Community-integrated omics links dominance of a microbial generalist to fine-tuned resource usage

Microbial communities are complex and dynamic systems that are primarily structured
according to their members’ ecological niches. To investigate how niche breadth (generalist
versus specialist lifestyle strategies) relates to ecological success, we develop and apply an
integrative workflow for the multi-omic analysis of oleaginous mixed microbial communities
from a biological wastewater treatment plant. Time- and space-resolved coupled metabolomic
and taxonomic analyses demonstrate that the community-wide lipid accumulation
phenotype is associated with the dominance of the generalist bacterium Candidatus Microthrix
spp. By integrating population-level genomic reconstructions (reflecting fundamental
niches) with transcriptomic and proteomic data (realised niches), we identify finely tuned
gene expression governing resource usage by Candidatus Microthrix parvicella over time.
Moreover, our results indicate that the fluctuating environmental conditions constrain the
accumulation of genetic variation in Candidatus Microthrix parvicella likely due to fitness
trade-offs. Based on our observations, niche breadth has to be considered as an important
factor for understanding the evolutionary processes governing (microbial) population sizes
and structures in situ.