Environmental heterogeneity overrides host phylogenetic distance in shaping the microbiome of Acropora corals

Abstract Coral ecosystems are among the most representative symbiosis systems, with profound scientific significance for understanding the relationships between host and their microbiome. Environmental filtering and host phylogeny play essential roles in maintaining the microbiome of coral holobionts, yet their relative contribution to community assembly remains unsettled. In this study, we analyzed the bacterial composition of 170 samples from 47 Acropora species across two geomorphologically contrasting habitats in the South China Sea, the steep-sloped Meiji Reef and the flat Beiwai Reef. Our results demonstrate that Acropora corals from the two microhabitats host specialized bacterial assemblages distinct from those in the surrounding seawater, which are primarily shaped by deterministic processes. Within Acropora genus, bacterial communities associated with hosts showed significant differences in taxonomic composition between the two habitats, and environmental drivers such as dissolved oxygen and primary production outweighed host phylogenetic signals in shaping bacterial community structure. Despite differences in microbial community composition, similar metabolic pathways were enriched in both habitats, representing core functional stability across environments. Co-occurrence network analysis further revealed that corals in these two habitats employed distinct topological strategies to achieve microbiome functional stability. These findings indicate that taxonomic flexibility combined with functional stability forms a stable yet adaptable strategy, allowing Acropora to adjust to diverse environmental conditions. Our study highlights the vital role of environmental-microbial synergy in coral resilience and offers a theoretical foundation for microbe-informed reef restoration amid rapid global change.