Abstract
A major goal of genetics is to define the relationship between phenotype and genotype, while a major goal of ecology is to identify the rules that govern community assembly. Achieving these goals by analyzing natural systems can be difficult, as selective pressures create dynamic fitness landscapes that vary in both space and time. Laboratory experimental evolution offers the benefit of controlling variables that shape fitness landscapes, helping to achieve both goals. We previously showed that a clonal population of E. coli experimentally evolved under continuous glucose limitation gives rise to a genetically diverse community consisting of one clone, CV103, that best scavenges but incompletely utilizes the limiting resource, and others, CV101 and CV116, that consume its overflow metabolites. Because this community can be disassembled and reassembled, and involves cooperative interactions that are stable over time, its genetic diversity is sustained by clonal reinforcement rather than by clonal interference. To understand the genetic factors that produce this outcome, and to illuminate the community's underlying physiology, we sequenced the genomes of ancestral and evolved clones. We identified ancestral mutations in intermediary metabolism that may have predisposed the evolution of metabolic interdependence. Phylogenetic reconstruction indicates that the lineages that gave rise to this community diverged early, as CV103 shares only one Single Nucleotide Polymorphism with the other evolved clones. Underlying CV103's phenotype we identified a set of mutations that likely enhance glucose scavenging and maintain redox balance, but may do so at the expense of carbon excreted in overflow metabolites. Because these overflow metabolites serve as growth substrates that are differentially accessible to the other community members, and because the scavenging lineage shares only one SNP with these other clones, we conclude that this lineage likely served as an “engine” generating diversity by creating new metabolic niches, but not the occupants themselves.
Highlights
It is interesting to contemplate a tangled bank, clothed with many plants of many kinds, with birds singing on the bushes, with various insects flitting about, and with worms crawling through the damp earth, and to reflect that these elaborately constructed forms, so different from each other, and dependent upon each other in so complex a manner, have all been produced by laws acting around us
We previously showed that a population of E. coli that originated from a single clone and was cultured in the presence of a single limiting resource, evolves into a stable, three-membered community, wherein one clone excretes metabolites that the others utilize as carbon sources
We found that the lineages which gave rise to the community diverged early on, and that the numerically dominant lineage that best scavenges limiting glucose does so as a result of adaptive mutations that enhance glucose uptake but favor fermentative over respiratory pathways, resulting in overflow metabolites
Summary
It is interesting to contemplate a tangled bank, clothed with many plants of many kinds, with birds singing on the bushes, with various insects flitting about, and with worms crawling through the damp earth, and to reflect that these elaborately constructed forms, so different from each other, and dependent upon each other in so complex a manner, have all been produced by laws acting around us. Multiple genotypes that arise from a single ancestral clone can coexist over evolutionary time; in other words, ex uno plures (out of one many). This phenomenon has been documented in spatially and temporally unstructured chemostats [3,4], in temporally-structured batch cultures [5,6,7,8,9] and in spatially-structured microcosms [10]. In serial dilution batch culture, multiple growth parameters can come under selection [14]: different clones may arise having reduced lag time, increased maximum specific growth rate, or enhanced capacity to survive at high cell densities
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