Insights into the physiological and metabolic features of Thalassobacterium, a novel genus of Verrucomicrobiota with the potential to drive the carbon cycle.

Verrucomicrobiota are widely distributed across various habitats but are difficult to culture. Some previous multiomics analyses reported that Verrucomicrobiota have outstanding metabolic capacity for organic matter degradation and are able to degrade and synthesize polysaccharides, two activities that could contribute significantly to the Earth's carbon cycle. Here, we isolated from marine sediment two novel strains, Thalassobacterium maritimum SDUM461003^T and Thalassobacterium sedimentorum SDUM461004^T, that represent a new genus of the difficult-to-culture phylum Verrucomicrobiota. Genome analysis, functional annotation, and experimental verification revealed that these two strains degrade polysaccharides and antibiotics, including some complex sulfated polysaccharides (SPs), primarily fucoidan and chondroitin sulfate. Moreover, electron microscopy images revealed that these bacteria can synthesize and store large amounts of glycogen. These polysaccharide degradation and synthesis capacities also exist but differ under nitrogen-deficient conditions, indicating that Verrucomicrobiota may have the potential to maintain their normal metabolism by nitrogen fixation under aerobic conditions. Given that polysaccharides and their degradation products are particularly crucial carbon sources for marine microorganisms, Verrucomicrobiota are thought to be important contributors to biogeochemical cycling in the ocean.

Importance: Verrucomicrobiota are widely distributed and able to utilize a variety of difficult-to-biodegrade polysaccharides, which have a significant impact on the marine carbon cycle. However, there are not enough pure culture strains of Verrucomicrobiota, as hard-to-cultivate bacteria, for us to study. Here, our study reports a new genus in the phylum Verrucomicrobiota and investigates their ability to degrade and synthesize a variety of polysaccharides as well as the mechanism of utilizing difficult-to-degrade polysaccharides. We also explored their special performance on carbon utilization in marine nitrogen-deficient environments. This contributes to deepening our understanding of the involvement of marine microorganisms in the marine carbon cycle.