Collaborative Research: Tracking the interacting roles of the environment, host genotype, and a novel Rickettsiales in coral disease susceptibility

鹿角珊瑚历来是佛罗里达和广大加勒比海地区最丰富的造礁珊瑚之一，现在被列为极度濒危珊瑚，主要是因为以前和反复发生的疾病事件。了解这种珊瑚疾病易感性的整体机制是从事保护和恢复工作的从业者最关心的问题。研究人员最近发现，当珊瑚礁暴露在营养物质污染的水域中时，它们会减少珊瑚的生长和健康，这群寄生细菌普遍存在于鹿角藻的微生物群落中。确定珊瑚宿主、这种寄生微生物和环境之间的相互作用如何与疾病易感性联系起来，为未来的恢复工作提供了关键的洞察力和更大的成功。然而，动物微生物群的复杂性和疾病的背景性质使人们很难确定许多疾病爆发的具体原因。在这个项目中，研究人员进行实验，探索不同遗传菌株的珊瑚与这些细菌在各种营养情景下的相互作用，以更好地了解这种细菌如何影响鹿角珊瑚对疾病的易感性。该项目还表征了这种细菌珊瑚寄生虫的基因组学、寄主范围以及局部和全球分布，以确定其进化史和生理如何驱动这种重要珊瑚物种的疾病易感性。该项目培训了两名博士后，一名技术员和七名学生(一名研究生，六名本科生)，涉及海洋科学、生理学、遗传学、微生物学、组学和统计建模等综合科学。佛罗里达州的一个以研究为基础的课外项目扩大到包括微生物学，并创建了一个名为微生物勇士的新项目模块，重点是科学领域的女性。研究人员制作纪录片和宣传材料，通过在Mote海洋实验室和俄勒冈州科学与工业博物馆的演示，向当地和国家社区广泛宣传项目科学和保护工作。该项目由海洋科学部的生物海洋学计划和综合组织系统部的共生、防御和自我识别计划共同资助。研究人员最近发现了一种海洋立克次体细菌，这种细菌可以在珊瑚中被刺激在高氮和高磷物种存在的情况下生长。根据基因组重组和系统地理学，该细菌被归类为一个新的细菌属--假丝酵母属(Candidatus Aquickettsia)，并表明它与世界各地的珊瑚广泛相关。重要的是，使用一个模型系统，濒危的颈角顶孢子虫珊瑚，研究小组还表明，这种细菌在体内的生长与宿主生长减少和疾病易感性增加有关。本项目旨在更全面地评估这些可诱导感染背后的机制和对珊瑚生理和宿主-细菌共生的影响。研究人员对具有不同立克次体丰度的不同珊瑚基因型进行了营养剂量实验。利用一系列组学和显微技术，该团队量化了由此产生的对Holobion表型的影响。研究人员还在比较不同顶孔宿主和其他珊瑚属中这些细菌的基因组，以评估细菌进化历史的各个方面，以及确定其增殖、毒力和宿主特异性的可能机制。这个跨学科的项目将营养物质与宿主、藻类共生体和细菌寄生虫生理学的时间变化机械地联系起来，并通过探索宿主和寄生虫的基因类型和生长动态以及环境背景如何改变完整的生物表型，解释了为什么这些反应存在自然变化。该奖项反映了NSF的法定使命，并通过使用基金会的智力优势和更广泛的影响审查标准进行评估，被认为值得支持。

Historically one of the most abundant reef-building corals in Florida and the wider Caribbean, the staghorn coral, Acropora cervicornis, is now listed as critically endangered primarily because of previous and reoccurring disease events. Understanding the holistic mechanisms of disease susceptibility in this coral is a top concern of practitioners engaged in conservation and restoration. The investigators recently discovered a group of parasitic bacteria common within the microbial community of A. cervicornis that can reduce the growth and health of corals when reefs are exposed to nutrient polluted waters. Determining how interactions among the coral host, this parasitic microbe, and the environment are linked to disease susceptibility provides critical insight and greater success of future restoration efforts. Yet the complexity of animal microbiomes and the contextual nature of disease make it difficult to identify the specific cause of many disease outbreaks. In this project, the investigators conduct experiments to explore the interactions among different genetic strains of coral and these bacteria in various nutrient scenarios to better understand how this bacterium affects the susceptibility of staghorn coral to diseases. This project also characterizes the genomics, host range, and local and global distribution of this bacterial coral parasite to determine how its evolutionary history and physiology drive disease susceptibility in this important coral species. The project trains two postdocs, one technician, and seven students (one graduate, six undergraduates) in integrative sciences that span marine science, physiology, genetics, microbiology, omics, and statistical modeling. A research-based after school program in Florida is expanded to include microbiology and create a new program module called Microbial warriors, with a focus on women in science. The investigators produce documentary style films and outreach materials to broadly communicate the project science and conservation efforts to local and national communities via presentations at Mote Marine Lab and the Oregon Museum of Science and Industry. This project is co-funded by the Biological Oceanography Program in the Division of Ocean Sciences and the Symbiosis, Defense, and Self-recognition Program in the Division of Integrative Organismal Systems.The investigators recently identified a marine Rickettsiales bacterium that, in corals, can be stimulated to grow in the presence of elevated nitrogen and phosphorous species. Based on genomic reconstruction and phylogeography, this bacteria is classified as a novel bacterial genus, Candidatus Aquarickettsia, and showed that it is broadly associated with scleractinian corals worldwide. Importantly, using a model system, the endangered Acropora cervicornis coral, the team has also shown that the growth of this bacterium in vivo is associated with reduced host growth and increased disease susceptibility. This project aims to more completely evaluate the mechanisms behind and impacts of these inducible infections on coral physiology and host-bacterial symbiosis. The investigators conduct nutrient dosing experiments on different coral genotypes with various Rickettsiales abundances. Using a range of omics and microscopy techniques, the team quantifies the resulting effects on holobiont phenotypes. The investigators are also comparing the genomes of these bacteria in the different Acroporid hosts and other coral genera to evaluate facets of the bacterium's evolutionary history, as well as to identify possible mechanisms of its proliferation, virulence, and host specificity. This interdisciplinary project mechanistically links nutrients to temporal changes in host, algal symbiont, and bacterial parasite physiology and also explain why there is natural variation in these responses by exploring how host and parasite genotypes and growth dynamics combined with environmental contextuality alter holobiont phenotypes.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.