Variations in Physiology and Genomic Function of Prochlorococcus Across the Eastern Indian Ocean

The widespread distribution of Prochlorococcus can be attributed to the extensive genetic diversity that allows them to adapt to various oligotrophic environments. We investigated the adaptation of Prochlorococcus to nutrient environments in the surface eastern Indian Ocean in November 2018. The growth rate of the Prochlorococcus population and its response to macronutrient enrichments and the abundance of functional gene modules related to nutrient utilization were examined by on-deck incubation experiments and metagenomic analysis, respectively. Although the dissolved inorganic nitrogen was depleted (~58 nM) and the Prochlorococcus populations were dominated by the high-light-adapted II ecotype, Prochlorococcus populations showed distinct physiological patterns, especially the response to macronutrient enrichments, indicating their adaptation to local nutrient environments. At the northernmost station in the Bay of Bengal, the significant increase in growth rate with macronutrient enrichments and the highest abundance of the phosphate starvation response two-component regulatory system module indicated adaptation to phosphorus-limited environments. In the southern EIO, the insignificant increase in growth rate with macronutrient enrichment and higher abundance of the iron complex transport system module suggested adaptation to iron-limited environments. However, genomic characteristics are not always associated with physiological characteristics. The abundance of the nitrate/nitrite transport system module was higher in the southern EIO, where the growth of Prochlorococcus relied on regenerated nitrogen sources as revealed by incubation experiments. These results reflected the complexity of Prochlorococcus adaptation especially in chronically oligotrophic environments, which was better revealed by combining physiological and genomic analyses.