Host filtering shapes diversity and community stability of Symbiodiniaceae in Tridacna maxima across the Nansha Archipelago in the South China Sea

The giant clam-Symbiodiniaceae symbiosis represents a classic mutualism in coral reef ecosystems, driving photosynthesis and nutrient cycling that fuel reef productivity. However, it remains unclear how association with a host influences the composition and stability of Symbiodiniaceae communities, and the extent to which these communities reflect or diverge from the surrounding free-living pool. Addressing this question, high throughput Symbiodiniaceae ribosome DNA Internal Transcribed Spacer 2 (ITS2) metabarcoding sequencing was performed in 48 seawater and Tridacna maxima mantle samples collected across three atolls of the Nansha Archipelago in the South China Sea. Compared with the highly diverse free-living pool in the surrounding water (680 amplicon sequence variants, ASVs; 11 ITS2 types), symbiotic communities exhibited significantly lower number of Symbiodiniaceae ITS2 types (247 ASVs; five ITS2 types). Free-living communities differed markedly among reefs primarily driven by geographical distance, and concentrations of various nutrients and heavy metals, whereas clam-associated communities remained spatially homogeneous. Symbionts were dominated by Cladocopium C1 and Symbiodinium A3, reflecting the host’s selection of Symbiodiniaceae. Moreover, clam-associated communities were predominantly shaped by deterministic processes and exhibited higher community stability, whereas free-living communities were co-influenced by deterministic and stochastic processes. This low species diversity yet high stability of symbiotic communities implies functional diversity among dominant genera might play a key role in maintaining holobiont resilience, whose stability could be reinforced by the buffered microenvironment created by the giant clam. These findings highlight the importance of host-mediated structuring of Symbiodiniaceae communities for holobiont stability and suggest that maintaining host-symbiont integrity maybe important for reef ecosystem resilience under environmental change.