Microbiome dynamics and multiscale environmental response patterns of later-diverging coral clade across latitudes, reefs and geomorphological zones in the South China Sea

The climatic adaptability and resilience of coral-associated microbiomes are pivotal under the global change. However, the environmental responses and acclimation patterns of microbiome within corals from the latest clades across multiple spatial scales remain unclear. This study analyzed the community and function characteristics of Symbiodiniaceae and bacteria in Lithophyllon scabra (latest-diverging clade of Fungiidae) across latitudes, reefs and geomorphological zones in the South China Sea. The results showed that L.scabra acclimated to environmental variation at multiple spatial scales by establishing specific symbioses with C27 sub-clade. The deterministic assembly of Symbiodiniaceae was associated with nutrient declines at latitudinal scales, while at reefal and geomorphological scales, it is driven by climatic factors and their interactions with local effects, respectively. However, the stochastic process of Symbiodiniaceae was shaped by symbionts dispersal across multiple spatial scales. Notably, environment filtration entirely governed the bacterial assembly process. At latitudinal and reefal scales, the environmental effects and responses pattern of bacterial community aligned with “Pierre Cardin principle” and “Anna Karenina principle”, respectively. Interestingly, bacterial community was enriched with nitrogen-metabolizing taxa and photoautotrophic functions in the lagoon, while exhibiting a higher abundance of heterotrophic functions and antibacterial taxa on the reef slope, which suggests that changes in nutritional patterns and composition of the bacterial community were crucial for the acclimation of L. scabra to distinct geomorphological zones. These results provide novel insights into the environmental interactions and adaptive strategies of the microbiome associated with younger clades of coral across multiple spatial scales in the context of climate change. • L. scabra respond to multiple changes via specific symbioses of Symbiodiniaceae. • Multiple environment variation and dispersal are closely link to symbiont assembly. • Latitudinal and reefal impact on bacteria is consistent with the Pierre Cardin Principle. • Environment response pattern of bacterial align with Anna Karenina Principle. • Shift of nutrition pattern in bacteria driver geomorphic acclimation of L. scabra .