The microbiome dynamics and interaction of endosymbiotic Symbiodiniaceae and fungi are associated with thermal bleaching susceptibility of coral holobionts.

The thermal bleaching percentage of coral holobionts shows interspecific differences under heat-stress conditions, which are closely related to the coral-associated microbiome. However, the ecological effects of community dynamics and interactions between Symbiodiniaceae and fungi on coral thermal bleaching susceptibility remain unclear. In this study, we analyzed the diversity, community structure, functions, and potential interaction of Symbiodiniaceae and fungi among 18 coral species from a high thermal bleaching risk atoll using next-generation sequencing. The results showed that heat-tolerant C3u sub-clade and Durusdinium dominated the Symbiodiniaceae community of corals and that there were no core amplicon sequence variants in the coral-associated fungal community. Fungal richness and the abundance of confirmed functional animal-plant pathogens were significantly positively correlated with the coral thermal bleaching percentage. Fungal indicators, including Didymellaceae, Chaetomiaceae, Schizophyllum, and Colletotrichum, were identified in corals. Each coral species had a complex Symbiodiniaceae-fungi interaction network (SFIN), which was driven by the dominant Symbiodiniaceae sub-clades. The SFINs of coral holobionts with low thermal bleaching susceptibility exhibited low complexity and high betweenness centrality. These results indicate that the extra heat tolerance of coral in Huangyan Island may be linked to the high abundance of heat-tolerant Symbiodiniaceae. Fungal communities have high interspecific flexibility, and the increase of fungal diversity and pathogen abundance was correlated with higher thermal bleaching susceptibility of corals. Moreover, fungal indicators were associated with the degrees of coral thermal bleaching susceptibility, including both high and intermediate levels. The topological properties of SFINs suggest that heat-tolerant coral have limited fungal parasitism and strong microbial network resilience.IMPORTANCEGlobal warming and enhanced marine heatwaves have led to a rapid decline in coral reef ecosystems worldwide. Several studies have focused on the impact of coral-associated microbiomes on thermal bleaching susceptibility in corals; however, the ecological functions and interactions between Symbiodiniaceae and fungi remain unclear. We investigated the microbiome dynamics and potential interactions of Symbiodiniaceae and fungi among 18 coral species in Huangyan Island. Our study found that the Symbiodiniaceae community of corals was mainly composed of heat-tolerant C3u sub-clade and Durusdinium. The increase in fungal diversity and pathogen abundance has close associations with higher coral thermal bleaching susceptibility. We first constructed an interaction network between Symbiodiniaceae and fungi in corals, which indicated that restricting fungal parasitism and strong interaction network resilience would promote heat acclimatization of corals. Accordingly, this study provides insights into the role of microorganisms and their interaction as drivers of interspecific differences in coral thermal bleaching.

Evolutionary radiation and microbial community dynamics shape the thermal tolerance of Fungiidae in the southern South China Sea.

Fungiidae have shown increased thermal adaptability in coral reef ecosystems under global warming. This study analyzes the evolutionary divergence and microbial communities of Fungiidae in the Sanjiao Reef of the southern South China Sea and explores the impact of coral evolution radiation and microbial dynamics on the heat tolerance of Fungiidae. The results found that Cycloseris was an ancient branch of Fungiidae, dating back approximately 147.8953 Mya, and Fungiidae differentiated into two ancestral clades (clades I and II) before 107.0312 Ma. Fungiidae exhibited specific symbioses with the Cladocopium C27 sub-clade. Notably, the Cladocopium C1 sub-clade has a high relative abundance in clade I, whereas the heat-tolerant Cladocopium C40 and C3u sub-clades subdominante in clade II. Regarding bacterial communities, Cycloseris costulata, the earliest divergent species, had higher bacterial ß-diversity, while the latest divergent species, Lithophyllon scabra, displayed lower bacterial α-diversity and higher community stability. Beneficial bacteria dominante Fungiidae's bacterial community (54%). The co-occurrence network revealed that microbial networks in clade II exhibited lower complexity and greater resilience than those in clade I. Our study highlights that host evolutionary radiation and microbial communities shaped Fungiidae's thermal tolerance. The variability in subdominant Symbiodiniaceae populations may contribute to interspecific differences in thermal tolerance along the evolutionary branches of Fungiidae. The presence of abundant beneficial bacteria may further enhance the thermal ability of the Fungiidae. Furthermore, the later divergent species of Fungiidae have stronger heat tolerance, possibly driven by the increased regulation ability of the host on the bacterial community, greater microbial community stability, and interaction network resistance.IMPORTANCECoral reefs are facing significant threats due to global warming. The heat tolerance of coral holobionts depends on both the coral host and its microbiome. However, the association between coral evolutionary radiation and interspecific differences in microbial communities remains unclear. In this study, we investigated the role of evolutionary radiation and microbial community dynamics in shaping the thermal acclimation potential of Fungiidae in the Sanjiao Reef of the southern South China Sea. The study's results suggest that evolutionary radiation enhances the thermal tolerance of Fungiidae. Fungiidae species that have diverged more recently have exhibited a higher presence of heat-tolerant Symbiodiniaceae taxa, more stable bacterial communities, and a robust and resilient microbial interaction network, improving the thermal adaptability of Fungiidae. In summary, this study provides new insights into the thermal adaptation patterns of corals under global warming conditions.

Metabolic and immune costs balance during natural acclimation of corals in fluctuating environments.

Epigenetic modifications based on DNA methylation can rapidly improve the potential of corals to adapt to environmental pressures by increasing their phenotypic plasticity, a factor important for scleractinian corals to adapt to future global warming. However, the extent to which corals develop similar adaptive mechanisms and their specific adaptation processes remain unclear. Here, to reveal the regulatory mechanism by which DNA methylation improves thermal tolerance in Pocillopora damicornis under fluctuating environments, we analyzed genome-wide DNA methylation signatures in P. damicornis and compared the differences in the methylation and transcriptional responses of P. damicornis from fluctuating and stable environments using whole-genome bisulfite sequencing and nanopore-based RNA sequencingtranscriptome sequencing. We discovered low methylation levels in P. damicornis (average methylation 4.14%), with CpG accounting for 74.88%, CHH for 13.27%, and CHG for 11.85% of this methylation. However, methylation levels did not change between coral samples from the fluctuating and stable environments. The varied methylation levels in different regions of the gene revealed that the overall methylation level of the gene body was relatively high and showed a bimodal methylation pattern. Methylation occurs primarily in exons rather than introns within the gene body In P. damicornis, there was only a weak correlation between methylation and transcriptional changes at the individual gene level, and the methylation and gene expression levels generally exhibited a bell-shaped relationship, which we speculate may be due to the specificity of cnidarian species. Correlation analysis between methylation levels and the transcriptome revealed that the highest proportion of the top 20 enriched KEGG pathways was related to immunity. Additionally, P. damicornis collected from a high-temperature pool had a lower metabolic rate than those collected from a low-temperature pool. We hypothesize that the dynamic balance of energy-expenditure costs between immunity and metabolism is an important strategy for increasing P. damicornis tolerance. The fluctuating environment of high-temperature pools may increase the heat tolerance in corals by increasing their immunity and thus lowering their metabolism.

The diversity, community dynamics, and interactions of the microbiome in the world's deepest blue hole: insights into extreme environmental response patterns and tolerance of marine microorganisms.

IMPORTANCE: This study comprehensively examined the community dynamics, functional profiles, and interactions of the microbiome in the world's deepest blue hole. The findings revealed a positive correlation between the α-diversities of Symbiodiniaceae and archaea, indicating the potential reliance of Symbiodiniaceae on archaea in an extreme environment resulting from a partial niche overlap. The negative association between the α-diversity and ß-diversity of the bacterial community suggested that the change rule of the bacterial community was consistent with the Anna Karenina effects. The core microbiome comprised nine microbial taxa, highlighting their remarkable tolerance and adaptability to sharp environmental gradient variations. Bacteria and archaea played significant roles in carbon, nitrogen, and sulfur cycles, while fungi contributed to carbon metabolism. This study advanced our understanding of the community dynamics, response patterns, and resilience of microorganisms populating the world's deepest blue hole, thereby facilitating further ecological and evolutional exploration of microbiomes in diverse extreme environments.

Adaptation strategies of relatively high-latitude marginal reef corals in response to severe temperature fluctuations.

The large seasonal temperature fluctuations caused by global warming and frequent marine heatwaves pose new challenges to survival of relatively high-latitude marginal reef corals. However, the adaptation strategies of high-latitude marginal corals are not fully understood. We employed integrated approach to investigate the response mechanism of hosts, Symbiodiniaceae, and symbiotic bacteria of marginal reef corals Acropora pruinosa and Pavona decussate in response to large seasonal temperature fluctuations. The coral holobiont maintained a high level of immunity to adapt to seasonal pressure by increasing Symbiodiniaceae energy supply. The symbiotic Symbiodiniaceae of two coral was dominated by C1 subgroup, and was stable across seasons. The α-diversity of symbiotic bacteria P. decussata and A. pruinosa in summer was higher than that in winter. The symbiotic bacterial community of two coral reorganized during different seasons. Scleractinian corals improve adaptability to seasonal stress by increasing energy supply to maintain high levels of immunity, increasing symbiotic bacterial α-diversity, and changing dominant bacteria. This study demonstrates the adaptation strategies of marginal reef corals to seasonal temperature fluctuations and provides novel insights into the study of the adaptation of corals and relatively high-latitude coral refuges in the context of global warming and intensified marine heatwaves.

Metabolomics Characterization of Scleractinia Corals with Different Life-History Strategies: A Case Study about Pocillopora meandrina and Seriatopora hystrix in the South China Sea.

Life-history strategies play a critical role in susceptibility to environmental stresses for Scleractinia coral. Metabolomics, which is capable of determining the metabolic responses of biological systems to genetic and environmental changes, is competent for the characterization of species' biological traits. In this study, two coral species (Pocillopora meandrina and Seriatopora hystrix in the South China Sea) with different life-history strategies ("competitive" and "weedy") were targeted, and untargeted mass spectrometry metabolomics combined with molecular networking was applied to characterize their differential metabolic pathways. The results show that lyso-platelet activating factors (lyso-PAFs), diacylglyceryl carboxyhydroxymethylcholine (DGCC), aromatic amino acids, and sulfhydryl compounds were more enriched in P. meandrina, whereas new phospholipids, dehydrated phosphoglycerol dihydroceramide (de-PG DHC), monoacylglycerol (MAG), fatty acids (FA) (C < 18), short peptides, and guanidine compounds were more enriched in S. hystrix. The metabolic pathways involved immune response, energy metabolism, cellular membrane structure regulation, oxidative stress system, secondary metabolite synthesis, etc. While the immune system (lysoPAF) and secondary metabolite synthesis (aromatic amino acids and sulfhydryl compounds) facilitates fast growth and resistance to environmental stressors of P. meandrina, the cell membrane structure (structural lipids), energy storage (storage lipids), oxidative stress system (short peptides), and secondary metabolite synthesis (guanidine compounds) are beneficial to the survival of S. hystrix in harsh conditions. This study contributes to the understanding of the potential molecular traits underlying life-history strategies of different coral species.

Significant Changes in Bacterial Communities Associated with Pocillopora Corals Ingestion by Crown-of-Thorns Starfish: An Important Factor Affecting the Coral's Health.

Coral ingestion by crown-of-thorns starfish (COTS) is an important cause of coral reef degradation, although the impacts of COTS feeding on coral-associated microbial communities are not well understood. Therefore, in this study, we analyzed the coral tissue-weight, Symbiodiniaceae density (SD), bacterial community composition, and the predicted functions of bacterial genes associated with Pocillopora corals in healthy portions and feeding scars, following COTS feeding. Coral tissue-weight loss rate in the feeding scars was 71.3-94.95%. The SDs were significantly lower in the feeding scars, and the SD-loss rate was 92.05% ± 2.12%. The relative abundances of bacterial communities associated with Pocillopora corals after COTS feeding changed significantly and were almost completely reorganized at the phylum and genus levels. Analysis of the microbial metagenomic-functional capacities showed that numerous physiological functions of the coral-bacterial holobionts in the feeding scars were different, including amino acid metabolism, xenobiotic biodegradation and metabolism, lipid metabolism, membrane transport, signal transduction, and cell motility, and all these capacities could be corroborated based on metagenomic, transcriptomic or proteomic technologies. Overall, our research suggests that coral holobionts may be destroyed by COTS, and our findings imply that bacterial communities in feeding scars could affect the health of Pocillopora corals.

Cross-Linked Regulation of Coral-Associated Dinoflagellates and Bacteria in Pocillopora sp. during High-Temperature Stress and Recovery.

As the problem of ocean warming worsens, the environmental adaptation potential of symbiotic Symbiodiniaceae and bacteria is directly related to the future and fate of corals. This study aimed to analyse the comprehensive community dynamics and physiology of these two groups of organisms in the coral Pocillopora sp. through indoor simulations of heat stress (which involved manually adjusting the temperature between both 26 °C and 34 °C). Heat treatment (≥30 °C) significantly reduced the abundance of Symbiodiniaceae and bacteria by more than 70%. After the temperature was returned to 26 °C for one month, the Symbiodiniaceae density was still low, while the absolute number of bacteria quickly recovered to 55% of that of the control. At this time point, the Fv/Fm value rose to 91% of the pretemperature value. The content of chlorophyll b associated with Cyanobacteria increased by 50% compared with that under the control conditions. Moreover, analysis of the Symbiodiniaceae subclade composition suggested that the relative abundance of C1c.C45, C1, and C1ca increased during heat treatment, indicating that they might constitute heat-resistant subgroups. We suggest that the increase in the absolute number of bacteria during the recovery period could be an important indicator of coral holobiont recovery after heat stress. This study provides insight into the cross-linked regulation of key symbiotic microbes in the coral Pocillopora sp. during high-temperature stress and recovery and provides a scientific basis for exploring the mechanism underlying coral adaptation to global warming.

Microbiome of juvenile corals in the outer reef slope and lagoon of the South China Sea: insight into coral acclimatization to extreme thermal environments.

Environmental conditions between the outer reef slope (ORS) and lagoon in tropical atolls are significantly different, but the variations of juvenile coral-microbiomes in the two environments and their relationship with coral thermal acclimatization are poorly understood. We explored this issue based on local water conditions and the microbiome of juvenile corals in the ORS and lagoon in the central South China Sea. Coral-symbiotic Symbiodiniaceae showed significant differences among coral species; Pocillopora verrucosa and Pachyseris rugosa in the ORS, and Acropora formosa in the lagoon were dominated by Durusdinium, but other corals were dominated by Cladocopium. Although A. formosa in the ORS were dominated by Cladocopium (C3u), they were dominated by Durusdinium (D1/D1a) and Cladocopium (C50) in the lagoon. Other coral species were both dominated by Cladocopium in the lagoon and ORS. The relative abundance of bacteria in the Deinococcus-Thermus was generally higher in the lagoon corals than in the ORS corals. Our study indicates that P. verrucosa, P. rugosa and Porites lutea may have high thermal tolerance based on the relatively high abundance of heat-tolerant Durusdinium and Thermus scotoductus. Likewise, A. formosa in the lagoon may acclimatize to the thermal environment based on a high relative abundance of heat-tolerant Durusdinium.

Seasonal fluctuations in symbiotic bacteria and their role in environmental adaptation of the scleractinian coral Acropora pruinosa in high-latitude coral reef area of the South China Sea.

Coral-associated bacterial communities are paramount for coral ecosystems and holobiont health. However, the role of symbiotic bacteria in the adaptation of high-latitude corals to seasonal fluctuations remains underexplored. Therefore, we used 16S rRNA-based high-throughput sequencing to analyze the symbiotic bacterial diversity, composition, and core bacterial community in high-latitude coral and explored the seasonal fluctuation characteristics of symbiotic bacterial communities. We found that bacterial richness and α-diversity changed significantly across different seasons. Additionally, the community structure recombined seasonally, with different dominant bacterial phyla and genera in different seasons. However, the symbiotic bacterial community structures of Acropora pruinosa in winter and spring were similar. Proteobacteria were the dominant bacteria in spring, autumn, and winter. In summer, the dominant bacterial taxa were Bacteroidota and Proteobacteria. Ralstonia was the dominant bacterial genus in spring and winter, whereas in autumn, BD1-7_clade was dominant. Linear discriminant analysis effect size identified 20 abundant genera between the different groups. Core microbiome analysis revealed that 12 core bacterial operational taxonomic units were associated with A. pruinosa in all seasons, seven of which varied with the seasons, changing between dominant and rare. Distance-based redundancy and variation partitioning analyses revealed that sea surface temperature was the major contributor of variation in the microbial community structure. We hypothesized that the high diversity and abundance of symbiotic bacteria and the increase in Prosthecochloris abundance in coral in summer can help A. pruinosa maintain its physiological functions, ameliorating the negative physiological effects of the decrease in Symbiodiniaceae density under high-temperature stress. Thus, the rapid reorganization of the symbiotic bacterial community structure and core microflora in different seasons may allow the corals to adapt to large seasonal environmental fluctuations. In conclusion, seasonal variation of bacteria plays an important role in coral adaptation to large environmental fluctuations.

Nanopore long-read RNAseq reveals regulatory mechanisms of thermally variable reef environments promoting heat tolerance of scleractinian coral Pocillopora damicornis.

Some scleractinian corals exhibit high thermal adaptability to climate changes, although the mechanism of their adaptation is unclear. This study investigated the adaptability of scleractinian coral Pocillopora damicornis to thermally variable reef environments by applying a nanopore-based RNA sequencing method to characterize different transcription responses that promote heat tolerance of P. damicornis. We identified 1414 novel genes and optimized 6256 mis-annotated loci. Based on full-length transcriptome data, we identified complex alternative polyadenylation and alternative splicing events, which can improve our understanding of the genome annotation and gene structures of P. damicornis. Furthermore, we constructed differentially expressed lncRNA-mRNA co-expression networks, which may play a crucial role in the P. damicornis thermal adaptive response. KEGG function enrichment analysis revealed that P. damicornis from the high-temperature pool had a lower metabolic rate than that from the low-temperature pool. We hypothesize that metabolic readjustment, in the form of a lower metabolic rate, positively correlated with increased heat tolerance in P. damicornis in thermally variable reef environments. Our study provides novel insights into lncRNAs that promote thermally tolerance of scleractinian corals in the thermally variable reef environment, suggesting potential mechanisms for their adaptation to global warming in the future.

Microbiome community and complexity indicate environmental gradient acclimatisation and potential microbial interaction of endemic coral holobionts in the South China Sea.

Regional acclimatisation and microbial interactions significantly influence the resilience of reef-building corals facing anthropogenic climate change, allowing them to adapt to environmental stresses. However, the connections between community structure and microbial interactions of the endemic coral microbiome and holobiont acclimatisation remain unclear. Herein, we used generation sequencing of internal transcribed spacer (ITS2) and 16S rRNA genes to investigate the microbiome composition (Symbiodiniaceae and bacteria) and associated potential interactions of endemic dominant coral holobionts (Pocillopora verrucosa and Turbinaria peltata) in the South China Sea (SCS). We found that shifts in Symbiodiniaceae and bacterial communities of P. verrucosa were associated with latitudinal gradient and climate zone changes, respectively. The C1 sub-clade consistently dominated the Symbiodiniaceae community in T. peltata; yet, the bacterial community structure was spatially heterogeneous. The relative abundance of the core microbiome among P. verrucosa holobionts was reduced in the biogeographical transition zone, while bacterial taxa associated with anthropogenic activity (Escherichia coli and Sphingomonas) were identified in the core microbiomes. Symbiodiniaceae and bacteria potentially interact in microbial co-occurrence networks. Further, increased bacterial, and Symbiodiniaceae α-diversity was associated with increased and decreased network complexity, respectively. Hence, Symbiodiniaceae and bacteria demonstrated different flexibility in latitudinal or climatic environmental regimes, which correlated with holobiont acclimatisation. Core microbiome analysis has indicated that the function of core bacterial microbiota might have changed in distinct environmental regimes, implying potential human activity in the coral habitats. Increased bacterial α diversity may lead to a decline in the stability of coral-microorganism symbioses, whereas rare Symbiodiniaceae may help to retain symbioses. Cladocopium, γ-proteobacteria, while α-proteobacteria may have been the primary drivers in the Symbiodiniaceae-bacterial interactions (SBIs). Our study highlights the association between microbiome shift in distinct environmental regimes and holobiont acclimatisation, while providing insights into the impact of SBIs on holobiont health and acclimatisation during climate change.

Intergeneric and geomorphological variations in Symbiodiniaceae densities of reef-building corals in an isolated atoll, central South China Sea.

The healthy status of corals in the isolated atolls of the central South China Sea (SCS) remains unclear. Symbiodiniaceae density (SD) can effectively reflect the thermal tolerance and health of hard corals. Here, the SDs of 238 samples from the Huangyan Atoll (HA) were analyzed. The results revealed significantly intergeneric and geomorphological differences in SD. Intergeneric variation may reflect that corals with high SD have stronger thermal tolerance. Geomorphic analysis showed that the SDs at the outer reef slope were higher than in the lagoon. Hydrodynamics and sea surface temperature were likely the main influencing factors. Most notably, corals in SCS HA had higher SDs than those at neighboring reefs, indicating that their thermal tolerance were strong, which may be related to HA's local upwelling. These results suggest that the HA has the potential to serve as a refuge for corals, but increasing human disturbance limit its function.

Diazotroph Diversity Associated With Scleractinian Corals and Its Relationships With Environmental Variables in the South China Sea.

Coral reef ecosystems cannot operate normally without an effective nitrogen cycle. For oligotrophic coral reef areas, coral-associated diazotrophs are indispensable participants in the nitrogen cycle. However, the distribution of these diazotrophs and the correlation with the physical and chemical variables of the surrounding seawater remain unclear. To this end, 68 scleractinian coral colonies were sampled from 6 coral reef areas with different environmental variables in the South China Sea to investigate the composition of associated diazotrophs based on nifH gene amplification using high-throughput sequencing. The six coral reefs can be clearly divided into two types (fringing reefs and island reefs), are affected by varying degrees of human activities and are located at different latitudes from 9°20'06"N to 22°34'55"N with different seawater temperatures. Alpha- and beta-diversity analyses showed that the distribution of diazotrophs among coral reefs exhibited significant geographical fluctuations (p ≤ 0.05) and non-significant interspecific fluctuations (p > 0.05). The predominant bacterial phyla included Proteobacteria, Chlorobi, Cyanobacteria, and two unclassified phyla. Chlorobi exhibited a relative abundance of 47-96% in coral samples from the high-latitude Daya Bay fringing reef affected by eutrophication. Unclassified bacteria II, with a relative abundance of 28-87%, was found in all coral samples from the midlatitude Luhuitou fringing reef affected by eutrophication. However, unclassified bacteria I and Proteobacteria dominated (>80% relative abundance) in most of the coral samples from the Weizhou Island fringing reef, which is far from land, and three island reefs (Huangyan Island, Xinyi Reef, and Sanjiao Reef) at relatively low latitudes. At the genus level, some core diazotrophs were found in different coral sample groups. In addition, correlation analysis with various environmental variables revealed that the variables were positively or negatively correlated with different diazotrophic genera. Coral-associated diazotrophs were common among coral individuals. However, their composition was closely related to the different environmental variables. These results provide insights into the geographical distribution characteristics of coral-associated diazotrophs and their evolutionary trends in response to environmental change in the South China Sea.

Thermal acclimation increases heat tolerance of the scleractinian coral Acropora pruinosa.

Field ecological observations indicate that scleractinian coral exposed to early thermal stress are likely to develop higher tolerance to subsequent heat stress. The causes of this phenomenon, however, remain enigmatic. To unravel the mechanisms underlying the increased heat tolerance, we applied different thermal treatments to the scleractinian coral Acropora pruinosa and studied the resulting differences in appearance, physiological index, Symbiodiniaceae and bacterial communities, and transcriptome response. We found that early heat stress improved the thermal tolerance of the coral holobiont. After thermal acclimation, the community structure and symbiotic bacterial diversity in the microbiota were reorganized, whereas those of Symbiodiniaceae remained stable. RNA-seq analysis revealed that the downregulated coral host genes were mainly involved in pathways relating to metabolism, particularly the nitrogen metabolism pathway. This indicates that thermal acclimation led to decrease in the metabolism level in the coral host, which might be a self-protection mechanism. We suggest that thermal acclimation may increase scleractinian coral thermal tolerance by slowing host metabolism, altering the dominant bacterial population, and increasing bacterial diversity. This study offers new insights into the adaptive potential of scleractinian coral to heat stress from global warming.

Dispersal, genetic variation, and symbiont interaction network of heat-tolerant endosymbiont Durusdinium trenchii: Insights into the adaptive potential of coral to climate change.

Global warming has degraded coral reef ecosystems worldwide. Some corals develop thermal tolerance by associating with heat-tolerant Symbiodiniaceae. Here, we studied the mechanisms surrounding the dispersal, genetic variation and symbionts interaction of heat-tolerant Durusdinium trenchii across 13° latitudes in the South China Sea (SCS), to explore the possible mechanisms underlying these changes. Our results showed that Durusdinium trenchii are widely distributed in the seawater from the SCS. Our analyses of microsatellite loci revealed that D. trenchii has a high genetic diversity in the SCS; STRUCTURE analysis indicated that D. trenchii can be divided into four populations within the SCS; There exist positive correlations between genetic variation and geographic isolation, average sea surface temperature (SST) and variations in SST. Network modelling inferences showed that D. trenchii is a key species in the Symbiodiniaceae communities in the tropical SCS and contributes the greatest number of co-exclusion relationships. These results indicated that D. trenchii can affect the rare Symbiodiniaceae community. The long lifespan and the monsoon-driven ocean currents have shaped the wide distribution of D. trenchii. But low SST limits the ability of D. trenchii to establish stable symbioses with coral in the subtropical habitats. Geographical isolation and SST have shaped significant genetic variation of D.trenchii around the SCS. Our data reveals the biogeography and genetic population characteristics of D. trenchii in the Indo-Pacific region, and suggests that heat-tolerance and high genetic diversity of D. trenchii aid the corals with their adaptation to climate change.

Latitudinal variation in reef coral tissue thickness in the South China Sea: Potential linkage with coral tolerance to environmental stress.

Coral tissue thickness (CTT) is an effective indicator of the adaptability of corals to environmental stress, but the relationships between the spatial and intergeneric variation of coral tissue across latitudes and tolerance to environmental stress are not well understood. To investigate this, the CTT of 768 specimens of 10 typical coral genera and surrounding seawater parameters were measured in six coral reef regions (CRRs) across the 9-22°N latitudes in the South China Sea (SCS). Results showed significant differences in CTT between different genera of corals and CRRs. CTTs were significantly higher in the northern SCS than in the southern SCS. There was also notable intergeneric variation, with the abundance of branching Acropora and foliaceous Pavona being significantly lower than that of massive Porites, Galaxea, Favia, Favites, Hydnophora, Platygyra, and encrusting Montipora, Psammocora across these CRRs. Redundancy analysis showed that dissolved inorganic nitrogen (DIN), soluble reactive phosphorus (SRP), sea surface temperature (SST), turbidity, and transparency were the main factors affecting CTT. Overall CTT, irrespective of genus, was significantly positively correlated with DIN, SRP, and latitude, but was significantly negatively correlated with transparency and SST. Further analysis suggested that corals in the southern SCS are mainly threatened by thermal stress, whereas in the northern SCS, corals have often suffered from destructive anthropogenic disturbance. Although seawater conditions were normal during on-site investigation, a large number of branching corals (e.g., Acropora corals) have been lost in the last several decades due to destructive human activity. In contrast, massive and encrusting corals may have higher energy reserves and photo-protective capacities due to their thicker tissues, and consequently have higher tolerance to environmental stress. Therefore, the coral communities of the SCS have gradually been transformed from branching corals to massive/encrusting corals.

Diversity of Symbiodiniaceae in 15 Coral Species From the Southern South China Sea: Potential Relationship With Coral Thermal Adaptability.

It is well-known that the adaptability of coral-Symbiodiniaceae symbiosis to thermal stress varies among coral species, but the cause and/or mechanism behind it are not well-understood. In this study, we aimed to explore this issue based on zooxanthellae density (ZD) and Symbiodiniaceae genus/subclade. Hemocytometry and next-generation sequencing of the internal transcribed spacer region 2 (ITS2) marker gene were used to observe ZDs and Symbiodiniaceae genera/subclades associated with 15 typical coral species in the southern South China Sea (SCS). Average ZDs of all corals were in low levels, ranging from 0.84 to 1.22 × 106 cells cm-2, with a total of five Symbiodiniaceae genera, Symbiodinium, Cladocopium, Durusdinium, Fugacium, and Gerakladium, as well as 24 dominant subclades, were detected and varied among these coral species. Pocillopora verrucosa was dominated by Durusdinium (subclade D1/D1a), and other colonial corals were dominated by Cladocopium, but the subclades were varied among these species. Porites lutea and Montipora efflorescens were dominated by C15, and Echinopora lamellosa, Hydnophora exesa, and Coscinaraea exesa were dominated by C40. Acropora corymbosa, Merulina ampliata, and five species of Faviidae were mainly associated with Cladocopium types of C3u and Cspc. In contrast to other colonial corals, the dominant subclade of solitary Fungia fungites was C27, with high host specificity. Our study indicates that coral thermal stress adaptability is mainly affected by dominant Symbiodiniaceae type instead of ZD in the southern SCS. Some heat-sensitive corals, such as P. verrucosa corals, have acquired a high abundance of heat-tolerant Durusdinium to adapt to thermal stress. This could be the main reason for these corals becoming the dominant corals in this reef region. Background subclades analyses showed significant differences among coral species in subclade quantity and diversity. These suggest that numbers of coral species may have adapted to high environmental temperature by adopting various symbionts and/or associating with heat-tolerant Symbiodiniaceae.

Potential impacts of anthropogenic nutrient enrichment on coral reefs in the South China Sea: evidence from nutrient and chlorophyll a levels in seawater.

Anthropogenic nutrient enrichment is considered to be one of the causes resulting in coral reef decline. In order to better understand the trophic status and to further explore the potential impacts of nutrients on the coral reef decline in the South China Sea (SCS), we investigated the nutrient and chlorophyll a (chl a) distributions in the surface water of reef areas across latitudes from 9-22° of the SCS. The results showed that nutrient and chl a concentrations in coastal reefs were obviously higher than those in the central and southern basin. Meanwhile, the investigation of two long-distance transects revealed an inshore-offshore nutrient decreasing trend. However, some offshore coral reefs, such as Yongxing Island, Huaguang Reef and Huangyan Island, were exceptions with relatively higher concentrations than in the surrounding reefs because of the ever-increasing human activity. Compared to other coral reefs worldwide, the nutrient concentration in reef regions of the northern and central SCS was obviously higher than that in healthy coral reefs, approaching that in unhealthy reef areas, which suggested that the present nutrient concentration may reach a risky level. Field survey showed a high ratio of macroalgal cover and coral cover in these reefs, and the significant correlation between the nutrient level and macroalgal cover indicated that elevated nutrients resulted in the phase shift from coral-dominated to macroalgal-dominated reef areas. On the other hand, a significant positive correlation between chl a in lagoons and the volume of lagoons indicated that the structural properties of large lagoons could enhance retention of nutrients and promote the growth of macroalgae, and human disturbance may aggravate the macroalgal overgrowth. Overall, anthropogenic nutrient enrichment has caused negative impacts on coral reefs of the SCS, such as regional macroalgal blooms in coastal reefs and disturbed remote reefs.

Latitudinal Variation in the Molecular Diversity and Community Composition of Symbiodiniaceae in Coral From the South China Sea.

Coral reefs are continuing to decline worldwide due to anthropogenic climate change. The study of the molecular diversity and biogeographical patterns of Symbiodiniaceae, is essential to understand the adaptive potential and resilience of coral-algal symbiosis. Next generation sequencing was used to analyze the Symbiodiniaceae rDNA internal transcribed spacer 2 marker genes from 178 reef-building coral samples in eight coral habitats across approximately 13° of latitude in the South China Sea (SCS). A total of three Symbiodiniaceae genera, Cladocopium, Durusdinium, and Gerakladium, as well as 31 dominant Symbiodiniaceae types, were identified. Symbiodiniaceae richness, diversity, and community composition varied according to latitude; intermediate and low latitude coral reefs (IR and LR) have higher Symbiodiniaceae richness and diversity than high latitude coral habitats (HC and HR). A PERMANOVA analysis found significant differences in the Symbiodiniaceae community composition in the SCS (F = 14.75, R 2 = 0.20, p = 0.001 < 0.01). The major dominant Symbiodiniaceae types were C1 in the HC and the HR, C1/Cspc/C50/C15 and D1 in the IR, and C3u and C15 in the LR. Canonical correspondence analysis showed that the relative abundance of different Symbiodiniaceae types is affected by multiple environmental factors. Phylogenetic analysis indicated that the Symbiodiniaceae type Cladocopium, which shared common ancestors, shows similar environmental adaptability. Based on these results, we suggest that coral host species played a relatively small role in the identity of the dominant Symbiodiniaceae type. Therefore, the biogeographical patterns of Symbiodiniaceae may be mainly affected by environmental factors. Our research provides a comprehensive overview of the biogeography of Symbiodiniaceae in the SCS, where coral communities and reefs are widely distributed across different latitude regions and have variable environmental conditions. Our data will provide support for further study of the regional diversification of Symbiodiniaceae and the ecological resilience of the coral-Symbiodiniaceae symbioses.