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.2019 Feb;13(2):334-345.
doi: 10.1038/s41396-018-0274-y. Epub 2018 Sep 18.

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

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

Matthew B Cooper et al. ISME J.2019 Feb.

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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Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
Determining the genetic basis for vitamin dependency.a Growth of axenicO. tauri andD. shibae (with 1% glucose) with and without various B-vitamins at stationary phase after two sub-cultures.b Schematic of biosynthetic pathways forp-aminobenzoic acid, niacin and biotin. Results of similarity sequence searches ofD. shibae andO. tauri genomes for genes encoding biosynthetic enzymes for these vitamins are indicated.O. tauri encodes the gene set necessary for synthesis forp-aminobenzoic acid, niacin and biotin (Supplementary Information), whereasD. shibae lacks a complete biosynthetic pathway for all three of these vitamins
Fig. 2
Fig. 2
Growth ofO. tauri andD.shibae under different B-vitamin combinations.a Growth assay to confirm B-vitamin auxotrophy in axenicO. tauri andD. shibae. Bacterial cultures were supplemented with 1% glucose.b Growth ofO. tauri in mono-culture (grey) or in co-culture withD. shibae (white) under different B-vitamin profiles. Cell density was determined at stationary phase.c Growth ofD. shibae in mono-culture (grey) or in co-culture withO. tauri (white) under different B-vitamin profiles. Error bars show standard deviation for three biological replicates
Fig. 3
Fig. 3
Growth dynamics ofO. tauri in co-culture withD. shibae.a The ratio ofD. shibae toO. tauri cells during growth in co-cultures initiated at different starting ratios. Cell densities of algae and bacteria were monitored untilO. tauri reached stationary phase at 25 days.b The effect of adding-back nutrients on the established ratio. Ratio ofO. tauri toD. shibae cells over the course of one culture when a stable co-culture is inoculated into medium favouring the bacteria (supplemented with 1% glucose and vitaminsp-aminobenzoic acid (pABA), B3 and B7), medium favouring the alga (with B1 and B12) or no nutrient addback
Fig. 4
Fig. 4
Rescue effect ofO. tauri andD. shibae for required B-vitamins is stable and long-term.a Log cell density ofO. tauri cells at stationary phase over four sub-cultures that were inoculated at differing initial ratios toD. shibae.b The average ratio ofD. shibae: O. tauri at each different starting bacterial: algal ratio at stationary phase. Error bars indicate standard error for mean of ratios at stationary phase across all sub-cultures (n = 4)
Fig. 5
Fig. 5
Distribution of pathways for the synthesis of vitamins B3, B7 and B12 in selected bacterial species. A range of bacterial species with sequenced genomes were subjected to a bioinformatics pipeline to predict their vitamin biosynthesis capabilities [16]. A set of 197 verified marine bacteria was obtained from the GOLD database [51], and a selection of 70 members of theRhodobacteraceae family were sampled from NCBI. Their taxonomic positions were determined using ETE 3 [66], and species that were unclassified at the family level were discarded from the final analysis. The data were summarised at the family level for each of the different data sets—marine non-Rhodobacteraceae n = 178, marineRhodobacteraceae n = 19,Rhodobacteraceae n = 70
Fig. 6
Fig. 6
The role of cofactors in the meta-metabolome of the O. tauri-D. shibae partnership. Many essential metabolic processes depend on enzyme cofactors derived from B-vitamins, including biosynthesis of some of the cofactors themselves. Red arrows indicate reactions dependent on vitamins synthesised by D. shibae (cobalamin, thiamine), blue arrows indicate reactions dependent on vitamins synthesised by O. tauri: biotin, pABA (leading to folate) and niacin (leading to NAD+/NADP+). Reactions shown are not exhaustive, and in particular there are many more NAD+/NADP+ dependent enzymes
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