White syndrome dynamics in Porites cylindrica: interactions among eutrophication, host structure, and microbial communities

Abstract

Coral white syndromes are among the most prevalent diseases affecting Indo-Pacific reefs, yet their etiology remains poorly understood, particularly in relation to eutrophication and microbial dynamics. Here, we investigated the drivers of Porites cylindrica white syndrome (PCYLWS) across two reef sites in Guam differing in nutrient enrichment and disease pressure. We combined 14 years of long-term disease monitoring with short-term lesion tracking, microbial community profiling of coral tissue and surrounding environments, and measurements of nutrient and environmental conditions. Long-term prevalence of PCYLWS was consistently higher at the oligotrophic site (Luminao) than at the eutrophic site (Tumon Bay), largely due to differences in host size structure and colony abundance. In contrast, lesions at Tumon Bay were larger and rapidly colonized by turf algae, whereas lesions at Luminao progressed faster but stabilized at smaller sizes. Microbial communities were strongly structured by sample type, with distinct assemblages in seawater, sediment, healthy tissue, and diseased tissue. Diseased tissues exhibited high spatial and temporal variability and signatures of microbial dysbiosis, characterized by reduced dominance of Parendozoicomonas and increased relative abundance of opportunistic taxa, including Ruegeria, Muricauda, and Vibrio. Environmental microbial communities and nutrient concentrations varied seasonally, particularly at the eutrophic site, suggesting transient environmental reservoirs of opportunistic bacteria. Together, these findings indicate that PCYLWS is shaped by context-dependent interactions among host population structure, environmental conditions, and dynamic microbial communities, supporting a multi-etiology framework for coral white syndromes. ImportanceCoral white syndromes are among the most common yet least mechanistically resolved coral diseases worldwide. By integrating 14 years of disease monitoring with lesion-scale dynamics, environmental microbiomes, and nutrient data, this study demonstrates that white syndrome expression in Porites cylindrica is shaped by context-dependent interactions among host population structure, eutrophication, and microbial dysbiosis rather than a single causative pathogen. These findings support a multi-etiology framework for coral disease and highlight the importance of environmental microbial reservoirs in modulating disease outcomes. This work provides a long-term, field-based perspective that is rarely available for coral disease systems and is broadly relevant to disease ecology in changing coastal environments.