Gabriel E. Leventhal
Profile Url: gabriel-e--leventhal
Researcher at Department of Civil and Environmental Engineering, Massachusetts Institute of Technology
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Nature Microbiology, 2018-09-24
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Nature Microbiology
Microbial communities are often highly diverse in their composition, both at the level of coarse-grained taxa such as genera as well as at the level of strains within species. This variability can be driven by both extrinsic factors like temperature, pH, etc., as well as by intrinsic ones, such as demographic fluctuations or ecological interactions. The relative contributions of these factors and the taxonomic level at which they influence community structure remain poorly understood, in part because of the difficulty of identifying true community replicates assembled under the same environmental parameters. Here, we address this problem using an activated granular sludge reactor in which millimeter scale biofilm granules represent true community replicates whose differences in composition are expected to be driven primarily by biotic factors. Using 142 shotgun metagenomes of single biofilm granules we found that, at the commonly used genus-level resolution, community replicates varied much more in their composition than would be expected from neutral assembly processes. This variation, however, did not translate into any clear partitioning into discrete community types, i.e. the equivalent of enterotypes in the human gut. However, a strong partition into community types did emerge at the strain level for the most abundant organism: strains of Candidatus Accumulibacter that coexisted in the metacommunity---i.e. the reactor---excluded each other within community replicates. Single-granule communities maintained a significant lineage structure, whereby the strain phylogeny of Accumulibacter correlated with the overall species composition of the community, indicating high potential for co-diversification among species and communities. Our results suggest that due to the high functional redundancy and competition between close relatives, alternative community types are most likely observed at the level of recently differentiated genotypes but not higher orders of genetic resolution.
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Niche construction through interspecific interactions can condition future community states on past ones. However, the extent to which such history dependency can steer communities towards functionally different states remains a subject of active debate. Using bacterial communities collected from wild pitchers of the carnivorous pitcher plant, Sarracenia purpurea , we tested the effects of history on composition and function across communities assembled in synthetic pitcher plant microcosms. We found that the diversity of assembled communities was determined by the diversity of the system at early, pre-assembly stages. Species composition was also contingent on early community states, not only because of differences in the species pool, but also because the same species had different dynamics in different community contexts. Importantly, compositional differences were proportional to differences in function, as profiles of resource use were strongly correlated with composition, despite convergence in respiration rates. Early differences in community structure can thus propagate to mature communities, conditioning their functional repertoire.
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Nature Communications, 2018-07-16
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Nature Communications
The degradation of particulate organic matter in the ocean is a central process in the global carbon cycle, the "mode and tempo" of which is determined by the bacterial communities that assemble on particle surfaces. Although recent studies have shed light on the dynamics of community assembly on particles -which serve as hotspots of microbial activity in the ocean, the mapping from community composition to function, i.e. particle degradation, remains completely unexplored. Using a collection of marine bacteria cultured from different stages of succession on chitin micro-particles we found that the hydrolytic power of communities is highly dependent on community composition. Different particle degrading taxa, all of which were early successional species during colonization, displayed characteristic particle half-lives that differed by ~170 hours, comparable to the residence time of particles in the ocean's mixed layer. These half-lives were in general longer in multispecies communities, where the growth of obligate cross-feeders limited the ability of degraders to colonize and consume particles. Remarkably, above a certain critical initial ratio of cross-feeder to degrader cells, particle degradation was completely blocked along with the growth of all members of the community. We showed that this interaction occurred between a variety of strains of different taxonomic origins and that it only appears when bacteria interact with particles, suggesting a mechanism by which non-degrading secondary consumers occlude access to the particle resource. Overall, our results show that micro-scale community ecology on particle surfaces can have significant impact on carbon turnover in the ocean.
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Supplementary Material
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Genomic data has revealed that genotypic variants of the same species, i.e., strains, coexist and are abundant in natural microbial communities. However, it is not clear if strains are ecologically equivalent, or if they exhibit distinct interactions and dynamics. Here, we address this problem by tracking 10 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 interactions between naturally occurring strains govern eco-evolutionary dynamics. Surprisingly, even fine-scale variants differing only by 100 base pairs can exhibit vastly different dynamics. We show that these differences may stem from ecological interactions in the communities, which are specific to 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 shows that strains are the relevant level of diversity at which to study the long-term dynamics of microbiomes.