Flexible B 12 ecophysiology of Phaeocystis antarctica due to a fusion B 12 –independent methionine synthase with widespread homologues

Abstract

Coastal Antarctic marine ecosystems are significant in carbon cycling because of their intense seasonal phytoplankton blooms. Southern Ocean algae are primarily limited by light and iron (Fe) and can be co-limited by cobalamin (vitamin B 12 ). Micronutrient limitation controls productivity and shapes the composition of blooms which are typically dominated by either diatoms or the haptophyte Phaeocystis antarctica . However, the vitamin requirements and ecophysiology of the keystone species P. antarctica remain poorly characterized. Using cultures, physiological analysis, and comparative omics, we examined the response of P. antarctica to a matrix of Fe-B 12 conditions. We show that P. antarctica is not auxotrophic for B 12 , as previously suggested, and identify mechanisms underlying its B 12 response in cultures of predominantly solitary and colonial cells. A combination of proteomics and proteogenomics reveals a B 12 -independent methionine synthase fusion protein (MetE-fusion) that is expressed under vitamin limitation and interreplaced with the B 12 -dependent isoform under replete conditions. Database searches return homologues of the MetE-fusion protein in multiple Phaeocystis species and in a wide range of marine microbes, including other photosynthetic eukaryotes with polymorphic life cycles as well as bacterioplankton. Furthermore, we find MetE-fusion homologues expressed in metaproteomic and metatranscriptomic field samples in polar and more geographically widespread regions. As climate change impacts micronutrient availability in the coastal Southern Ocean, our finding that P. antarctica has a flexible B 12 metabolism has implications for its relative fitness compared to B 12 -auxotrophic diatoms and for the detection of B 12 -stress in a more diverse set of marine microbes.