Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations

Abstract

Widespread coral bleaching occurred in the central Red Sea in 2010 and 2015. During both events, a cross-shelf and depth gradient of bleaching severity was identified within the Thuwal reef system, central Red Sea, Saudi Arabia. While bleaching and survival of coral taxa were monitored, neither in situ reef temperatures nor coralassociated algal communities (family Symbiodiniaceae) were characterized. Here, we determined coral host-associated Symbiodiniaceae communities and monitored temperatures along the same cross-shelf and depth gradient on six reefs in 2017 to better understand the role of these factors in the observed bleaching patterns and to generate a baseline for further studies. We characterized [ 600 coralalgal associations across winter and summer in six genera of scleractinian coral (Pocillopora, Stylophora, Seriatopora, Galaxea, Gardineroseris, and Porites) and one fire coral (Family Milleporidae) using ITS2 next-generation sequencing in conjunction with the SymPortal analytical framework. We show that previous bleaching patterns correlate poorly with the largely coral host-specific structure of the 2017 Symbiodiniaceae community and are in better agreement with absolute and intraday sea water temperature variations monitored on the reefs. We demonstrate a greater distinctiveness of Symbiodiniaceae communities at the more severely bleached inshore reefs compared to those reefs further offshore. However, the potential Symbiodiniaceae community changes at these reefs prior to our sampling prevent us from evaluating this distinctiveness as determinative of the differences in bleaching severities. Based on our analyses, we discuss how fine-scale delineation of algal genotypes, including host-specific putative genotypes of Durusdinium trenchii that represent alluring targets for further taxonomic identification, corroborate a niche-adapted rather than generalist character of many coral-Symbiodiniaceae associations. In conclusion, as studies such as this one continue to build the global catalogue of coral-Symbiodiniaceae associations, we may be afforded a better oversight of how specialized coral-algal associations really are and how restricted their modification may be, both of which are critical considerations in predicting the adaptive potential of corals and the reef ecosystems they build. Keywords Symbiodiniaceae Á Coral bleaching Á SymPortal Á ITS2 Á Red Sea Topic Editor Simon Davy B. C. C. Hume and A. Mejia-Restrepo have contributed equally.

Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance

“…3B). The observed pattern of symbiont association indicates high host delity of algal symbionts across sites, as reported previously (Terraneo et al 2019;Howells et al 2020;Hume et al 2020). Further to that, our results support ne-scale differentiation even between geographically close-by sites, as the central Red Sea sites (AF, ExT, ExP) all differed with regard to symbiont identities (Fig.…”

“…At large, the level of responsiveness in algal symbionts from GoA corals was unexpected, given that the common notion is that of a paucity of regulation at the transcriptional level for Symbiodiniaceae (Bayer et al 2012;Baumgarten et al 2013), signi ed by xed expression differences between symbiont genera and species (Barshis et al 2014;Parkinson et al 2016). Notably, corals from all sites associated with distinct and largely consistent microalgal symbiont genotypes, suggesting host delity and local adaptation (Howells et al 2020;Hume et al 2020). Despite the differences across sites, the consistent gene expression stasis of algal symbionts across CRS corals and the disparate responsiveness in Symbiodiniaceae from GoA corals potentially suggests that geographically more distant symbionts are also more differentiated.…”

“…The common notion is that corals can bleach and suffer mortality at just 1-2 °C above their maximum monthly mean (MMM) temperatures Coles 1977, 1990;Glynn and D'croz 1990), but we actually know little about empirical temperature thresholds, as most of our knowledge comes from predictive modeling, observational studies, or long-term thermal exposure experiments. Similarly, susceptibility of corals to bleaching has been attributed to genomic differences of corals and algal symbionts (DeSalvo et al 2008(DeSalvo et al , 2010; Barshis et al 2013;Aranda et al 2016;Bhattacharya et al 2016;Voolstra et al 2017), association with different microalgal symbiont species (Hume et al 2016(Hume et al , 2020Ziegler et al 2017a), or changes in the associated bacteria (Ziegler et al 2017b;Osman et al 2020). However, it is unknown whether the same mechanisms or factors contribute to thermal tolerance of corals at large, i.e., across species and sites.…”

Patterns, Drivers, and Ecological Implications of Upwelling in Coral Reef Habitats of the Southern Red Sea

“…3). Likewise,Hume et al (2020) reported similar cool biases (~0.5 to >1°C) in satellites compared to reef temperatures across the shelf in the Thuwal area of the central Red Sea, approximately 300 km north of the Farasan Banks. Together, this suggests that satellite-derived SST in portions of the Red Sea may substantially underestimate reef-water temperatures.…”

Unlocking the phylogenetic diversity, primary habitats, and abundances of free‐living Symbiodiniaceae on a coral reef

“…However, most Symbiodiniaceae are recalcitrant to culturing (Coffroth, 2005; Krueger & Gates, 2012; Santos et al., 2001), and not all free‐living Symbiodiniaceae can initiate symbiosis (Coffroth et al., 2006; LaJeunesse, 2002; Yamashita et al., 2014), therefore these early studies likely underestimated diversity. Next generation sequencing (NGS) has revolutionised community‐level assessments of marine dinoflagellates, uncovering extensive cryptic biodiversity (Hume et al., 2020; Kohli et al., 2014; Stern et al., 2010) and is increasingly utilised to profile in hospite Symbiodiniaceae community structure (Boulotte et al., 2016; Camp et al., 2020; Hume et al., 2020; Thomas et al., 2014; Ziegler et al., 2017). Few studies have leveraged NGS for free‐living Symbiodiniaceae characterisation.…”