Reduced diversity and stability of coral-associated bacterial communities and suppressed immune function precedes disease onset in corals adjacent to reef platforms

Disease represents an emerging threat to coral reef ecosystems worldwide, highlighting the need to understand how stressful environmental conditions interact with coral immune function and the structure of associated microbial communities to affect holobiont health. Reported increases in coral disease levels at sites adjacent to permanently moored platforms on Australia's Great Barrier Reef (GBR) provide a unique opportunity to investigate environment-host-microbe interactions in situ. Here, we evaluate water quality (i.e. dissolved organic and inorganic nutrients), coral immune function (i.e. phenoloxidase activity) and coral-associated bacterial community structure (i.e. 16S rRNA gene amplicon sequencing) before, during and after a disease event that affected corals adjacent to reef platforms in the central (Whitsunday) sector of the GBR. Over the course of the 8-month study, 31% of tagged colonies of Acropora millepora adjacent to reef platforms developed signs of white syndrome (WS), while all conspecific, control colonies on a nearby reef remained visually healthy. Among the corals remaining visually healthy throughout the study, significant reductions in coral immune function and coral-associated bacterial diversity were recorded for those adjacent to reef platforms compared to those at the platform-free control site. Interestingly, two months prior to the first observation of macroscopic disease signs, bacterial diversity on corals that would develop WS was reduced, while heterogeneity in coral-associated bacterial communities among the group was significantly elevated relative to corals remaining healthy at the same location. These results indicate that proximity to reef platforms impacts coral immunocompetence and coral-associated bacterial community structure and diversity, which could profoundly affect the susceptibility of corals to disease.

海洋病害已成为全球珊瑚礁生态系统面临的新兴威胁，这凸显出研究胁迫性环境条件如何与珊瑚免疫功能、共生微生物群落结构相互作用，进而影响珊瑚全共生体（holobiont）健康的必要性。澳大利亚大堡礁（Great Barrier Reef, GBR）永久停泊平台周边海域的珊瑚病害发生率据报有所上升，这为原位开展环境-宿主-微生物互作研究提供了绝佳契机。本研究针对大堡礁中部（惠森迪（Whitsunday）片区）珊瑚平台周边受病害影响的珊瑚群体，在病害发生前、发生期间及发生后，对水质（即溶解态有机与无机营养盐）、珊瑚免疫功能（即酚氧化酶活性）以及珊瑚共生细菌群落结构（即16S rRNA基因扩增子测序）进行了评估。在为期8个月的研究周期内，毗邻珊瑚平台的31%标记株细枝鹿角珊瑚（Acropora millepora）出现了白色综合征（white syndrome, WS）症状，而附近无平台对照礁体上所有同种的对照珊瑚群体外观均保持健康。在整个研究期间外观保持健康的珊瑚中，与无平台对照位点的珊瑚相比，毗邻珊瑚平台的珊瑚其免疫功能及共生细菌多样性均出现显著下降。值得注意的是，在首次观测到肉眼可见的病害症状前两个月，后续出现WS症状的珊瑚其共生细菌多样性已出现下降，而该组珊瑚的共生细菌群落异质性相较于同区域内保持健康的珊瑚则显著升高。上述结果表明，毗邻珊瑚平台会影响珊瑚的免疫能力及其共生细菌群落的结构与多样性，这可能会极大地改变珊瑚对病害的易感性。