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

Vitamin B12 (cobalamin) is a major cofactor required by most marine microbes, but only produced by a few prokaryotes in the ocean, which is globally B12 -depleted. Despite the ecological importance of B12 , the seasonality of B12 metabolisms and the organisms involved in its synthesis in the ocean remain poorly known. Here we use metagenomics to assess the monthly dynamics of B12 -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 B12 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 B12 synthesis potential through the anaerobic pathway (cbi genes). In turn, Alphaproteobacteria (HIMB11, UBA8309, Puniceispirillum) contributed to B12 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 B12 synthesis genes were replaced by others having the same gene, thus maintaining the potential for B12 production. Such ecological insurance could contribute to the long-term functional resilience of marine microbial communities exposed to contrasting inter-annual environmental conditions.