Metaproteomics reveals nutrient availability shaping distinct microbial community and metabolic niche in the nutrient-depleted and replete layers of an oligotrophic euphotic zone

The oligotrophic oceanic euphotic zone comprises the upper nutrient-depleted layer (NDL) and the lower nutrient-replete layer (NRL). However, knowledge of microbial metabolic processes in these two distinct regimes is limited. Here, we characterized the functional microbial proteins of two regimes in two contrasting environments, sites SEATS and SS1 located in the north and the center of the oligotrophic South China Sea using a metaproteomic approach. Proteobacteria was the predominant functional group in both the NDL and the NRL, and Alteromonadales, Oceanospirillales and Rhodobacterales were the most abundant proteobacterial functional groups at the order level, while eukaryotic phytoplankton had a more important metabolic role in the NRL. In contrast to the NDL, prokaryotic composition in the NRL significantly differed between the two sites. The more abundant cyanobacteria in the NRL of SEATS were attributed to higher nutrient concentration. Rhodobacterales were mainly associated with aerobic anoxygenic photosynthetic activity in the two regimes and were actively involved in organic carbon degradation. Free-living proteobacterial members along with the mixotrophic picocyanobacteria were the predominant carbon fixers in the NDL. However, microbial CO2 assimilation was more active in the NRL and eukaryotic phytoplankton contributed significantly to carbon fixation in this regime. This study provides insight into the different metabolic processes of microbial community between the NDL and NRL, and photomixotroph- and heterotroph-driven carbon fixation in the NDL, together with phytoplankton-driven carbon fixation in the NRL, determines primary production in the euphotic zone of the oligotrophic SCS.