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

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 (B) and cobalamin (B) Here we demonstrate that the B and B 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 (B), biotin (B), and p-aminobenzoic acid (a precursor for folate, B), 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 B, 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 B 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.

A community perspective on the concept of marine holobionts: current status, challenges, and future directions

“…The Vibrio-squid model provides insights into the effect of microbiota on animal development, circadian rhythms, and immune systems (McFall-Ngai 2014). The unicellular green alga Ostreococcus, an important marine primary producer, has been shown to exchange vitamins with specific associated bacteria (Cooper et al 2019). The green macroalga Ulva mutabilis has enabled the exploration of bacteria-mediated growth and morphogenesis including the identification of original chemical interactions in the holobiont (Wichard 2015;Kessler et al 2018).…”

Specificity of cobamide remodeling, uptake and utilization in Vibrio cholerae

“…Studies of Antarctic seas showed that cobalamin levels directly correlate with diatom blooms, suggesting an important environmental dependency (Bertrand et al , ; Bertrand et al , ). Some eukaryotic algae have mutualistic relationships with cobalamin‐producing bacteria (Croft et al , ; Xie et al , ; Cooper et al , ), while two species have been shown to remodel pseudocobalamin in the presence of DMB (Helliwell et al , ). In the eukaryotic organisms in which different cobamide variants have been examined, the general trend of specificity for the cobalamin variant has been observed (Stupperich and Nexo, ; Helliwell et al , ; Ma et al , ).…”

Spatial Structure of Marine Host-Associated Microbiomes: Effect of Taxonomy, Species Traits, and Study Design

“…Additionally, host-associated microbiomes can also influence and reflect the host's health (e.g., skin microbiome of marine mammals, Bierlich et al, 2018). The green alga and major marine primary producer Ostreococcus exchanges B vitamins with bacterial partners, highlighting the importance of mutualistic interactions between the microbiome and the host (Cooper et al, 2019). Sponge and coral microbiomes also play important roles in cycling key nutrients including phosphorus, carbon, nitrogen, and sulfur (Raina et al, 2009;Pita et al, 2018).…”