Fine-scale diversity of microbial communities due to satellite niches in boom-and-bust environments

Abstract

Recent observations have revealed that closely related strains of the same microbial species can stably coexist in natural and laboratory settings subject to boom-and-bust dynamics and serial dilutions, respectively. However, the possible mechanisms enabling the coexistence of only a handful of strains, but not more, have thus far remained unknown. Here, using a consumer-resource model of microbial ecosystems, we propose that by differentiating on Monod parameters characterizing microbial growth rates in high and low nutrient conditions, strains can coexist in patterns similar to those observed. In our model, boom-and-bust environments create satellite niches due to resource concentrations varying in time. These satellite niches can be occupied by closely related strains, thereby enabling their coexistence. We demonstrate that this result is valid even in complex environments consisting of multiple resources and species. In these complex communities, each species partitions resources differently and creates separate sets of satellite niches for their own strains. While there is no theoretical limit to the number of coexisting strains, in our simulations, we always find between 1 and 3 strains coexisting, consistent with experiments and observations. Author summaryRecent genomic data has exposed to us the remarkable spectrum of microbial diversity in natural communities surrounding us, which harbor not only hundreds of species, but also a handful of closely related strains within each of those species (termed "oligo-colonization"). While the mechanisms behind species coexistence are much better studied, the mechanisms behind the coexistence of closely related strains have remained understudied. Here, using a simple consumer-resource model, we show that if strains differ on their Monod growth parameters, they can coexist even on a single limiting resource, provided that the environments vary with time in boom-and-bust cycles. The Monod growth parameters describe how a strains growth rate changes with resource concentration, namely the half-maximal concentration and maximal growth rate. Simulations of our model show that both in simple and complex environments, even though an arbitrary number of strains can coexist, typically it is between 1 and 3 strains of a species that coexist over several randomly assembled communities, consistent with some experimental observations. This is because the allowed parameter space for coexistence shrinks significantly with the number of strains that coexist.