Draft genome and description of Waterburya agarophytonicola gen. nov. sp. nov. (Pleurocapsales, Cyanobacteria): a seaweed symbiont

Abstract

This work introduces Waterburya agarophytonicola Bonthond and Shalygin gen. nov., sp. nov, a baeocyte producing cyanobacterium that was isolated from the rhodophyte Agarophyton vermiculophyllum (Ohmi) Gurgel et al., an invasive seaweed that has spread across the northern hemisphere. The new species genome reveals a diverse repertoire of chemotaxis and adhesion related genes, including genes coding for type IV pili assembly proteins and a high number of genes coding for filamentous hemagglutinin family (FHA) proteins. Among a genetic basis for the synthesis of siderophores, carotenoids and numerous vitamins, W. agarophytonicola is potentially capable of producing cobalamin (vitamin B₁₂), for which A. vermiculophyllum is an auxotroph. With a taxonomic description of the genus and species and a draft genome, this study provides as a basis for future research, to uncover the nature of this geographically independent association between seaweed and cyanobiont.

Keywords: Cobalamin; Gracilaria vermiculophylla; Holobiont; Pleurocapsales; Symbiosis; Vitamin B12.

Fig. 1

Estimated abundances of the W. agarophytonicola core OTU, across sampled substrates (i.e., seawater, algal surface and algal tissue) from 6 populations (Japan, China, Germany, France, Virginia, California, details in Bonthond et al. 2020). The 95% confidence intervals are indicated with shaded columns. Estimates and intervals were back-transformed from the log scale and multiplied by a 100 to be presented in percentages

Fig. 2

16S rRNA megaphylogeny with a total of 9593 taxa, showing the position of the new genus and species Waterburya agarophytonicola. a General view on the collapsed phylogeny with leaves depicting major cyanobacterial orders. Units near the names of the orders show the number of sequences in the collapsed clades. High support values on the backbone are not shown (they were 89–99); the node connecting the Prochlorothrix clade with the rest of the phylogeny did not show high support. b Zoomed view on the clade containing the order Pleurocapsales, with several Chrooccocales clades as sister taxa. c Detailed view of the order Pleurocapsales, including W. agarophytonicola. A large asterisk indicates the maximum support value of the Maximum Likelihood, “hyphen” depicts support < 50. Note a, b and c are the same tree with different levels of resolution (b and c are zoomed parts of the tree focused on Pleurocapsales and on Waterburya agarophytonicola). See Fig. S2 for an uncollapsed version of the order Pleurocapsales fraction in panel c

Fig. 3

Maximum-likelihood tree based on 31 conserved proteins extracted from 96 cyanobacterial genomes. The analysis was conducted with 4 outgroup taxa which have been removed from the figure. Waterburya agarophytonicola is displayed in bold. Branches corresponding to nodes with > 95 bootstrap support values are thickened and ex-type strains are labelled with an uppercase ‘T’

Fig. 4

Microphotographs showing the morphology of Waterburya agarophytonicola. a Released baeocytes; b Growing cells, note that adjacent cells are not a product of binary fission; c Aggregation of the cells and initial baeocyte formation within mother cell (arrow); d Massive baeocyte formation adjacent to the small group of growing cells; e Clear example of baeocyte production; f: Unreleased, released and growing baeocytes. The scale bar equals 10 μm