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

Abstract

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.