Insights into the Evolution of Vitamin B12 Auxotrophy from Sequenced Algal Genomes

Abstract

Vitamin B(12) (cobalamin) is a dietary requirement for humans because it is an essential cofactor for two enzymes, methylmalonyl-CoA mutase and methionine synthase (METH). Land plants and fungi neither synthesize or require cobalamin because they do not contain methylmalonyl-CoA mutase, and have an alternative B(12)-independent methionine synthase (METE). Within the algal kingdom, approximately half of all microalgal species need the vitamin as a growth supplement, but there is no phylogenetic relationship between these species, suggesting that the auxotrophy arose multiple times through evolution. We set out to determine the underlying cellular mechanisms for this observation by investigating elements of B(12) metabolism in the sequenced genomes of 15 different algal species, with representatives of the red, green, and brown algae, diatoms, and coccolithophores, including both macro- and microalgae, and from marine and freshwater environments. From this analysis, together with growth assays, we found a strong correlation between the absence of a functional METE gene and B(12) auxotrophy. The presence of a METE unitary pseudogene in the B(12)-dependent green algae Volvox carteri and Gonium pectorale, relatives of the B(12)-independent Chlamydomonas reinhardtii, suggest that B(12) dependence evolved recently in these lineages. In both C. reinhardtii and the diatom Phaeodactylum tricornutum, growth in the presence of cobalamin leads to repression of METE transcription, providing a mechanism for gene loss. Thus varying environmental conditions are likely to have been the reason for the multiple independent origins of B(12) auxotrophy in these organisms. Because the ultimate source of cobalamin is from prokaryotes, the selective loss of METE in different algal lineages will have had important physiological and ecological consequences for these organisms in terms of their dependence on bacteria.

Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

“…However, MIT1002 has the potential capability to utilize vitamin B 12 facultatively-even though it cannot produce this compound itself-as it also encodes the B 12 -dependent MetH methionine synthetase, an isoform of MetE. Although we do not know which form was being used by Alteromonas in co-culture, MetH is typically used preferentially in the presence of vitamin B 12 (Helliwell et al, 2011;Bertrand and Allen, 2012), presumably due to the 4100-fold higher catalytic efficiency of MetH over MetE (Gonzalez et al, 1992). Thus Prochlorococcus may have directly or indirectly provided Alteromonas with vitamin B 12 in co-culture to facilitate growth of the 'helper', although these transcriptional changes could also represent increased production for its own use due to other changes in its metabolism.…”

Molecular insights into a dinoflagellate bloom

“…Some phytoplankton require cobalamin for cobalamin-dependent methionine synthase (MetH), whereas an alternative form of methionine synthase (MetE) exists in some microalgae that do not require B 12 , alleviating them of most of their B 12 requirement (Helliwell et al, 2011;Bertrand et al, 2012). Eukaryotic phytoplankton must obtain B 12 from their environment and/or close bacterial associations (Croft et al, 2005).…”

Batchelor Prize Lecture Fluid dynamics at the scale of the cell

“…The first is the broad class of problems in the general area of symbiosis between different kingdoms of life, such as between bacteria and algae. This has come to the fore through the discovery (Croft et al 2005) that certain species of algae acquire the needed vitamin B 12 through a symbiotic relationship with bacteria (see also Helliwell et al 2011). How do these species find each other and stay close enough for the symbiosis from one generation to the next?…”