Atypical distribution of SAR11 ecotypes in highly connected wetlands with strong salinity gradients

Ecotypes are key to understanding speciation in bacteria. They are defined as monophyletic subgroups of larger microbial clades that possess well-defined patterns in abundance dependent on distinct environmental conditions. The SAR11 clade is one of the few model systems to study ecotype variation and speciation in aquatic heterotrophic bacteria and is the only lineage that comprises significant populations in both freshwater and marine environments. In fact, one main driver of ecotype separation in this clade is salinity, but for most of the SAR11 ecotypes, e.g. the highly abundant open-ocean clades Ia and Ib, the environmental parameters and the consequential genetic and physiological adaptations that are responsible for divergent abundances are mostly unknown. SAR11 consists of five main clades that are present in freshwater, brackish, and oceanic waters, and multiple, but infrequent, transitions from freshwater to marine and vice versa have occurred throughout the evolutionary history of the group. Here, we use time-series data of 16S rRNA gene amplicon sequences in two highly connected transects of wetlands from freshwater marshes to coastal and marine habitats in South Florida, and from oceanic waters along the Florida Keys to study SAR11 ecotype distribution. Contrary to previous studies, we detected the oceanic SAR11 clades Ia.3 and IIa.B not only in marine and coastal waters but also in similar relative abundances in freshwater and brackish environments, all of which were dominated by the presumably brackish water-preferring SAR11 clade IIIa.1. Genome sequencing and comparative genomics of a novel isolate of the most abundant clade IIIa.1 did not identify clear adaptations that would explain this dominance over the canonical freshwater SAR11 clade IIIb or the ability to sustain populations at lower salinity than previously reported. Genotyping of clades Ia.3 and IIIa.1 suggests a selective sweep in freshwater populations of these subclades. Our study indicates SAR11 ecotypes are more adaptable than previously acknowledged and that proximity and connectivity between habitats with distinct salinity seem to be important factors that can drive these adaptations.