Department of Microbiology, Oregon State University, Corvallis, OR, 97331, USA.
Cooperative Institute for Marine and Atmospheric Studies, University of Miami, Miami, FL, 33149, USA.
ISME J. 2019 Dec;13(12):2938-2953. doi: 10.1038/s41396-019-0482-0. Epub 2019 Aug 5.
Bacterial symbionts are integral to the health and homeostasis of invertebrate hosts. Notably, members of the Rickettsiales genus Wolbachia influence several aspects of the fitness and evolution of their terrestrial hosts, but few analogous partnerships have been found in marine systems. We report here the genome, phylogenetics, and biogeography of a ubiquitous and novel Rickettsiales species that primarily associates with marine organisms. We previously showed that this bacterium was found in scleractinian corals, responds to nutrient exposure, and is associated with reduced host growth and increased mortality. This bacterium, like other Rickettsiales, has a reduced genome indicative of a parasitic lifestyle. Phylogenetic analysis places this Rickettsiales within a new genus we define as "Candidatus Aquarickettsia." Using data from the Earth Microbiome Project and SRA databases, we also demonstrate that members of "Ca. Aquarickettsia" are found globally in dozens of invertebrate lineages. The coral-associated "Candidatus A. rohweri" is the first finished genome in this new clade. "Ca. A. rohweri" lacks genes to synthesize most sugars and amino acids but possesses several genes linked to pathogenicity including Tlc, an antiporter that exchanges host ATP for ADP, and a complete Type IV secretion system. Despite its inability to metabolize nitrogen, "Ca. A. rohweri" possesses the NtrY-NtrX two-component system involved in sensing and responding to extracellular nitrogen. Given these data, along with visualization of the parasite in host tissues, we hypothesize that "Ca. A. rohweri" reduces coral health by consuming host nutrients and energy, thus weakening and eventually killing host cells. Last, we hypothesize that nutrient enrichment, which is increasingly common on coral reefs, encourages unrestricted growth of "Ca. A. rohweri" in its host by providing abundant N-rich metabolites to be scavenged.
细菌共生体是无脊椎动物宿主健康和体内平衡的重要组成部分。值得注意的是，立克次氏体属沃尔巴克氏体的成员影响其陆地宿主的几个方面的适应性和进化，但在海洋系统中很少发现类似的伙伴关系。我们在此报告一种普遍存在且新颖的立克次氏体物种的基因组、系统发育和生物地理学，该物种主要与海洋生物有关。我们之前曾表明，这种细菌存在于硬珊瑚中，对营养物质暴露有反应，并且与宿主生长减少和死亡率增加有关。这种细菌与其他立克次氏体一样，基因组减少表明其寄生生活方式。系统发育分析将这种立克次氏体置于我们定义为“候选Aquarickettsia”的新属中。使用来自地球微生物组计划和 SRA 数据库的数据，我们还表明，“候选 Aquarickettsia”的成员在全球数十种无脊椎动物谱系中被发现。与珊瑚相关的“候选 A. rohweri”是该新分支中第一个完成的基因组。“候选 A. rohweri”缺乏合成大多数糖和氨基酸的基因，但拥有几个与致病性相关的基因，包括 Tlc，一种用于交换宿主 ATP 为 ADP 的反向转运蛋白，以及一个完整的 IV 型分泌系统。尽管“候选 A. rohweri”不能代谢氮，但它拥有参与感应和响应细胞外氮的 NtrY-NtrX 双组分系统。鉴于这些数据，以及寄生虫在宿主组织中的可视化，我们假设“候选 A. rohweri”通过消耗宿主的营养和能量来降低珊瑚的健康，从而削弱并最终杀死宿主细胞。最后，我们假设营养丰富，这在珊瑚礁中越来越普遍，通过提供丰富的 N 丰富代谢物来促进“候选 A. rohweri”在其宿主中的无限制生长。
