Abstract
Genomic data has revealed that genotypic variants of the same species, that is, strains, coexist and are abundant in natural microbial communities. However, it is not clear if strains are ecologically equivalent, and at what characteristic genetic distance they might exhibit distinct interactions and dynamics. Here, we address this problem by tracking 10 taxonomically diverse microbial communities from the pitcher plant Sarracenia purpurea in the laboratory for more than 300 generations. Using metagenomic sequencing, we reconstruct their dynamics over time and across scales, from distant phyla to closely related genotypes. We find that most strains are not ecologically equivalent and exhibit distinct dynamical patterns, often being significantly more correlated with strains from another species than their own. Although even a single mutation can affect laboratory strains, on average, natural strains typically decouple in their dynamics beyond a genetic distance of 100 base pairs. Using mathematical consumer-resource models, we show that these taxonomic patterns emerge naturally from ecological interactions between community members, but only if the interactions are coarse-grained at the level of strains, not species. Finally, by analyzing genomic differences between strains, we identify major functional hubs such as transporters, regulators, and carbohydrate-catabolizing enzymes, which might be the basis for strain-specific interactions. Our work suggests that fine-scale genetic differences in natural communities could be created and stabilized via the rapid diversification of ecological interactions between strains.
Highlights
In nature, microbial communities contain individuals on a continuum of phylogenetic diversity, 33 where both evolutionarily distant and proximate members coexist [1, 2]
We found that strains, which were pre-existing genetic variants belonging to the same species, were the key determinants of long-term community dynamics
Once the communities settled into unique equilibria, we found that the dynamics of even extremely closely related strains, with as few as 100 single nucleotide polymorphisms (SNPs), could be decoupled from each other
Summary
Microbial communities contain individuals on a continuum of phylogenetic diversity, 33 where both evolutionarily distant and proximate members coexist [1, 2]. Closely and distantly related community members perform many vital ecological functions such as the regulation of biogeochemical cycles and fiber digestion in animal guts [7, 8] Identifying how these different levels of diversity interact and co-evolve in complex communities remains an elusive and challenging problem. A common strategy to study this problem is to analyze the dynamics of complex communities at different levels of diversity with metagenomic sequence data Such data have been successfully leveraged to reconstruct the linkage between polymorphic sites in natural microbial populations, effectively allowing one to resolve both species and strain abundances [9,10,11,12]. By studying multiple communities domesticated in parallel in the same abiotic environment , we can disentangle which observations about community dynamics are repeatable and general, and which ones are chance and context-specific
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