The Recent Evolution of a Maternally-Inherited Endosymbiont of Ticks Led to the Emergence of the Q Fever Pathogen, Coxiella burnetii.
The Recent Evolution of a Maternally-Inherited Endosymbiont of Ticks Led to the Emergence of the Q Fever Pathogen, Coxiella burnetii.
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DOI：
10.1371/journal.ppat.1004892
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发表时间：
2015-05
期刊：
影响因子：
6.7
通讯作者：
Chevillon C
中科院分区：
文献类型：
--
作者：
Duron O;Noël V;McCoy KD;Bonazzi M;Sidi-Boumedine K;Morel O;Vavre F;Zenner L;Jourdain E;Durand P;Arnathau C;Renaud F;Trape JF;Biguezoton AS;Cremaschi J;Dietrich M;Léger E;Appelgren A;Dupraz M;Gómez-Díaz E;Diatta G;Dayo GK;Adakal H;Zoungrana S;Vial L;Chevillon C
Q热是一种高度传染性疾病，在世界范围内都有分布。其病原体是细胞内细菌伯内氏柯克斯体，可感染多种脊椎动物，包括人类。它的进化起源几乎仍然完全未知，并且其祖先的身份和生活方式仍然存在不确定性。最近发现一些蜱种含有母系遗传的类柯克斯体生物，参与共生相互作用，但它们与 Q 热病原体的关系仍不清楚。在这里，我们对蜱虫进行了广泛采样，从 58 个检查物种中的 40 个物种中鉴定出新的非典型柯克斯体菌株，并利用这些数据推断导致伯内特蜱出现的进化过程。多位点分型和全基因组测序数据的系统发育分析表明，类柯克斯体生物代表了一个与蜱相关的古老单系类群。值得注意的是，所有已知的伯内特蜱菌株都起源于该群体，并且是蜱寄主的类柯克斯体祖先的后代。使用群体饲养和现场收集的妊娠雌性，我们进一步确定了这些类柯克斯体生物在四种受检蜱种中存在高效母体传播，这种模式与内共生生活方式一致。我们的实验室培养测定还表明，这些类柯克斯体生物不适合在脊椎动物细胞环境中培养，这表明与伯内特柯克斯体相比，其代谢要求不同。总而言之，该数据集表明，伯内特蜱最近从遗传性蜱共生体进化而来，该共生体成功感染脊椎动物细胞，可能是通过获得新的毒力因子。剧毒传染病如何从非病原生物中产生是一个具有挑战性的问题。在这里，我们以 Q 热为例来解决这个进化问题。其病原体是细胞内细菌伯内氏柯克斯体，对人类和多种动物具有极强的传染性。然而，其进化起源仍然存在不确定性，包括其祖先的身份和生活方式。在本文中，我们表明伯内特蜱是由母系遗传的蜱内共生体罕见的进化转变为脊椎动物的一种特殊的剧毒病原体。虽然节肢动物共生体通常通过母系传播，并且被认为不会传染给脊椎动物，但我们在此确定，一种柯克斯体共生体已经进化出必要的适应能力来利用脊椎动物细胞，从而导致 Q 热的出现。
Q fever is a highly infectious disease with a worldwide distribution. Its causative agent, the intracellular bacterium Coxiella burnetii, infects a variety of vertebrate species, including humans. Its evolutionary origin remains almost entirely unknown and uncertainty persists regarding the identity and lifestyle of its ancestors. A few tick species were recently found to harbor maternally-inherited Coxiella-like organisms engaged in symbiotic interactions, but their relationships to the Q fever pathogen remain unclear. Here, we extensively sampled ticks, identifying new and atypical Coxiella strains from 40 of 58 examined species, and used this data to infer the evolutionary processes leading to the emergence of C. burnetii. Phylogenetic analyses of multi-locus typing and whole-genome sequencing data revealed that Coxiella-like organisms represent an ancient and monophyletic group allied to ticks. Remarkably, all known C. burnetii strains originate within this group and are the descendants of a Coxiella-like progenitor hosted by ticks. Using both colony-reared and field-collected gravid females, we further establish the presence of highly efficient maternal transmission of these Coxiella-like organisms in four examined tick species, a pattern coherent with an endosymbiotic lifestyle. Our laboratory culture assays also showed that these Coxiella-like organisms were not amenable to culture in the vertebrate cell environment, suggesting different metabolic requirements compared to C. burnetii. Altogether, this corpus of data demonstrates that C. burnetii recently evolved from an inherited symbiont of ticks which succeeded in infecting vertebrate cells, likely by the acquisition of novel virulence factors. How virulent infectious diseases emerge from non-pathogenic organisms is a challenging question. Here, we address this evolutionary issue in the case of Q fever. Its causative agent, the intracellular bacterium Coxiella burnetii, is extremely infectious to humans and a variety of animals. However, uncertainty persists regarding its evolutionary origin, including the identity and lifestyle of its ancestors. In this article, we show that C. burnetii arose from a rare evolutionary transformation of a maternally-inherited endosymbiont of ticks into a specialized and virulent pathogen of vertebrates. While arthropod symbionts are typically transmitted maternally and thought not to be infectious to vertebrates, we establish here that one Coxiella symbiont has evolved the necessary adaptations to exploit the vertebrate cell, leading to the emergence of Q fever.
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