Microbial community transcriptional networks are conserved in three domains at ocean basin scales

Significance Microbes drive biogeochemical cycles across the globe, collectively playing a central role in shaping the biosphere. Despite their immense importance, the in situ activities of communities of microbes, in particular uncultivated lineages of “microbial dark matter,” remain poorly elucidated. In this study, we report that common temporal and ecological dynamics underpin disparate marine microbial communities, providing the first evidence that trans-Pacific diurnal transcriptional patterns in these communities may regulate ecological and biogeochemical processes across the ocean. In total, our findings indicate a remarkable regularity in the timing of community-wide activity in the ocean, and suggest that global patterns of a variety of biogeochemical transformations may be temporally predictable and governed by structured ecological determinants. Planktonic microbial communities in the ocean are typically dominated by several cosmopolitan clades of Bacteria, Archaea, and Eukarya characterized by their ribosomal RNA gene phylogenies and genomic features. Although the environments these communities inhabit range from coastal to open ocean waters, how the biological dynamics vary between such disparate habitats is not well known. To gain insight into the differential activities of microbial populations inhabiting different oceanic provinces we compared the daily metatranscriptome profiles of related microbial populations inhabiting surface waters of both a coastal California upwelling region (CC) as well as the oligotrophic North Pacific Subtropical Gyre (NPSG). Transcriptional networks revealed that the dominant photoautotrophic microbes in each environment (Ostreococcus in CC, Prochlorococcus in NPSG) were central determinants of overall community transcriptome dynamics. Furthermore, heterotrophic bacterial clades common to both ecosystems (SAR11, SAR116, SAR86, SAR406, and Roseobacter) displayed conserved, genome-wide inter- and intrataxon transcriptional patterns and diel cycles. Populations of SAR11 and SAR86 clades in particular exhibited tightly coordinated transcriptional patterns in both coastal and pelagic ecosystems, suggesting that specific biological interactions between these groups are widespread in nature. Our results identify common diurnally oscillating behaviors among diverse planktonic microbial species regardless of habitat, suggesting that highly conserved temporally phased biotic interactions are ubiquitous among planktonic microbial communities worldwide.