Vitamins B1 and B12 and biosynthetic precursors affect bacterioplankton growth dynamics and community composition in oceanic systems

Vitamins function in myriads of metabolic reactions as co-factors and are indispensable for life. However, numerous organisms, including marine microbial communities, lack de novo synthesis of the two most pivotal vitamins, B1 and B12. Therefore vitamin transfer and cycling is essential for growth dynamics of microbial communities in marine pelagic ecosystems. Vitamin auxotrophy is not exclusively encountered by the exchange of final vitamin cofactors, but increasing evidence exists that also exogenously provided vitamin precursors can substitute lacking genetic capacities. To identify the relevance of such phenomena among marine prokaryotes, we screened 3024 genomes for genes encoding biosynthetic pathways of B1 and B12. Our findings not only elucidated vitamin producers and auxotrophs, but also that particular groups of bacteria solely synthesize building blocks of respective vitamins. Further, to shed more light on the complex exchange of vitamins and respective precursors in marine pelagic ecosystems we conducted five mesocosm experiments in distinct biogeographic provinces in the Pacific. Three mesocosms were supplemented with cobalamin (B12) and its lower ligand α-ribazole and two mesocosms with thiamin (B1), the B1-precursors 4-methyl-5-(β-hydroxyethyl)thiazol, 4-amino-5-hydroxymethyl-2-methylpyrimidine alone and in combination. We observed a significant enhancement of bacterial growth not only upon the addition of vitamin B12, but also when supplemented by α-ribazole or the two thiamin moieties relative to an unsupplemented control. Further, the addition of α-ribazole and B12 altered the composition of the prokaryotic and eukaryotic communities and metatranscriptomic analyses provided evidence that the intracellular metabolic processes were affected accordingly. Our findings provide evidence for the complexity of microbial vitamin cycling in the ocean and that single vitamin metabolites and precursors possess the potential to alter microbial activity.