Multi-omics analysis reveals important role for microbial-derived metabolites from Botryllus schlosseri in metal interactions.

Abstract

Marine microbial communities govern many of the biological and chemical processes in the ocean, including element cycles, ecosystem health, and disease. Marine organisms are surrounded by microbes, with complex molecular interactions occurring between bacterial symbionts, eukaryotic hosts, and their pathogens or prey. Trace metals in the ocean can be either beneficial or detrimental to marine life depending on their concentrations and bioavailability. Multiple marine tunicate species are known to bioaccumulate trace metals in their mantel, and research suggests that tunicate microbiota plays an important role in this process. Botryllus schlosseri, a marine colonial tunicate, has become a model organism for cellular and developmental studies, yet its ecological interactions are still not well understood. Using an integrated multidisciplinary approach, we established a comprehensive baseline and explored correlations between members of the B. schlosseri microbiome, metabolome, and metallome to elucidate the ecological effects of trace metals in host-microbe-pathogen interactions. We identified significant correlations between metals, including manganese, nickel, cerium, zinc, and cobalt, with various metabolites and bacterial taxa. These findings offer insights into B. schlosseri's biological and chemical interactions with microorganisms and their environment, contributing to bridging the knowledge gap of host-microbiome-environment interactions and establishing a foundation for continuing research on the ecological effects of trace metals in these biological systems.IMPORTANCEGiven the importance of marine invertebrates and their microbial communities in marine ecosystems, we sought to characterize the largely unknown microbial associates, metal sequestration, and metabolite production of the marine colonial tunicate, Botryllus schlosseri, a model organism for cellular and developmental studies. Using an integrated multidisciplinary approach, we identified significant correlations between metals, metabolites, and bacterial taxa. B. schlosseri tissue was highly enriched in metals compared to seawater, and B. schlosseri microbiome beta-diversity was significantly different from seawater. We also introduced the concept of the pan-metabolome to classify metabolites based on their presence or absence across complex samples and found microbial metabolites in both the core and flexible metabolome. These findings offer insights into B. schlosseri's biological and chemical interactions with microorganisms and their environment, bridging the knowledge gap of host-microbiome-environment interactions and establishing a foundation for continuing research on the ecological effects of trace metals in these biological systems.