Exploiting Adaptation in Phytoplankton as Environmental Biosensors for Nutrient Stress

Primary productivity in large parts of the ocean is commonly regarded as nutrient limited. However, there is a large uncertainty in which single nutrient or even multiple nutrients control primary productivity in specific regions. Our current understanding of nutrient stress in the ocean is primarily based on ship-board experiments. However, multiple issues have been associated with this technique including bottle-effects and difficulties in simulating environmental conditions in oligotrophic regions. Here, we propose to use the principle that marine microorganisms rapidly adapt to shift in nutrient availability via gene gains and losses to determining the global patterns of nutrient limitation. To this end, we quantified the relative frequency of phosphorus, nitrogen, and iron acquisition genes in ~1000 surface communities from the Atlantic, Indian, and Pacific Oceans. We focused on Prochlorococcus, Synechococcus, and Pelagibacter, as they are present in most nutrient-limited regions. We found clear evidence of variation in nutrient stress between regions. As expected, we found enriched abundances of iron acquisition genes in equatorial upwelling regions and high abundance P acquisition genes in the North Atlantic Ocean. However, we also saw evidence of P stress in the northern Indian Ocean and Bay of Bengal. In addition, N acquisition genes were frequent in the central North Pacific suggesting widespread N stress. These findings suggest that we can use mechanisms of microbial adaptation to monitor and understand the global regulation of primary production.