Branched-chain amino acid metabolism supports Roseobacteraceae positive interactions in marine biofilms.

Abstract

Interspecies interactions are key factors affecting the stability of microbial communities. However, microbial interactions in marine biofilms, which constitute up to 80% of the microbial biomass in certain marine environments, are not well understood. We addressed this knowledge gap by coculturing four marine biofilm-derived Roseobacteraceae strains (Leisingera aquaemixtae M597, Roseibium aggregatum S1616, Alloyangia pacifica T6124, and Sulfitobacter indolifex W002) in 14 single carbon sources. Overall, 140 coculture experiments revealed 39.3% positive interactions compared to 8.3% negative interactions. When the carbon source was consumed by only one strain, the interaction between the strains was more likely to be positive. The interaction between S1616 and M597, when cultured in D-gluconic acid, was further studied as an example. S1616-M597 coculture displayed a higher D-gluconic acid consumption rate than S1616 monoculture, whereas M597 could not use D-gluconic acid as the sole carbon source. The supernatant of S1616 monoculture supported the growth of M597, and branched-chain amino acids in the supernatant were consumed. Transcriptomic analysis suggested that M597 induced the expression of genes for branched-chain amino acid biosynthesis in S1616. Additionally, metagenomic analysis revealed the wide distribution and a strongly correlated co-occurrence of the four strains in global oceanic biofilms. Together, our findings show that interspecies positive interactions are prevalent among marine-biofilm Roseobacteraceae, and the interactions are likely to be mediated by branched-chain amino acids metabolism.

Importance: Interspecies interactions are crucial for microbial community structure and function. Despite well-studied social behaviors in model microorganisms, species interactions in natural marine biofilms especially Roseobacteraceae with complex metabolic pathways are not well understood. Our findings suggest that positive microbial interactions, which can be mediated by branched-chain amino acid biosynthesis, are common among marine-biofilm Roseobacteraceae. This study provides new insights into microbial interactions and the ecology of marine biofilms.