Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility

Abstract

Reef‐building corals are at risk of extinction from ocean warming. While some corals can enhance their thermal limits by associating with dinoflagellate photosymbionts of superior stress tolerance, the extent to which symbiont communities will reorganize under increased warming pressure remains unclear. Here we show that corals in the hottest reefs in the world in the Persian Gulf maintain associations with the same symbionts across 1.5 years despite extreme seasonal warming and acute heat stress (≥35°C). Persian Gulf corals predominantly associated with Cladocopium (clade C) and most also hosted Symbiodinium (clade A) and/or Durusdinium (clade D). This is in contrast to the neighbouring and milder Oman Sea, where corals associated with Durusdinium and only a minority hosted background levels of Cladocopium. During acute heat stress, the higher prevalence of Symbiodinium and Durusdinium in bleached versus nonbleached Persian Gulf corals indicates that genotypes of these background genera did not confer bleaching resistance. Within symbiont genera, the majority of ITS2 rDNA type profiles were unique to their respective coral species, confirming the existence of host‐specific symbiont lineages. Notably, further differentiation among Persian Gulf sites demonstrates that symbiont populations are either isolated or specialized over tens to hundreds of kilometres. Thermal tolerance across coral species was associated with the prevalence of a single ITS2 intragenomic sequence variant (C3gulf), definitive of the Cladocopium thermophilum group. The abundance of C3gulf was highest in bleaching‐resistant corals and at warmer sites, potentially indicating a specific symbiont genotype (or set of genotypes) that may play a role in thermal tolerance that warrants further investigation. Together, our findings indicate that co‐evolution of host–Symbiodiniaceae partnerships favours fidelity rather than flexibility in extreme environments and under future warming.

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.…”

Extreme environmental conditions reduce coral reef fish biodiversity and productivity

“…1), with the seven highest temperatures all occurring in the Arabian Gulf. In situ data loggers deployed on the substrate (4-6 m depth) at our study sites 60 recorded summer maximum temperatures of 36.0°C (mean daily maximum from 2012 to 2017: 33.7°C) in the Arabian Gulf and 34.8°C (mean daily maximum from 2012 to 2014: 29.9°C) in the Gulf of Oman, while recording minimum winter temperatures of 17.3°C (mean daily minimum = 22.0°C) in the Arabian Gulf and 21.5°C (mean daily minimum = 23.7°C) in the Gulf of Oman ( Supplementary Fig. 2).…”

“…Thus, maximum temperatures on reefs along the Arabian Gulf coast of the United Arab Emirates closely approach forecasted temperatures for tropical coral reefs at the end of the century 62 . While the two locations also differ in several co-varying environmental factors, including salinity, productivity, or reef geomorphology, temperature is commonly considered the strongest environmental force that shapes life in the Arabian Gulf 60 – 64 . Despite the seemingly unfavorable conditions for tropical reef building corals in the past and present, corals have persisted in this region for approximately 15,000 years, with the modern coastline harboring coral reef structures for circa 6000 years 62 .…”

Homogenization of Endosymbiont Communities Hosted by Equatorial Corals during the 2016 Mass Bleaching Event

“…For the last decade, high-throughput sequencing has been a mainstream technique for characterizing coral endosymbionts [ 9 , 75 , 107 , 108 ]. Most recently, development of the SymPortal analytical framework specifically for the processing of ITS2 amplicon data obtained from HTS has allowed us to characterize Symbiodiniaceae communities at a much finer resolution by accounting for intragenomic ITS2 diversity [ 81 , 109 , 110 ]. Overall, we found qPCR and HTS to produce consistent patterns of relative Durusdinium and Cladocopium abundances ( Figure 2 ), even though the relationship between relative qPCR-estimated concentrations and HTS read abundances was weak ( Figure S1 ).…”