Massive export of diazotrophs across the tropical south Pacific Ocean

Abstract

Diazotrophs are widespread microorganisms that regulate marine productivity in 60% of our oceans by alleviating nitrogen limitation. Yet, their contribution to organic carbon and nitrogen export fluxes has never been quantified, making an assessment of their impact on the biological carbon pump impossible. Here, we examine species-specific fates of several groups of globally-distributed unicellular (UCYN) and filamentous diazotrophs in the mesopelagic ocean. We used an innovative approach consisting of the combined deployment of surface-tethered drifting sediment traps, Marine Snow Catcher, and Bottle-net, in which we performed nifH sequencing and quantitative PCR on major diazotroph groups across the subtropical South Pacific Ocean. nifH sequencing data from sediment traps deployed at 170 m, 270 m and 1000 m provide clear evidence that cyanobacterial and non-cyanobacterial diazotrophs are systematically present in sinking particles down to 1000 m, with export fluxes being the highest for the UCYN-A1 symbiosis, followed by UCYN-B or Trichodesmium (depending on station and depth), Gamma A and UCYN-C. Specific export turnover rates (a metric similar to the export efficiency adapted to organisms) point to a more efficient export of UCYN groups relative to the filamentous Trichodesmium. This is further confirmed by Marine Snow catcher data showing that the proportion of sinking cells was significantly higher for UCYN compared to Trichodesmium. Phycoerythrin-containing UCYN-B and UCYN-C-like cells were indeed recurrently found embedded in large (> 50 µm) seemingly organic aggregates, or organized into clusters of tens to hundreds of cells linked by an extracellular matrix, facilitating the export. Overall, diazotrophs accounted for 6-13% (170 m) to 45-100% (1000 m) of the total particulate nitrogen export fluxes in our study. We thus conclude that diazotrophs are important contributors to carbon sequestration in the subtropical South Pacific Ocean and need to be considered in future studies to improve the accuracy of current regional and global estimates of export.