Functional complementarity between vitamin B1 and B12 metabolisms shapes seasonal marine microbial communities

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Abstract
Marine microbial communities are fundamental to nutrient and biogeochemical cycling, with intricate networks of metabolic interdependencies influencing their structure and dynamics. Among these, vitamins B1 (thiamin) and B12 (cobalamin) play crucial roles as enzymatic cofactors in central metabolic pathways. Despite their importance, the temporal dynamics of vitamin production, bioavailability, and associated microbial interactions, remain poorly understood. Using a 7-year monthly metagenomic time series from the NW Mediterranean Sea (SOLA station), we found that vitamin B1/B12 auxotrophs (need for an exogenous vitamin source) were present throughout the year. Among B1 auxotrophs, those requiring the thiamin precursor HMP were the most prevalent, with peak abundances in summer. Distinct metagenome-assembled genome co-abundance patterns between B1 and B12 producers/auxotrophs across seasons suggested mutualistic relationships. Double B1/B12 vitamin complementarities were more common in summer, and single vitamin complementarity was dominant in winter. As previously shown for vitamin B12, which is limiting during winter, bioassays revealed variable availability of vitamin B1 in winter seawater despite the abundance of its producers, suggesting potential transfer of vitamin B1 among microorganisms. Finally, microcosm experiments showed that B1 and B12 amendments significantly influenced the composition of microbial communities, with temporal variations in their impact. In some cases, B12 and B1 amendments favored both vitamin auxotrophs and producers, highlighting complex interdependencies between B1 and B12 producers and consumers. Our findings highlight the complexity of B vitamin-mediated metabolic interactions that shape microbial community dynamics and underscore the need for long-term, high-resolution studies to better understand vitamin-driven ecological processes in marine systems.
Funding Information
  • French Agence Nationale de la Recherche (ANR-24-CE02-7681)

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