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.

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.

Regulation of the Coral-Associated Bacteria and Symbiodiniaceae in Acropora valida Under Ocean Acidification.

Ocean acidification is one of many stressors that coral reef ecosystems are currently contending with. Thus, understanding the response of key symbiotic microbes to ocean acidification is of great significance for understanding the adaptation mechanism and development trend of coral holobionts. Here, high-throughput sequencing technology was employed to investigate the coral-associated bacteria and Symbiodiniaceae of the ecologically important coral Acropora valida exposed to different pH gradients. After 30 days of acclimatization, we set four acidification gradients (pH 8.2, 7.8, 7.4, and 7.2, respectively), and each pH condition was applied for 10 days, with the whole experiment lasting for 70 days. Although the Symbiodiniaceae density decreased significantly, the coral did not appear to be bleached, and the real-time photosynthetic rate did not change significantly, indicating that A. valida has strong tolerance to acidification. Moreover, the Symbiodiniaceae community composition was hardly affected by ocean acidification, with the C1 subclade (Cladocopium goreaui) being dominant among the Symbiodiniaceae dominant types. The relative abundance of the Symbiodiniaceae background types was significantly higher at pH 7.2, indicating that ocean acidification might increase the stability of the community composition by regulating the Symbiodiniaceae rare biosphere. Furthermore, the stable symbiosis between the C1 subclade and coral host may contribute to the stability of the real-time photosynthetic efficiency. Finally, concerning the coral-associated bacteria, the stable symbiosis between Endozoicomonas and coral host is likely to help them adapt to ocean acidification. The significant increase in the relative abundance of Cyanobacteria at pH 7.2 may also compensate for the photosynthesis efficiency of a coral holobiont. In summary, this study suggests that the combined response of key symbiotic microbes helps the whole coral host resist the threats of ocean acidification.

Multi-Omics Revealing the Response Patterns of Symbiotic Microorganisms and Host Metabolism in Scleractinian Coral Pavona minuta to Temperature Stresses.

Global climate change has resulted in large-scale coral reef decline worldwide, for which the ocean warming has paid more attention. Coral is a typical mutually beneficial symbiotic organism with diverse symbiotic microorganisms, which maintain the stability of physiological functions. This study compared the responses of symbiotic microorganisms and host metabolism in a common coral species, Pavona minuta, under indoor simulated thermal and cold temperatures. The results showed that abnormal temperature stresses had unfavorable impact on the phenotypes of corals, resulting in bleaching and color change. The compositions of symbiotic bacteria and dinoflagellate communities only presented tiny changes under temperature stresses. However, some rare symbiotic members have been showed to be significantly influenced by water temperatures. Finally, by using ultra-performance liquid chromatography tandem mass spectrometry (UPLC-MS) method, we found that different temperature stresses had very different impacts on the metabolism of coral holobiont. The thermal and cold stresses induced the decrease of anti-oxidation metabolites, several monogalactosyldiacylglycerols (MGDGs), and the increase of lipotoxic metabolite, 10-oxo-nonadecanoic acid, in the coral holobiont, respectively. Our study indicated the response patterns of symbiotic microorganisms and host metabolism in coral to the thermal and cold stresses, providing theoretical data for the adaptation and evolution of coral to a different climate in the future.

Potential molecular traits underlying environmental tolerance of Pavona decussata and Acropora pruinosa in Weizhou Island, northern South China Sea.

Coral species display varying susceptibilities to biotic or abiotic stress. To address the causes underlying this phenomenon, we profiled the Symbiodiniaceae clade type, bacterial communities and coral transcriptome responses in Pavona decussata and Acropora pruinosa, two species displaying different environmental tolerances in the Weizhou Island. We found that C1 was the most dominant Symbiodiniaceae subclade, with no difference detected between A. pruinosa and P. decussata. Nevertheless, P. decussata exhibited higher microbial diversity and significantly different community structure compared with that of A. pruinosa. Transcriptome analysis revealed that coral genes with significantly high expression in P. decussata were mostly related to immune and stress-resistance responses, whereas, those with significantly low expression were metabolism-related. We postulate that the higher tolerance of P. decussata as compared with that of A. pruinosa is the result of several traits, such as higher microbial diversity, different dominant bacteria, higher immune and stress-resistant response, and lower metabolic rate.