these mutations and depict the dynamics of evolving lineages we sequenced the genomes of 96 clones from each population when allelic diversity was greatest. Operon-specific mutations that enhance glucose uptake arose to high frequency first, followed by global regulatory mutations. Late-arising mutations were related to energy conservation as well as to mitigating pleiotropic effects wrought by earlier regulatory changes. We discovered extensive polymorphism at relatively few loci, with identical mutations arising independently in different lineages, both between and within replicate populations. Out of more than 3,000 SNPs detected in nearly 1,800 genes or intergenic regions, only 17 reached a frequency [≥] 98%, indicating that the evolutionary dynamics of adaptive lineages was dominated by clonal interference. Finally, our data show that even when mutational input is increased by an ancestral defect in DNA repair, the spectrum of beneficial mutations that reach high frequency in a simple, constant resource-limited environment is narrow, resulting in extreme parallelism where many adaptive mutations arise but few ever go to fixation. Author SummaryMicrobial evolution experiments open a window on the tempo and dynamics of evolutionary change in asexual populations. High-throughput sequencing can be used to catalog de novo mutations, determine in which lineages they arise, and assess allelic interactions by tracking the fate of those lineages. This adaptive genetics approach makes it possible to discover whether clonal interactions are antagonistic or synergistic, and complements genetic screens of induced deleterious/loss-of-function mutants. We carried out glucose-limited chemostat experiments founded by an E. coli mutator and performed whole-genome, whole-population sequencing on 300-500 generation evolutions, cataloging 3,346 de novo mutations that reached [≥]1% frequency. Mutations enhancing glucose uptake rose to high frequency first, followed by global regulatory changes that modulate growth rate and limiting resource assimilation, then by mutations that favor energy conservation or mitigate pleiotropic effects of earlier regulatory changes. We discovered that a few loci were highly polymorphic, with identical mutations arising independently in different lineages, both between and within replicate populations. Thus, when mutational input is increased by an ancestral defect in DNA repair, the spectrum of beneficial mutations that arises under constant resource-limitation is narrow, resulting in extreme parallelism where many adaptive mutations arise but few ever become fixed.

evolutionary biology