Vitamin B₁₂-auxotrophy in dinoflagellates caused by incomplete or absent cobalamin-independent methionine synthase genes (metE)

Dinoflagellates are responsible for most marine harmful algal blooms (HABs) and play vital roles in many ocean processes. More than 90% of dinoflagellates are vitamin B₁₂ auxotrophs and that B₁₂ availability can control dinoflagellate HABs, yet the genetic basis of B₁₂ auxotrophy in dinoflagellates in the framework of the ecology of dinoflagellates and particularly HABs, which was the objective of this work. Here, we investigated the presence, phylogeny, and transcription of two methionine synthase genes (B₁₂-dependent metH and B₁₂-independent metE) via searching and assembling transcripts and genes from transcriptomic and genomic databases, cloning 38 cDNA isoforms of the two genes from 14 strains of dinoflagellates, measuring the expression at different scenarios of B₁₂, and comprehensive phylogenetic analyses of more than 100 organisms. We found that 1) metH was present in all 58 dinoflagellates accessible and metE was present in 40 of 58 species, 2) all metE genes lacked N-terminal domains, 3) metE of dinoflagellates were phylogenetically distinct from other known metE genes, and 4) expression of metH in dinoflagellates was responsive to exogenous B₁₂ levels while expression of metE was not responding as that of genuine metE genes. We conclude that most, hypothetically all, dinoflagellates have either non-functional metE genes lacking N-terminal domain for most species, or do not possess metE for other species, which provides the genetic basis for the widespread nature of B₁₂ auxotrophy in dinoflagellates. The work elucidated a fundamental aspect of the nutritional ecology of dinoflagellates.