Microbial metabolism in laboratory reared marine snow as revealed by a multi-omics approach

Marine snow represents an organic matter-rich habitat and provides substrates for diverse microbial populations in the marine ecosystem. However, the functional diversity and metabolic interactions within the microbial community inhabiting marine snow remain largely underexplored, particularly for specific metabolic pathways involved in marine snow degradation. Here, we used a multi-omics approach to explore the microbial response to laboratory-reared phytoplankton-derived marine snow. Our results demonstrated a dramatic shift in both taxonomic and functional profiles of the microbial community after the formation of phytoplankton-derived marine snow using a rolling tank system. The changes in microbial metabolic processes were more pronounced in the metaproteome than in the metagenome in response to marine snow. Fast-growing taxa within the Gammaproteobacteria were the most dominant group at both the metagenomic and metaproteomic level. These Gammaproteobacteria possessed a variety of carbohydrate-active enzymes (CAZymes) and transporters facilitating substrate cleavage and uptake, respectively. Analysis of metagenome-assembled genomes (MAGs) revealed that the response to marine snow amendment was primarily mediated by Alteromonas, Vibrio, and Thalassotalea. Among these, Alteromonas exclusively expressing auxiliary activities 2 (AA2) of the CAZyme subfamily were abundant in both the free-living (FL) and marine snow-attached (MA) microbial communities. Thus, Alteromonas likely played a pivotal role in the degradation of marine snow. The enzymes of AA2 produced by these Alteromonas MAGs are capable of detoxifying peroxide intermediates generated during the breakdown of marine snow into smaller poly- and oligomers, providing available substrates for other microorganisms within the system. In addition, Vibrio and Thalassotalea MAGs exhibited distinct responses to these hydrolysis products of marine snow in different size fractions, suggesting a distinct niche separation. Although chemotaxis proteins were found to be enriched in the proteome of all three MAGs, differences in transporter proteins were identified as the primary factor contributing to the niche separation between these two groups. Vibrio in the FL fraction predominantly utilized ATP-binding cassette transporters (ABCTs), while Thalassotalea MAGs in the MA fraction primarily employed TonB-dependent outer membrane transporters (TBDTs). Our findings shed light on the essential metabolic interactions within marine snow-degrading microbial consortia, which employ complementary physiological mechanisms and survival strategies to effectively scavenge marine snow. This work advances our understanding of the fate of marine snow and the role of microbes in carbon sequestration in the ocean. Video Abstract.