Functional redundancy of seasonal vitamin B12 biosynthesis pathways in coastal marine microbial communities

Vitamin B-12 (cobalamin) is a major cofactor required by most marine microbes, but only produced by a few prokaryotes in the ocean, which is globally B-12-depleted. Despite the ecological importance of B-12, the seasonality of B-12 metabolisms and the organisms involved in its synthesis in the ocean remain poorly known. Here we use metagenomics to assess the monthly dynamics of B-12-related pathways and the functional diversity of associated microbial communities in the coastal NW Mediterranean Sea over 7 years. We show that genes related to potential B-12 metabolisms were characterized by an annual succession of different organisms carrying distinct production pathways. During the most productive winter months, archaea (Nitrosopumilus and Nitrosopelagicus) were the main contributors to B-12 synthesis potential through the anaerobic pathway (cbi genes). In turn, Alphaproteobacteria (HIMB11, UBA8309, Puniceispirillum) contributed to B-12 synthesis potential in spring and summer through the aerobic pathway (cob genes). Cyanobacteria could produce pseudo-cobalamin from spring to autumn. Finally, we show that during years with environmental perturbations, the organisms usually carrying B-12 synthesis genes were replaced by others having the same gene, thus maintaining the potential for B-12 production. Such ecological insurance could contribute to the long-term functional resilience of marine microbial communities exposed to contrasting inter-annual environmental conditions.