Geographic population structure and distinct intra-population dynamics of globally abundant freshwater bacteria

Implications of geographic separation and temporal dynamics on the evolution of free-living bacterial species are widely unclear. However, the vast amount of metagenome sequencing data generated during the last decades from various habitats around the world provides an unprecedented opportunity for such investigations. Here we exploited publicly available and new freshwater metagenomes in combination with genomes of abundant freshwater bacteria to reveal geographic and temporal population structure. We focused on species that were detected across broad geographic ranges at high enough sequence coverage for meaningful population genomic analyses, associated to the predominant freshwater taxa acI, LD12, Polynucleobacter and Ca. Methylopumilus. Despite the broad geographic ranges, each species appeared as sequence-discrete cluster, in contrast to abundant marine taxa, for which continuous diversity structures were reported on global scale. Population differentiation increased significantly with spatial distance in all species, but notable dispersal barriers (e.g. oceanic) were not apparent. Yet, the different species showed contrasting rates of geographic divergence and strikingly different intra-population dynamics in time series within individual habitats. Change of an LD12 population over seven years was minor (F_ST = 0.04) compared to differentiation between lakes, whereas a Polynucleobacter population displayed strong changes within merely two months (F_ST up to 0.54), similar in scale to differentiation between populations separated by thousands of kilometers. The slowly and steadily evolving LD12 population showed high strain diversity, whereas the dynamic Polynucleobacter population exhibited alternating clonal expansions of mostly two strains only. Based on the contrasting population structures we propose distinct models of speciation.