Low-Level Resource Partitioning Supports Coexistence Among Functionally Redundant Bacteria During Successional Dynamics

Members of microbial communities can substantially overlap in substrate use. However, what enables functionally redundant microorganisms to coassemble or even stably coexist remains poorly understood. Here, we show that during unstable successional dynamics on complex, natural organic matter, functionally redundant bacteria can coexist 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 and then analyzed the 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 four-isolate community with two isolates from each of the early and late stages. We found that, although the short-term dynamics of the four-isolate communities in F. vesiculosus leachate was dependent on initial isolate ratios, in the long term, the four isolates stably coexist in F. vesiculosus leachate, albeit with some strains at low abundance. We therefore explored the potential for nonredundant substrate use by genomic content analysis and RNA expression patterns. This analysis revealed that the four 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

<i>Prevotella copri</i> sub-species diversity in human gut microbiome samples (LifelinesDeep) and MIT sewage samples, as revealed by ten phylogenetic marker genes.

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Classifier performance of models utilizing gut microbiome taxon abundances.

Classifier performance of models utilizing gut microbiome taxon abundances.</p

<i>Bacteroides vulgatus</i> sub-species diversity in human gut microbiome samples (LifelinesDeep) and MIT sewage samples, as revealed by ten phylogenetic marker genes.

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An ideal sewage mixture simulation shows the potential of microbiome taxon abundance profiles as population census information sources.

(A) We generated an “ideal sewage mixture” consisting of gut microbiomes from different numbers of people. (B) Ranked abundance curves for gut microbiomes of one person and mixtures of multiple people exhibit different levels of dominance and diversity. Blue lines show the rank abundance curves in stool samples (one person), red lines show 10-person mixtures, and saffron lines show 100-person mixtures. In each scenario, ten examples are shown. All samples were rarefied to the same sequencing depths (4,000 seqs/sample). (C) The probability density function of the relative abundance of one taxon for different population sizes. OTU-2379, a Bifidobacterium taxon, was used as an example. Maroon dashed lines indicate the sample means. (D) Multiple taxa’s abundance variances in one-person samples and 100-person samples. The dominant taxa are shown (top100) and are sorted by their ranks in variance. (E) The ratios of the variances of one-person samples and 100-person samples across dominant gut microbial taxa.</p

Supplementary Texts.

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Correlation of sub-species diversity with population size revealed by simulation.

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Family-level taxa for taxonomic filter in model application.

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Sub-species diversity of bacteria prevalent in sewage samples.

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Performance of a cross-validated Random Forest regression model utilizing microbiome features to predict population size.

Black solid dots indicate the means of the predicted values, and error bars indicate the standard deviations of the predicted values. (TIFF)</p