High diversity of crustose coralline algae microbiomes across species and islands, and implications for coral recruits

Abstract

Background: Crustose Coralline Algae (CCA) play a crucial role in coral reef ecosystems, contributing significantly to reef formation and serving as substrates for coral recruitment. The microbiome associated with CCAs may promote coral recruitment, yet these microbial communities remain largely understudied. This study investigates the microbial communities associated with a large number of different CCA species across six different islands of French Polynesia, and assess their potential influence on the microbiome of coral recruits.

Results: Our findings reveal that CCA harbor a large diversity of bacteria that had not been reported until now. The composition of these microbial communities was influenced by geographic location, and was also closely linked to the host species, identified at a fine taxonomic unit using the 16S rRNA gene of the CCA chloroplast. We demonstrate the usefulness of these ecologically meaningful units that we call CCA chlorotypes. Additionally, we observed a correlation between host phylogeny and microbiome composition (phylosymbiosis) in two CCA species. Contrary to expectations, the CCA microbiome did not act as a microbial reservoir for coral recruits. However, the microbial community of coral recruits varied according to the substrate on which they grew.

Conclusions: The study significantly expands the number of characterized CCA microbiomes, and provides new insight into the extensive diversity of these microbial communities. We show distinct microbiomes between and within CCA species, characterized by specific chloroplast 16S rRNA gene sequences. We term these distinct groups "chlorotypes", and demonstrate their utility to differentiate CCA. We also show that only few bacterial taxa were shared between CCA and coral recruits growing in contact with them. Nevertheless, we observed that the microbial community of coral recruits varied depending on the substrate they grew on. We conclude that CCA and their associated bacteria influence the microbiome composition of the coral recruits.

Keywords: Bacteria; Coral; Coral recruitment; Crustose coralline algae; Interaction; Microbiome.

Fig. 1

Underwater photographs of a°Pocillopora recruit in association with the CCA P. onkodes, and b°Pocillopora recruit in association with turf algae. Two samples were taken for each association type. For the coral-CCA association: (1) the CCA associated with the recruit and (2) the recruit growing on/near the CCA. For the coral-turf association: (3) the turf associated with the recruits and (4) the recruit growing near the turf. Samples were also taken of adult Pocillopora corals and of P. onkodes not associated with corals (i.e., CCA- or turf-dominated area). The scale bar = 1 cm

Fig. 2

Bacterial diversity and community composition of crustose coralline algae (CCA), coral, and turf algae across six islands in the Tuamotu archipelago (French Polynesia). a Map of the islands and sites sampled. b Microbial community diversity (Shannon index) in the different host types. The box plot horizontal bars show the median value, the box indicates the first and third QRs, and the whiskers indicate 1.5*IQR. The asterisks indicate p values < 0.001. c Non-metric multidimensional scaling (nMDS) of bacterial community composition in the corals (Pocillopora), CCA (N. fosliei, N. frutescens, P. gardineri, P. onkodes, and unk. - unknown), and turf algae (stress: 0.17)

Fig. 3

Distance tree based on chloroplast 16S rRNA genes (chlorotype) from CCA samples across six islands of French Polynesia. The bar on the right shows in which sampled CCA species the chlorotype was found. The vertical ribbon indicates the species names inferred through the chlorotype. Nf1, Nf2 and Po1 are clades mentioned in the description of the CCA bacterial community composition

Fig. 4

Bacterial diversity and community composition of CCA in 6 islands of French Polynesia. a Accumulation curve of community richness. Vertical plain lines delimit the different CCA species; vertical dashed line delimit the different CCA chlorotypes. Chlorotypes found in more than eight samples have their names displayed. b Non-metric multidimensional scaling (nMDS) of bacterial community composition in known and unknown CCA (stress = 0.18). Colors represent the different chlorotypes and shapes indicate the CCA species names

Fig. 5

UpSet plot showing the number (a) and abundance (b) of ASVs unique to or shared between CCA species

Fig. 6

Bacterial diversity and community composition of the coral Pocillopora, the CCA P. onkodes and turf algae. a Shannon diversity for the coral Pocillopora associated or not to a CCA or turf algae, for the CCA P. onkodes associated or not to the coral, and for the turf algae associated with the coral. b Shannon diversity in different colony size of Pocillopora. c Bray-Curtis based nMDS ordination (stress = 0.15) of the microbial community composition coral recruits, adult corals, turf algae, and CCA P. onkodes under different association conditions. nd: not determined; Unass.: unassociated

Fig. 7

UpSet plot showing the number (a) and abundance (b) of ASVs unique or shared between Pocillopora (recruits and adult), P. onkodes and turf algae microbiome