Biogeography at the limits of life: Do extremophilic microbial communities show biogeographical regionalization?

Aim Biogeographical regions are the fundamental geographical units for grouping Earth's biodiversity. Biogeographical regionalization has been demonstrated for many higher taxa, such as terrestrial plants and vertebrates, but not in microbial communities. Therefore, we sought to test empirically whether microbial communities, or taxa, show patterns consistent with biogeographical regionalization. Location Within halite (NaCl) crystals from coastal solar salterns of western Europe, the Mediterranean and east Africa. Time period Modern (2006–2013). Major taxa studied Archaea. Methods Using high-throughput Illumina amplicon sequencing, we generated the most high-resolution characterization of halite-associated archaeal communities to date, using samples from 17 locations. We grouped communities into biogeographical clusters based on community turnover to test whether these communities show biogeographical regionalization. To examine whether individual taxa, rather than communities, show biogeographical patterns, we also tested whether the relative abundance of individual genera may be indicative of a community's biogeographical origins using machine learning methods, specifically random forest classification. Results We found that the rate of community turnover was greatest over subregional spatial scales (< 500 km), whereas at regional spatial scales the turnover was independent of geographical distance. Biogeographical clusters of communities were either not statistically robust or lacked spatial coherence, inconsistent with biogeographical regionalization. However, we identified several archaeal genera that were good indicators of biogeographical origin, providing classification error rates of < 10%. Main conclusions Overall, our results provide little support for the concept of biogeographical regions in these extremophilic microbial communities, despite the fact that some taxa do show biogeographical patterns. We suggest that variable dispersal ability among the halite-associated Archaea may disrupt biogeographical patterns at the community level, preventing the formation of biogeographical regions. This means that the processes that lead to the formation of biogeographical regions operate differentially on individual microbial taxa rather than on entire communities.