Low-level resource partitioning supports coexistence among functionally redundant bacteria during successional dynamics

Abstract Members of microbial communities can substantially overlap in substrate use. However, what enables functionally redundant microorganisms to co-assemble or even stably coexist remains poorly understood. Here, we show that during unstable successional dynamics on complex, natural organic matter, functionally redundant bacteria can co-exist by partitioning low-concentration substrates even though they compete for one simple, dominant substrate. We allowed ocean microbial communities to self-assemble on leachates of the brown seaweed Fucus vesiculosus (FL), and then analyzed competition among 10 taxonomically diverse isolates representing two distinct stages of the succession. All but two isolates exhibited an average of 90 ± 6% pairwise overlap in resource use, and functional redundancy of isolates from the same assembly stage was higher than that from between assembly stages, leading us to construct a simpler 4-isolate community with 2 isolates from each of the early and late stages. We found that although the short-term dynamics of the 4-isolate communities in FL was dependent on initial isolate ratios, in the long term the 4 isolates stably coexist in FL, albeit with some strains at low abundance. We therefore explored potential for non-redundant substrate use by genomic content analysis and RNA expression patterns. This analysis revealed that the 4 isolates mainly differed in peripheral metabolic pathways, such as the ability to degrade pyrimidine, leucine, and tyrosine, as well as aromatic substrates. These results highlight the importance of fine-scale differences in metabolic strategies for supporting the frequently observed coexistence of large numbers of rare organisms in natural microbiomes.