Regional environmental heterogeneity under contrasting anthropogenic pressures has differential effects on particle-attached than free-living bacteria communities in coral reef waters

Coral reef ecosystems are facing increasing environmental and anthropogenic pressures worldwide. Their health and prosperity depend, at least partly, on the surrounding water environment, where the free-living (FL) and particle-attached (PA) bacterial communities play essential yet distinct ecological roles. However, these communities' distributions and variations across coral reef ecosystems with large environmental and anthropogenic gradients remain scarcely understood. In this study, we investigated FL and PA communities in coral reef waters from three regions of the South China Sea (SCS): Hainan, ZhongXisha, and Nansha. Among the various factors influencing bacterial communities, the region exhibited the greatest impact when compared to lifestyle (PA versus FL) and layer (surface versus bottom water). The Hainan waters exhibited higher contents of total organic carbon (TOC) and ammonia yet lower temperature, which likely contributes to the higher alpha diversity and the increase of Alphaproteobacteria and Bacteroidetes. While stochastic processes showed dominance for communities' assembly, the relative importance of homogeneous selection increased particularly for the Hainan PA community. Network analyses showed that the Hainan PA community network was more complex and densely connected than other community networks. The anthropogenic (TOC and ammonia as proxies) and environmental contexts in the region of Hainan may elevate the robustness of the PA network but reduce that of the FL network. In conclusion, our results indicated that the regional environmental heterogeneity under contrasting anthropogenic pressures had differential effects on PA than FL bacteria communities in coral reef waters, which may provide clues for understanding ecosystem resilience and targeted management strategies for coral reef conservation. IMPORTANCE: Particle-attached (PA) and free-living (FL) represent two basic lifestyles for waterborne bacteria. While the knowledge about their differences in community diversity, assembly processes, and network structure is increasing, their variations and responsive patterns in coral reef waters in a large area with environmental heterogeneity and anthropogenic pressure differences remain scarcely understood. Here, we investigated their community dynamics in coral reef waters in the South China Sea. We found that the regional environmental heterogeneity had more prominent effects on PA than FL communities. In Hainan waters with lower temperature and higher contents of TOC and ammonia-N, the PA other than FL communities showed a more connected and robust network structure. The rich organics and specialized microniches within particles might help PA communities adapt and resist environmental perturbations under high anthropogenic pressure. Our results would help provide insights into understanding ecosystem resilience and inform targeted management strategies for coral reef conservation.