Abstract
Ostreococcus tauri, a picoeukaryotic alga that contributes significantly to primary production in oligotrophic waters, has a highly streamlined genome, lacking the genetic capacity to grow without the vitamins thiamine (B1) and cobalamin (B12). Here we demonstrate that the B12 and B1 auxotrophy of O. tauri can be alleviated by co-culturing with a heterotrophic bacterial partner Dinoroseobacter shibae, a member of the Rhodobacteraceae family of alpha-proteobacteria, genera of which are frequently found associated with marine algae. D. shibae lacks the complete pathway to synthesise three other B-vitamins: niacin (B3), biotin (B7), and p-aminobenzoic acid (a precursor for folate, B9), and the alga is in turn able to satisfy the reciprocal vitamin requirements of its bacterial partner in a stable long-term co-culture. Bioinformatics searches of 197 representative marine bacteria with sequenced genomes identified just nine species that had a similar combination of traits (ability to make vitamin B12, but missing one or more genes for niacin and biotin biosynthesis enzymes), all of which were from the Rhodobacteraceae. Further analysis of 70 species from this family revealed the majority encoded the B12 pathway, but only half were able to make niacin, and fewer than 13% biotin. These characteristics may have either contributed to or resulted from the tendency of members of this lineage to adopt lifestyles in close association with algae. This study provides a nuanced view of bacterial–phytoplankton interactions, emphasising the complexity of the sources, sinks and dynamic cycling between marine microbes of these important organic micronutrients.
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Acknowledgements
We thank Herve Moreau at Banyuls-sur-mer Oceanological Observatory in France for the gift of O. tauri OTH95. We are grateful to Nigel Miller (Department of Pathology, University of Cambridge) for help with FACS. We acknowledge funding from BBSRC grant (BB/I013164/1) and EU FP7 DEMA (Project no. 309086). MBC was in recipient of a CASE studentship with the UK Biotechnology and Biological Sciences Research Council (BBSRC) and Plymouth Marine Laboratory Applications Ltd, UJK was supported by EU FP7 Marie Curie ITN Photo.Comm (Project No 317184), and AS by the Cambridge BBSRC Doctoral Training Partnership.
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Cooper, M.B., Kazamia, E., Helliwell, K.E. et al. Cross-exchange of B-vitamins underpins a mutualistic interaction between Ostreococcus tauri and Dinoroseobacter shibae. ISME J 13, 334–345 (2019). https://doi.org/10.1038/s41396-018-0274-y
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DOI: https://doi.org/10.1038/s41396-018-0274-y
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