Prokaryotic communities of the French Polynesian sponge Dactylospongia metachromia display a site-specific and stable diversity during an aquaculture trial

Abstract

Dynamics of microbiomes through time are fundamental regarding survival and resilience of their hosts when facing environmental alterations. As for marine species with commercial applications, such as marine sponges, assessing the temporal change of prokaryotic communities allows us to better consider the adaptation of sponges to aquaculture designs. The present study aims to investigate the factors shaping the microbiome of the sponge Dactylospongia metachromia, in a context of aquaculture development in French Polynesia, Rangiroa, Tuamotu archipelago. A temporal approach targeting explants collected during farming trials revealed a relative high stability of the prokaryotic diversity, meanwhile a complementary biogeographical study confirmed a spatial specificity amongst samples at different longitudinal scales. Results from this additional spatial analysis confirmed that differences in prokaryotic communities might first be explained by environmental changes (mainly temperature and salinity), while no significant effect of the host phylogeny was observed. The core community of D. metachromia is thus characterized by a high spatiotemporal constancy, which is a good prospect for the sustainable exploitation of this species towards drug development. Indeed, a microbiome stability across locations and throughout the farming process, as evidenced by our results, should go against a negative influence of sponge translocation during in situ aquaculture.

Keywords: Biogeography; Farming trials; French Polynesia; Holobiont; Marine sponges; Microbiome.

Fig. 1

Locations of the sampling sites of the study. A: map of all sampling sites (Mercator projection). B: map of the six French Polynesian islands of the study (Tetiaroa, Rangiroa, Raroia, Makemo Tematangi and Mangareva). C: map of sampling sites located in Rangiroa atoll (Avatoru, Tiputa, Lagon 1 and Lagon 2). Farming trials were conducted on the Western reef side of Rangiroa, roughly 1 km away from the Avatoru channel

Fig. 2

Diversity of the prokaryotic communities associated with Dactylospongia metachromia samples collected during the temporal study. A, B and C: boxplots representing the α-diversity metrics (A for Shannon, B for Chao1 and C for Pielou indices). D and E: NMDS plots representing the β-diversity (Bray–Curtis distances). F and G: db-RDA plots representing the environmental parameters as explanatory variables of the β-diversity (Bray–Curtis distances). D and F: plots of the sample scores of the NMDS and db-RDA, respectively. E and G: plots of the ASVs scores of the NMDS and db-RDA, respectively

Fig. 3

β-diversity of the prokaryotic communities associated with Dactylospongia metachromia samples from the biogeographical study. A and B: NMDS plot. C and D: db-RDA plots representing the environmental parameters as explanatory variables of the β-diversity. A and C: plots of the sample scores of the NMDS and db-RDA, respectively. B and D: plots of the ASVs scores of the NMDS and db-RDA, respectively

Fig. 4

Barplots of the relative percentages of the core prokaryotic community composition (at the family level) of Dactylospongia metachromia. Core ASVs are present at least in 90% of the samples. A: samples from the farming trials (Donor: samples collected in December 2019; 9-, 12-, 15- and 18-months samples: cultured samples respectively collected in September 2020, December 2020, March 2021 and May 2021). B: samples from the biogeographical study (abbreviations used: Mal: Maldives, Mak: Makemo)