Metaexoproteomics Reveals Microbial Behavior in the Ocean’s Interior

The proteins present in the extracellular environment of cells, named the “exoproteome,” are critical for microbial survival, growth, and interaction with their surroundings. However, little is known about microbial exoproteomes in natural marine environments. Here, we used a metaproteomic approach to characterize the exoprotein profiles (10 kDa-0.2 μm) throughout a water column in the South China Sea. Viruses, together with Alpha- and Gammaproteobacteria were the predominant contributors. However, the exoprotein-producing microbial communities varied with depth: SAR11 in the shallow waters, Pseudomonadales and Nitrososphaeria in the mesopelagic layer, and Alteromonadales, Rhizobiales, and Betaproteobacteria in the bathypelagic layer. Besides viral and unknown proteins, diverse transporters contributed substantially to the exoproteomes and varied vertically in their microbial origins, but presented similar patterns in their predicted substrate identities throughout the water column. Other microbial metabolic processes subject to vertical zonation included proteolysis, the oxidation of ammonia, nitrite and carbon monoxide, C1 metabolism, and the degradation of sulfur-containing dissolved organic matter (DOM). Our metaexoproteomic study provides insights into the depth-variable trends in the in situ ecological traits of the marine microbial community hidden in the non-cellular world, including nutrient cycling, niche partitioning and DOM remineralization.