Distinct biogeographical patterns of marine bacterial taxonomy and functional genes

Aim: While paradigms of macroecology are challenged by the high rates of reproduction, dispersal and horizontal gene exchange of bacterial communities, environmental DNA sequencing makes community profiles accessible. We test fundamental hypotheses of macroecological theories, showing that both taxonomic and functional classifications have distinct biogeographical variation across distance and environments depending on trophic composition. Location: Studies spanning the global oceans. Methods: Taxonomic and functional profiles were obtained from metagenomes and were compared across oceanographic regions and tested for patterns of co-occurrence. The influences of sampling method (filter size), environmental variables and geographical distribution were compared with distance-based linear models to test predictors of taxonomic and functional composition. Macroecological drivers were compared with bacterial community structure to test four biogeographical hypotheses: (1) no biogeographical patterns, (2) community structure reflects environmental dissimilarity, (3) community structure reflects distance, (4) community structure reflects environment and distance. Results: Bacterial families were clustered into four trophic groups – phototrophic, oligotrophic, eutrophic and copiotrophic – by changes in abundance across oceanographic regions and co-occurrence with core functions. Changes in community composition were best modelled by longitude for free-living communities and dissolved oxygen for mixed communities of free-living and particle-associated bacteria. Both microhabitat and community assignment had an impact on biogeographical patterns, with taxonomic compositions following our hypotheses 2 and 4 and functional gene compositions following hypotheses 3 and 4. Main conclusions: We described four trophic groups adding to the current dichotomy of the classification of marine bacteria as oligotrophic or copiotrophic. Taxonomic composition of mixed communities reflected environmental differences but not geographical distance, whereas functional gene composition in free-living communities was independent of environmental dissimilarity and reflected geographical distance. Patterns of biogeography in bacterial communities differed depending on the description of taxa or function. Therefore, we developed a new paradigm for bacterial ecology which shows that some aspects of bacterial evolution depend on trophic complexity, history and current environmental conditions.