High variability in organic carbon sources and microbial activities in the hadopelagic waters

Hadal sediments are recognized as organic carbon depocenters with intensified microbial activity compared to adjacent abyssal sites due to focusing of relatively labile organic materials. However, the sources and turnover of hadopelagic organic carbon and its linkages to microbial activities have not been studied. We present the first synergic research on particulate organic carbon, dark carbon fixation, and size-fractionated microbial community respiration proxy over the Atacama Trench. The results demonstrate that all parameters attenuate rapidly from surface to mesopelagic water (~ 1000 m). Progressing deeper, values remain relatively stable throughout bathypelagic (~ 4000 m) and abyssopelagic (~ 6000 m) waters. However, in the hadopelagic zone (> 6000 m), highly variable values indicate dynamic organic carbon sources and microbial activities in the deepest trench. On average, 71% of the microbial community respiration proxy is attributable to particle-associated communities, indicating importance of particles for microbial metabolism. No apparent relationship was observed between the microbial community respiration proxy and microbial 16S rRNA gene abundance below the epipelagic depth, indicating variable supply and quality of organic carbon likely constrained heterotrophic activities rather than microbial abundances in the deep ocean. The depth-integrated dark carbon fixation (> 1000 m) accounts for 11.5% ± 7.6% of the surface net primary production, of which 2.9% ± 0.4% is from hadopelagic depth. Dark carbon fixation is thus an important in situ organic carbon source for hadal life. This study suggests that high variability in organic carbon sources and microbial activities in the hadopelagic trench cannot be simply extrapolated from findings in the shallower dark ocean (e.g., 1000–6000 m).