Strain-level diversity drives alternative community types in millimeter scale granular biofilms

Microbial communities that perform important biogeochemical, host-metabolic and bioengineering processes are often highly diverse in their composition, both at the level of coarse-grained taxa (e.g. genera) as well as at the level of strains within species. This variability can be driven by both extrinsic factors---like differences in abiotic conditions---and intrinsic ones---such as demographic fluctuations or ecological interactions. The relative contribution of these factors and the taxonomic level at which they influence community structure remain, however, poorly understood. Here, we exploit the meta-community structure of an activated granular sludge reactor to ask how much and at what taxonomic resolution replicate island communities---represented by millimeter-scale biofilm granules---differ between each other when assembled from the same species pool and in the same abiotic environment. Using 142 metagenomes from single biofilm granules we found that at the commonly used genus-level resolution community islands varied much more in their composition than would be expected from neutral assembly processes but without any clear partitioning into discrete community types. However, a strong partition into community types emerged at the strain level: strains that coexisted in the meta-community---i.e. the reactor---excluded each other within islands, where they tended to form clonal populations. These island communities maintained a weak but significant lineage structure, whereby the strain phylogeny of the most abundant species was predictive of community composition at high taxonomic levels, indicating high potential for co-diversification among species and communities. Our results suggest that analysis of community types is highly sensitive to phylogenetic resolution and that---due to 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-levels of genetic resolution.