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Cross-exchange of B-vitamins underpins a mutualistic interaction between Ostreococcus tauri and Dinoroseobacter shibae.

Accepted version
Peer-reviewed

Type

Article

Change log

Authors

Cooper, Matthew B 
Kazamia, Elena 
Helliwell, Katherine E 
Kudahl, Ulrich Johan 
Sayer, Andrew 

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.

Description

Keywords

Biotin, Chlorophyta, Heterotrophic Processes, Niacin, Phytoplankton, Rhodobacteraceae, Symbiosis, Thiamine, Vitamin B 12, Vitamin B Complex

Journal Title

ISME J

Conference Name

Journal ISSN

1751-7362
1751-7370

Volume Title

13

Publisher

Oxford University Press (OUP)
Sponsorship
Biotechnology and Biological Sciences Research Council (BB/I013164/1)
Economic and Social Research Council (RES-168-26-0125)
Biotechnology and Biological Sciences Research Council (BB/M011194/1)
Engineering and Physical Sciences Research Council (EP/J004847/1)
Royal Society (unknown)
European Commission (317184)
EU FP7