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Phylogenetic, genomic, and biogeographic characterization of a novel and ubiquitous marine invertebrate-associated Rickettsiales parasite, Candidatus Aquarickettsia rohweri, gen. nov., sp. nov.
The ISME Journal ( IF 10.8 ) Pub Date : 2019-08-05 , DOI: 10.1038/s41396-019-0482-0
J Grace Klinges 1 , Stephanie M Rosales 1, 2, 3 , Ryan McMinds 1, 4 , Elizabeth C Shaver 5 , Andrew A Shantz 6, 7 , Esther C Peters 8 , Michael Eitel 9 , Gert Wörheide 9, 10, 11 , Koty H Sharp 12 , Deron E Burkepile 6 , Brian R Silliman 5 , Rebecca L Vega Thurber 1
Affiliation  

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.

中文翻译:

一种新型且普遍存在的海洋无脊椎动物相关立克次体寄生虫的系统发育、基因组和生物地理学特征,Candidatus Aquarickettsia rohweri,gen。十一月,sp。十一月

细菌共生体对于无脊椎动物宿主的健康和体内平衡是不可或缺的。值得注意的是,立克次氏体属 Wolbachia 的成员影响了其陆地宿主的适应性和进化的几个方面,但在海洋系统中几乎没有发现类似的伙伴关系。我们在此报告主要与海洋生物相关的普遍存在的新型立克次氏体物种的基因组、系统发育和生物地理学。我们之前表明,这种细菌是在石珊瑚中发现的,对营养暴露有反应,并且与宿主生长减少和死亡率增加有关。与其他立克次氏体一样,这种细菌的基因组减少,表明寄生生活方式。系统发育分析将这种立克次氏体置于我们定义为“Candidatus 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,我们还证明了“Ca. Aquarickettsia”的成员在全球数十个无脊椎动物谱系中被发现。与珊瑚相关的“Candidatus A. rohweri”是这个新进化枝中第一个完成的基因组。“Ca. A. rohweri”缺乏合成大多数糖类和氨基酸的基因,但拥有几个与致病性相关的基因,包括 Tlc、一种将宿主 ATP 交换为 ADP 的反转运蛋白和完整的 IV 型分泌系统。尽管它无法代谢氮,但“Ca. A. rohweri”拥有 NtrY-NtrX 双组分系统,参与感知和响应细胞外氮。鉴于这些数据,以及宿主组织中寄生虫的可视化,我们假设“Ca. 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,我们假设在珊瑚礁中越来越普遍的营养富集通过提供丰富的富氮代谢物来促进“Ca. A. rohweri”在其宿主中的无限制生长。
更新日期:2019-08-05
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