Mesoscale eddies shape Prochlorococcus community structure and dynamics in the oligotrophic open ocean

Mesoscale eddies, horizontally rotating currents sometimes referred to as "ocean weather," influence open ocean macronutrient distributions, primary production, and microbial community structure. Such eddies impact ecosystems like the North Pacific Subtropical Gyre, where year-round thermal stratification limits the mixing of subsurface macronutrients with surface waters. Populations of the dominant primary producer Prochlorococcus in the North Pacific Subtropical Gyre consist of genetic variants with differential adaptive traits to light intensity, temperature, and macronutrient availability. How Prochlorococcus population variants respond to transient, localized environmental changes, however, remains an open question. Leveraging microbial community phylogenetic, metagenomic, and metatranscriptomic data, we report here a consistent, specific enrichment of Prochlorococcus high-light I ecotypes around the deep chlorophyll maximum (DCM) in cyclonic eddies, but not adjacent anticyclonic eddies. The shallower DCM depths of cyclones had lower temperatures, higher light intensities, and elevated nutrient concentrations compared to adjacent anticyclones, which favored Prochlorococcus high-light I ecotype proliferation. Prochlorococcus high-light I ecotypes in the cyclone DCM exhibited unique genetic traits related to nitrogen metabolism and were enriched in gene transcripts associated with energy production, cell replication, and proliferation. Prochlorococcus gene transcripts involved in amino acid transport, metabolism, and biosynthesis were also elevated in the cyclone. These results suggest the potential importance of nitrogen metabolism in Prochlorococcus high-light I ecotype proliferation in cyclonic eddies. Our findings demonstrate how mesoscale eddies shape microbial community structure in the oligotrophic ocean and how Prochlorococcus communities respond to short-term localized environmental variability.