Seasonality drives temporal niche partitioning of pelagic prokaryotes

Prokaryote seasonality is well documented in lakes, coastal areas, and inland seas, yet microbial annual periodicity in diverse open ocean settings is less well characterized. Here, we report seasonality in pelagic prokaryotes from open ocean depth profiles collected over 8.5 years in the North Pacific Subtropical Gyre. At depths shallower than 150 m, we found significant annual cycling in >62% of all pelagic prokaryote taxa. Although the proportion of seasonally cycling taxa diminished at depths >150 m, annual periodicity to depths of 4000 m was observed in some taxa. Even among closely related prokaryotes in the same clade, variable seasonal maxima were observed, a sub-clade-level temporal niche partitioning referred to here as seasonal ecotypes. One prevailing trend in the euphotic zone was a seasonal shift from surface water abundance maxima in winter, to spring and summer annual peaks at greater depths. In the upper mixed layer, most Prochlorococcus seasonal ecotypes had winter abundance maxima, while bacterial heterotrophs typically peaked in summer. In the euphotic subsurface, common seasonal ecotypes included Prochlorococcus having spring or summer maxima, and heterotrophic and chemolithoautotrophic prokaryotes having winter or fall maxima. At meso- and bathypelagic depths, most prokaryotes exhibited winter, spring, or fall seasonal maxima, alongside annual peaks of surface-dwelling photoautotrophs exported to the deep sea. The results indicate that seasonal ecotype annual cycling is a central feature of open ocean prokaryote communities, and suggest that subtle yet predictable seasonal niche partitioning helps drive and sustain prokaryote genetic diversification throughout the open ocean's interior.