Eco-phylogenetic analyses reveal divergent evolution of vitamin B-12 metabolism in the marine bacterial family 'Psychromonadaceae'

Cobalamin (vitamin B-12) is an essential micronutrient required by both prokaryotes and eukaryotes. Nevertheless, with high genetic and metabolic cost, de novo cobalamin biosynthesis is exclusive to a subset of prokaryotic taxa. Many Cyanobacterial and Archaeal taxa have been implicated in de novo cobalamin biosynthesis in epi- and mesopelagic ocean respectively. However, the contributions of Gammaproteobacteria particularly the family 'Psychromonadaceae' is largely unknown. Through phylo-pangenomic analyses using concatenated single-copy proteins and homologous gene clusters respectively, the phylogenies within 'Psychromonadaceae' recapitulate both their taxonomic delineations and environmental distributions. Moreover, uneven distribution of cobalamin de novo biosynthetic operon and cobalamin-dependent light-responsive regulon were observed, and of which the linkages to the environmental conditions where cobalamin availability and light regime can be varied respectively were discussed, suggesting the impacts of ecological divergence in shaping their disparate cobalamin-related metabolisms. Functional analysis demonstrated a varying degree of cobalamin dependency for both central metabolic processes and cobalamin-mediated light-responsive regulation, and underlying sequence characteristics of cis- and trans-regulatory elements were revealed. Our findings emphasized the potential roles of cobalamin in shaping the ecological distributions and driving the metabolic evolution in the marine bacterial family 'Psychromonadaceae', and have further implications for an improved understanding of nutritional interdependencies and community metabolism modulated by cobalamin.