Availability of vitamin B12 and its lower ligand intermediate α-ribazole impact prokaryotic and protist communities in oceanic systems

Abstract

Genome analyses predict that the cofactor cobalamin (vitamin B₁₂, called B₁₂ herein) is produced by only one-third of all prokaryotes but almost all encode at least one B₁₂-dependent enzyme, in most cases methionine synthase. This implies that the majority of prokaryotes relies on exogenous B₁₂ supply and interacts with producers. B₁₂ consists of a corrin ring centred around a cobalt ion and the lower ligand 5'6-dimethylbenzimidazole (DMB). It has never been tested whether availability of this pivotal cofactor, DMB or its intermediate α-ribazole affect growth and composition of prokaryotic microbial communities. Here we show that in the subtropical, equatorial and polar frontal Pacific Ocean supply of B₁₂ and α-ribazole enhances heterotrophic prokaryotic production and alters the composition of prokaryotic and heterotrophic protist communities. In the polar frontal Pacific, the SAR11 clade and Oceanospirillales increased their relative abundances upon B₁₂ supply. In the subtropical Pacific, Oceanospirillales increased their relative abundance upon B₁₂ supply as well but also downregulated the transcription of the btuB gene, encoding the outer membrane permease for B₁₂. Surprisingly, Prochlorococcus, known to produce pseudo-B₁₂ and not B₁₂, exhibited significant upregulation of genes encoding key proteins of photosystem I + II, carbon fixation and nitrate reduction upon B₁₂ supply in the subtropical Pacific. These findings show that availability of B₁₂ and α-ribazole affect growth and composition of prokaryotic and protist communities in oceanic systems thus revealing far-reaching consequences of methionine biosynthesis and other B₁₂-dependent enzymatic reactions on a community level.