Presence of vitamin B12metabolism in the last common ancestor of land plants

Abstract

AbstractVitamin B12, or cobalamin, (hereinafter B12) is an essential organic micronutrient, required by humans as a cofactor for methionine synthase (METH) and for methylmalonyl CoA mutase (MCM), involved in the propionate shunt. B12is a complex corrinoid molecule made only by a subset of bacteria. Plants and fungi have an alternative methionine synthase (METE) that does not need a B12cofactor, so these organisms are typically considered to neither synthesise nor utilise B12. In contrast many algal species utilise B12if it is available, because they encode both METE and METH. Moreover, a large proportion of algal species encode METH only, and so are like animals in being dependent on an external source of the vitamin. Here, we performed a detailed phylogenetic analysis of the distribution of METE, METH and eleven further proteins implicated in B12metabolism in eukaryotic cells across an exhaustive library of over 1,500 plant and algal genomes and transcriptomes. The results reveal the hitherto undetected existence of B12-associated metabolism deep into the streptophytes. The B12-dependent synthase METH, and the accessory proteins MTRR, CblB, CblC, CblD and CblJ were detected in the basally divergent plant lineage of hornworts, and CblB and CblJ were further identified in liverworts. Using phylogenetic and PFAM analysis we demonstrate this is due to retention of ancestral B12-metabolism pathways in the last common ancestor of land plants, followed by at least two independent complete losses in mosses and vascular plants. We further show more limited distributions of genes encoding B12-related proteins across the algal tree of life, including MCM and type II ribonucleotide reductase, alongside an obligate B12-dependency across several major marine algal orders. Finally, by considering the functional biology of early-diverging land plants, together with the collection sites of ten further algal species inferred to have lost B12-dependent metabolism, we propose freshwater-to-land transitions and symbiotic associations to have been major constraining factors in B12availability in early plant evolution.