Temporal shifts in prokaryotic metabolism in response to organic carbon dynamics in the mesopelagic ocean during an export event in the Southern ocean

As the major term in downward organic carbon flux attenuation, determining prokaryotic metabolism over depth in the mesopelagic ocean is crucial for constraining the efficiency of the gravitational biological carbon pump (BCP). We hypothesize that the enhancement of particulate organic carbon (POC) concentrations in the mesopelagic twilight zone during export events leads to a temporally dynamic prokaryotic metabolic response, which likely has consequences for the efficiency of the BCP. We tested this hypothesis by making repeated measurements of leucine assimilation and leucine respiration at in situ concentrations over six depths throughout the upper 500 m of the water column during the collapse of a large-scale Southern Ocean spring diatom bloom. Rates of prokaryotic leucine assimilation were used to indicate levels of prokaryotic heterotrophic production, and leucine assimilation efficiency (LAE; the proportion of leucine used for growth versus respiration) was taken as an indicator of prokaryotic growth efficiency. Thus, relative shifts in LAE are indicative of shifts in rates of prokaryotic production relative to respiration. The flux of POC through the oceans’ interior led to a dynamic prokaryotic response, characterized by a temporary elevation in mesopelagic prokaryote leucine assimilation rates, LAE and prokaryotic abundance. By the final measurement these changes had already begun to revert, despite POC concentrations still being enriched. As hypothesized, our data revealed distinctions in the phases of the mesopelagic system, likely due to an evolution in bulk prokaryotic metabolic status and the amount and composition of organic matter available. This indicates that estimating ocean carbon sequestration during export events necessitates a time course of measurements throughout the period of POC downward flux. Our findings also revealed distinctions in the ecophysiological prokaryotic responses to substrate regimes between the surface mixed layer and the mesopelagic. Specifically, in the latter in situ leucine concentrations appeared more significant in controlling prokaryote metabolism than POC concentration, and were more closely related to per cell leucine assimilation, than respiration. Whereas, in the mixed layer, the concentration of in situ leucine did not seem to drive rates of its assimilation, rather POC concentration was a strong negative driver of cell specific leucine respiration. These findings are suggestive of stronger levels of energy limitation in the deeper ocean. We surmised that ocean regions with sporadic substrate supply to the mesopelagic are likely to experience stronger energy limitation which favors prokaryotic respiration over production.