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

ABSTRACT Blue holes are unique marine sinkholes with extreme environments and biogeochemical processes. However, our understanding of community dynamics, functional profiles, and microbial interactions in blue holes remains limited. We studied the extreme environmental response pattern of the microbiome (Symbiodiniaceae, bacteria, archaea, and fungi) across 14 depths in the world’s deepest blue hole, the Sansha Yongle Blue Hole. The α-diversities of Symbiodiniaceae and archaea were stable to extreme environmental conditions, whereas those of bacteria and fungi varied. Physical and nutrient factors primarily influenced the β-diversities of these four microbes, and there were significant differences in microbial communities among water layers. Nine microbial taxa of Cladocopium sp, γ-proteobacteria, Nanoarchaeota, and Ascomycota representing the core microbiome occurred in all water layers. These four microbial groups exhibited potential interactions, with a positive correlation between Symbiodiniaceae and archaea α-diversities. The microbial biogeochemical profiles exhibited notable enrichment characteristics among distinct water layers. Archaea metabolized sulfides in the oxic and upper deep layers, while bacteria dominated sulfide decomposition in the chemocline and lower deep layers. These findings suggest the acclimation of Symbiodiniaceae to an extreme environment may rely on archaea, as a result of a partial niche overlap. The bacterial communities exhibited an environmental response pattern consistent with the Anna Karenina effects, whereas fungal communities displayed an opposite trend. The wide tolerance of the core microbiome to environmental gradients may be linked to evolution, acclimatization, and symbiosis. Bacteria, archaea, and fungi have distinct ecological niches and biogeochemical functions in the Sansha Yongle Blue Hole. 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 β-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.