Abstract
Vitamin B12 (cobalamin) can control phytoplankton development and community composition, with around half of microalgal species requiring this vitamin for growth. B12 dependency is determined by the absence of cobalamin-independent methionine synthase and is unrelated across lineages. Despite their important role in carbon and sulphur biogeochemistry, little is known about haptophytes utilization of vitamin B12 and their ability to cope with its limitation. Here we report the first evaluation of B12 auxotrophy among this lineage based on molecular data of 19 species from 9 families. We assume that all species encode only a B12-dependent methionine synthase, suggesting ubiquitous B12 auxotrophy in this phylum. We further address the effect of different B12 limitations on the molecular physiology of the model haptophyte Tisochrysis lutea. By coupling growth assays in batch and chemostat to cobalamin quantification and expression analyses, we propose that haptophytes use three strategies to cope with B12 limitation. Haptophytes may assimilate dissolved methionine, finely regulate genes involved in methionine cycle and B12 transport and/or limit B12 transport to the mitochondrion. Taken together, these results provide better understanding of B12 metabolism in haptophytes and represent valuable data for deciphering how B12-producing bacteria shape the structure and dynamics of this important phytoplankton community.
Highlights
Vitamin B12, or cobalamin, can control phytoplankton growth[1] and community composition in Polar Regions[2,3,4] including the Southern Ocean[5,6], and in some temperate coastal waters[7]
Since no haptophyte sequence was retrieved in these large datasets, this reinforces the hypothesis of absence of B12-independent methionine synthase in the haptophyte lineage
It has been observed that cobalamin auxotrophy is determined by the presence of metH and the absence of the cobalamin-independent methionine synthase metE11,12
Summary
Vitamin B12, or cobalamin, can control phytoplankton growth[1] and community composition in Polar Regions[2,3,4] including the Southern Ocean[5,6], and in some temperate coastal waters[7]. Haptophytes, whose origin has been dated around 830 million years ago[16], are important contributors to global marine primary production, representing significant carbon sink in oceans[17,18] These widespread eukaryotic microalgae are one of the main producers of dimethylsulfoniopropionate (DMSP), the precursor of dimethyl sulfide (DMS), an important component of sulphur cycle that acts as a cloud condensation nuclei[19,20]. RNR II converts ribonucleotides into deoxyribonucleotides for DNA synthesis using MeCbl[9] and MMCM (gene mmcm) is involved in the citric acid (TCA) cycle in the mitochondrion, where it converts methylmalonyl-CoA into succinyl-CoA with AdoCbl[13] Species with these B12-dependent enzymes can grow without the vitamin if they possess the cobalamin-independent METE isoform. Vitamin B12 may be important in haptophytes and dinoflagellates cellular processes, especially in nitrogen-limited environments
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