Basin-scale biogeography of Prochlorococcus and SAR11 ecotype replication

Establishing links between microbial diversity and environmental processes requires resolving the high degree of functional variation among closely related lineages or ecotypes. Here, we implement and validate an improved metagenomic approach that estimates the spatial biogeography and environmental regulation of ecotype-specific replication patterns (R(Obs)) across ocean regions. A total of 719 metagenomes were analyzed from meridional Bio-GO-SHIP sections in the Atlantic and Indian Ocean. Accounting for sequencing bias and anchoring replication estimates in genome structure were critical for identifying physiologically relevant biological signals. For example, ecotypes within the dominant marine cyanobacteria Prochlorococcus exhibited distinct diel cycles in R(Obs) that peaked between 19:00–22:00. Additionally, both Prochlorococcus ecotypes and ecotypes within the highly abundant heterotroph Pelagibacter (SAR11) demonstrated systematic biogeographies in R(Obs) that differed from spatial patterns in relative abundance. Finally, R(Obs) was significantly regulated by nutrient stress and temperature, and explained by differences in the genomic potential for nutrient transport, energy production, cell wall structure, and replication. Our results suggest that our new approach to estimating replication is reflective of gross population growth. Moreover, this work reveals that the interaction between adaptation and environmental change drives systematic variability in replication patterns across ocean basins that is ecotype-specific, adding an activity-based dimension to our understanding of microbial niche space.