Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales

Abstract

Reef-building corals are well regarded not only for their obligate association with endosymbiotic algae, but also with prokaryotic symbionts, the specificity of which remains elusive. To identify the central microbial symbionts of corals, their specificity across species and conservation over geographic regions, we sequenced partial SSU ribosomal RNA genes of Bacteria and Archaea from the common corals Stylophora pistillata and Pocillopora verrucosa across 28 reefs within seven major geographical regions. We demonstrate that both corals harbor Endozoicomonas bacteria as their prevalent symbiont. Importantly, catalyzed reporter deposition–fluorescence in situ hybridization (CARD–FISH) with Endozoicomonas-specific probes confirmed their residence as large aggregations deep within coral tissues. Using fine-scale genotyping techniques and single-cell genomics, we demonstrate that P. verrucosa harbors the same Endozoicomonas, whereas S. pistillata associates with geographically distinct genotypes. This specificity may be shaped by the different reproductive strategies of the hosts, potentially uncovering a pattern of symbiont selection that is linked to life history. Spawning corals such as P. verrucosa acquire prokaryotes from the environment. In contrast, brooding corals such as S. pistillata release symbiont-packed planula larvae, which may explain a strong regional signature in their microbiome. Our work contributes to the factors underlying microbiome specificity and adds detail to coral holobiont functioning.

Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome

“…In contrast, Endozoicomonas OTU 1 and OTU 2 remained proportionally stable under excess DON over 14 days (about 56% for OTU 1 vs. 29% for OTU 2 average relative contribution). The reasons for this are unclear at present, although metabolic subfunctionalization/specialization of Endozoicomonas taxa residing in corals was suggested previously (Neave, Michell, Apprill, & Voolstra, 2017; Neave, Rachmawati, et al., 2017). …”

“…More generally, Endozoicomonas are commonly assumed to provide an important role in coral holobiont functioning due to their widespread prevalence and high abundance in many coral species (Bayer et al., 2013; Gignoux‐Wolfsohn, Aronson, & Vollmer, 2017; Glasl et al., 2016; Jessen et al., 2013; Meyer, Gunasekera, Scott, Paul, & Teplitski, 2016; Neave et al., 2016; Neave, Rachmawati, et al., 2017) and apparent metabolic versatility (Ding, Shiu, Chen, Chiang, & Tang, 2016; Hyun et al., 2014; Neave, Michell, et al., 2017; Yang et al., 2010). Further, reductions in the abundance of Endozoicomonas in stressed, diseased, or bleached corals are reported in a number of studies, suggesting that pervasive abundance of Endozoicomonas might be an indicator of habitat suitability (Bourne et al., 2008; Cárdenas et al., 2012; Gignoux‐Wolfsohn et al., 2017; Meyer et al., 2016; Morrow et al., 2014; Roder et al., 2015; Röthig et al., 2016; Ziegler et al., 2016).…”

Distinct Bacterial Microbiomes Associate with the Deep-Sea Coral Eguchipsammia fistula from the Red Sea and from Aquaria Settings

“…More importantly, these microbiomes align functionally to the different environments (see below). As such, the notion of species-specific core microbiomes that are consistent over large geographical and environmental scales (Bayer et al, 2013a;Ainsworth et al, 2015;Roder et al, 2015;Hernandez-Agreda et al, 2016Ziegler et al, 2016;Neave et al, 2017) is in contrast to the highly variable core microbiome in E. fistula. Rather, it may suggest a limited association with obligate bacterial symbionts and/or a high flexibility in regard to bacterial symbionts.…”

Laboratory-Cultured Strains of the Sea Anemone Exaiptasia Reveal Distinct Bacterial Communities

“…Moreover, coevolution of bacteria and coral has been proposed (Thompson et al, 2015), as it was demonstrated for Endozoicomonas symbionts in corals with contrasting life-history traits and across global scales (Bayer et al, 2013;Neave et al, 2016Neave et al, , 2017. Detailed analysis of these studies revealed fine scale host-Endozoicomonas specific patterns suggesting phylosymbiosis between corals and this bacterial genus.…”