Response And Adaptation Of Scleractinian Coral To High Temperature Stress In The Northern South China Sea

Coral bleaching,caused by global warming,is the main cause of coral reef ecosystem degradation.Relatively high-latitude sea areas are considered potential“shelters” from global warming because the sea surface temperature in summer does not exceed the thermal bleaching threshold of corals.However,in recent years,marine heat waves have led to large-scale coral bleaching in relatively highlatitude coral reef areas.Therefore,the response and adaptability of corals to high temperatures in relatively high-latitude sea areas has attracted substantial attention.In view of these scientific concerns,this study focused on Weizhou Island in Guangxi and Luhuitou in Sanya,Hainan,which are located on the northern edge of the tropics in the northern South China Sea.We selected the high temperaturesensitive corals Acropora pruinosa and Pocillopora damicornis and relatively high temperature-resistant coral Pavona decussata as the species of focus.According to the coral holobiont theory,we used ecological,molecular biology,genetic,and cell biology techniques to analyze the phenotypic characteristics,antioxidant enzyme activities,transcriptional regulation,long non-coding RNAs(lnc RNAs),and genome-wide methylation in coral hosts;the density,photosynthetic intensity,community composition,and transcriptional response of symbiotic Symbiodiniaceae;and the diversity and community composition of symbiotic bacteria.Using these tools,we examined the following:(1)variation in the characteristics of coral holobionts of A.pruinosa and their adaptive mechanisms to large seasonal temperature fluctuations in Weizhou Island;(2)inter-individual differences in the response to high-temperature stress and the potential adaptive mechanism of A.pruinosa on Weizhou Island;(3)differential responses of A.pruinosa and P.decussata to high-temperature stress on Weizhou Island and their significance to the thermal adaptability of corals;(4)molecular response mechanisms of P.damicornis to high-temperature stress in the fluctuating environment of Luhuitou;and(5)molecular mechanisms of thermal acclimation to increase coral thermal adaptability.We reached the following conclusions:(1)Scleractinian corals may increase their adaptation to large seasonal temperature fluctuations at relatively higher latitudes by regulating the transcriptional responses of hosts and symbiotic Symbiodiniaceae,along with theα-diversity and community structure of symbiotic bacteria.Transcriptome sequencing revealed that,similar to the seasonal changes in Symbiodiniaceae density,there are also seasonal differences in the transcriptional responses of coral hosts and the Symbiodiniaceae symbiont,which can be an adaptation strategy of A.pruinosa to large seasonal temperature fluctuations on Weizhou Island.In summer,the coral host transcriptome was found to be enriched in disease-related metabolic pathways,whereas the transcriptome of Symbiodiniaceae was only enriched in the steroid biosynthesis pathway.Many of the same Kyoto Encyclopedia of Genes and Genomes(KEGG)pathways of the coral host and Symbiodiniaceae were enriched in both winter and spring.However,many metabolism-related pathways in Symbiodiniaceae were enriched only in spring.The symbiotic Symbiodiniaceae of A.pruinosa in different seasons was dominated by clade C1.Symbiotic bacteria are highly plastic,with the highest α-diversity and abundance detected in summer and the lowest detected in spring.Although the symbiotic bacterial community structure was reorganized across the different seasons,the similarity in symbiotic bacterial structure was higher in winter and spring.The dominant bacterial genera in spring,summer,autumn,and winter were Ralstonia,Prosthecochloris with BD1-7＿clade,BD1-7＿clade,and Ralstonia,respectively.Moreover,the function of core bacteria changed under environmental conditions in different seasons.The dominant core bacteria in spring,summer,autumn,and winter were Rhodococcus(OTU538),BD1-7＿clade(OTU538),BD1-7＿clade(OTU538),and Rhodococcus(OTU538),respectively.There were differences in the relative abundances of the core bacteria,which exhibited a shift from a dominant type to a rare type in different seasons.(2)Extreme high-temperature events disrupt coral holobiont stability,and A.pruinosa may enhance symbiotic bacterial α-diversity,alter the commensal bacterial community structure,and elevate host symbiont interactions and immunity to adapt to extreme heat events.Transcriptome sequencing indicated that highly expressed coral host genes in bleached A.pruinosa were mainly associated with disease and autophagy,whereas highly expressed coral host genes in unbleached A.pruinosa were mainly associated with maintaining hostsymbiont relationships and immune defense.C1 was the dominant Symbiodiniaceae clade in both bleached and unbleached A.pruinosa.In addition,the α-diversity of symbiotic bacteria was significantly higher in unbleached than in bleached A.pruinosa.Although both Ralstonia sp.(OTU2147)and Rhodococcus sp.(OTU2162)were the dominant bacteria in both bleached and unbleached A.pruinosa,there were significant differences in their relative abundances.The core bacterial operational taxonomic units(OTUs)that were significantly enriched in unbleached A.pruinosa were mainly related to nitrogen cycle functions,whereas the bacterial OTUs enriched in bleached A.pruinosa were related to antibacterial activity.(3)The higher thermal tolerance in P.decussata as compared to A.pruinosa could be a complex biological process orchestrated by the host,symbiont Symbiodiniaceae,and bacteria.Transcriptome sequencing indicated higher levels of host immunity in P.decussata than in A.pruinosa.With regards to the symbiont Symbiodiniaceae,transcriptome results showed that material transport,catabolism,and photosynthetic biosolidation were more enriched in P.decussata than in A.pruinosa.C1 was the dominant Symbiodiniaceae clade in A.pruinosa and P.decussata.In addition,there were significant differences between the symbiotic bacteria of the two coral species.The symbiotic bacterial α-diversity of P.decussata was higher than that of A.pruinosa.The dominant bacterial genera of A.pruinosa were Ralstonia,Prosthecochloris,BD1-7＿clade,and Acinetobacter,whereas the dominant bacterial genera of P.decussata were BD1-7＿clade,Cohaesibacter,Fusibacter,Vibrio,and Ralstonia.Thus,differences in the bacterial community composition and core bacteria could contribute to the differential adaptation of the two corals to high temperatures.(4)Fluctuating environments,which were viewed as “natural acclimation pools,” can improve coral heat tolerance by regulating the metabolism and immunity of the organism.Transcriptome sequencing indicated that 6.86% of the total transcripts in P.damicornis were generated by alternative splicing,with intron retention being the most prevalent variable shearing form.In total,207,955 alternative polyadenylation sites were identified at 88,092 loci.The KEGG enrichment analysis of lnc RNA-targeted m RNAs showed that the metabolic rate of P.damicornis in fluctuating environments was lower than that in stable environments.In addition,whole-genome bisulfite sequencing analysis showed that the methylation level of P.damicornis was low,with an average of 4.14% and methylation at Cp G,CHH,and CHG sites accounting for 74.88%,13.27%,and11.85% of the total methylation,respectively.There were also differences in the methylation levels in different regions of the gene,with gene body methylation levels being relatively high and exhibiting a bimodal methylation pattern.Within gene bodies,methylation occurs predominantly in the exons.The results of targeted gene KEGG functional enrichment analysis of differentially expressed genes and differential methylated gene association analysis in P.damicornis in fluctuating environments showed the highest proportion of pathways related to immunity compared with those in stable environments.We hypothesize that the dynamic balance of energy–expenditure costs between immunity and metabolism is an important strategy that increases the tolerance of P.damicornis.The fluctuating environment of high-temperature pools may increase heat tolerance in corals by increasing their immunity and thus reducing their metabolism.(5)Thermal acclimation may increase scleractinian coral thermal tolerance by slowing down host metabolism,altering the dominant bacterial population,and increasing bacterial diversity.Transcriptome sequencing suggested that downregulation of the thermal acclimation of A.pruinosa coral host genes was mainly associated with organismal metabolic pathways,particularly those related to nitrogen metabolism.C1 was the dominant Symbiodiniaceae clade of A.pruinosa.Following thermal acclimation,the community structure and symbiotic bacterial α-diversity were reorganized,whereas that of the Symbiodiniaceae remained stable.Symbiotic bacteria can be regulated more rapidly,and in thermal acclimation at 31 °C,the dominant bacterium of A.pruinosa was the norank＿o＿＿Chloroplast and unclassified＿c＿＿Alphaproteobacteria,whereas the dominant bacteria changed to Family＿XII＿o＿＿Clostridiales after thermal acclimation.The results of thermal acclimation simulation experiments further validated the conclusions of the field study indicating that scleractinian corals adapt to hightemperature stress to a certain extent and that this thermal acclimation increases their thermal tolerance.Collectively,these results indicate that coral hosts,symbiotic Symbiodiniaceae,and bacteria are all involved in the adaptation of coral holobionts to high-temperature stress.Coral host metabolism and immune response adjustments help coral holobionts adapt to environmental stress.Symbiotic Symbiodiniaceae density,photosynthetic rates,and transcriptional responses were rapidly adjusted under high-temperature stress;however,the community structure remained relatively stable.Symbiotic bacteria exhibit high plasticity in terms of their α-diversity,composition,and function.These characteristics work together to promote the adaptation of coral holobionts to high-temperature stress.This study systematically analyzed the adaptive mechanism of scleractinian coral holobionts to global warming in the northern South China Sea.This knowledge is crucial for the survival of coral reefs in this region,which are expected to face a more severe environment than this in the near future.