Integrated meta-omics reveals organic matter processing by bacteria in the dark ocean

The dark ocean plays a critical role in organic matter cycling and global carbon sequestration; however, a detailed mechanistic understanding of the bacteria-mediated organic matter processes is still in its infancy. Here, we characterized the functional diversity, metabolic potential, and activities of particle-attached (PA, 1.6-200 µm) and free-living (FL, 0.2-1.6 µm) bacterial communities collected from a depth of 3,000 m at two sites with contrasting environments in the South China Sea using a combined metaproteomic and metagenomic approach. The taxonomic composition of the microbial communities varied between the two size fractions. Prominent bacterial groups exhibited distinct lifestyle preferences. Oceanospirillales preferred a PA lifestyle while Pelagibacterales favored an FL lifestyle. Moreover, the dominant bacterial groups occupied distinct metabolic niches in the remineralization of organic carbon. Alteromonadales, Oceanospirillales, and Sphingomonadales adopted a ‘sharing’ mode by expressing peptidases, non-proteolytic hydrolases, oxygenases, and dehydrogenases to cleave particulate organic matter into labile organic substrates presumably taken up by the enzyme-producing bacteria or by co-occurring bacteria. Rhodobacterales, however, exhibited a ‘selfish’ mode, and Pelagibacterales adopted a ‘scavenging’ mode, expressing only low and even no extracellular enzymes but abundant transporters to take up different ranges of available substrates. Role allocation among bacteria with varying life strategies and nutritive modes effectively drives organic matter processing in the dark ocean. Our results provide insights into the metabolic features, lifestyles, and nutritional strategies of deep-sea bacteria, thereby advancing our understanding of the biogeochemistry of organic matter driven by bacteria in the dark ocean.