Riboflavin Provisioning Underlies Wolbachia's Fitness Contribution to Its Insect Host.
Riboflavin Provisioning Underlies Wolbachia's Fitness Contribution to Its Insect Host.
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DOI：
10.1128/mbio.01732-15
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发表时间：
2015-11-10
期刊：
影响因子：
6.4
通讯作者：
Fukatsu T
中科院分区：
文献类型：
--
作者：
Moriyama M;Nikoh N;Hosokawa T;Fukatsu T
沃尔巴克氏菌属内共生细菌是陆地生态系统中最成功的共生细菌。沃尔巴克氏菌的成功被归因于它对宿主繁殖的显著表型效应，例如细胞质不亲和性，即母系遗传的细菌可以以牺牲宿主的适合性为代价在宿主种群中传播。同时，最近的理论和经验研究表明，弱的和/或有条件的正向适应效应可能显著促进沃尔巴克氏菌感染在宿主群体中的入侵和传播。在这里，我们报告了一个以前不为人知的营养方面，提供核黄素(维生素B2)，这可能支持沃尔巴克氏菌介导的昆虫宿主的健康益处。对B类维生素合成能力的比较基因组研究表明，在不同的昆虫相关沃尔巴克氏菌株中，只有核黄素的合成途径高度保守，而其他B类维生素的合成途径要么不完整，要么不存在。不同沃尔巴克氏菌核黄素合成基因的分子系统发育和基因组分析表明，它们的系统发育关系与沃尔巴克氏菌的基因组系统发育是一致的，这表明核黄素合成基因在沃尔巴克氏菌进化过程中得到了稳定的维持。在控制B维生素含量的血粉上用臭虫(Cimex Lectularius)饲养实验表明，沃尔巴克氏菌的核黄素供应对昆虫宿主的生长、存活和繁殖有显著贡献。这些结果提供了一个生理基础，在此基础上显示了沃尔巴克氏菌介导的积极适合性结果，并为沃尔巴克氏菌感染的生态和进化相关性提供了新的线索。传统上，沃尔巴克氏菌被认为是一种寄生细菌内共生菌，以自私的方式操纵寄主昆虫的繁殖，这往往会对寄主的适合性产生负面影响。同时，也有理论预测，沃尔巴克氏菌对寄主的适合度有直接的正向影响，有可能调和其负面影响，促进共生关系的传播和稳定。在这里，我们通过比较基因组学和实验方法证明，在B类维生素的合成途径中，核黄素(维生素B2)的合成途径在不同的昆虫相关沃尔巴克氏菌株中异常保守，而沃尔巴克氏菌的核黄素供应肯定有助于昆虫的生长、生存和繁殖。这些发现揭示了沃尔巴克氏菌介导的健身益处的营养机制，这提供了经验证据，突出了沃尔巴克氏菌感染的“Jekyll and Hyde”方面。
Endosymbiotic bacteria of the genus Wolbachia represent the most successful symbiotic bacteria in the terrestrial ecosystem. The success of Wolbachia has been ascribed to its remarkable phenotypic effects on host reproduction, such as cytoplasmic incompatibility, whereby maternally inherited bacteria can spread in their host populations at the expense of their host’s fitness. Meanwhile, recent theoretical as well as empirical studies have unveiled that weak and/or conditional positive fitness effects may significantly facilitate invasion and spread of Wolbachia infections in host populations. Here, we report a previously unrecognized nutritional aspect, the provision of riboflavin (vitamin B2), that potentially underpins the Wolbachia-mediated fitness benefit to insect hosts. A comparative genomic survey for synthetic capability of B vitamins revealed that only the synthesis pathway for riboflavin is highly conserved among diverse insect-associated Wolbachia strains, while the synthesis pathways for other B vitamins were either incomplete or absent. Molecular phylogenetic and genomic analyses of riboflavin synthesis genes from diverse Wolbachia strains revealed that, in general, their phylogenetic relationships are concordant with Wolbachia’s genomic phylogeny, suggesting that the riboflavin synthesis genes have been stably maintained in the course of Wolbachia evolution. In rearing experiments with bedbugs (Cimex lectularius) on blood meals in which B vitamin contents were manipulated, we demonstrated that Wolbachia’s riboflavin provisioning significantly contributes to growth, survival, and reproduction of the insect host. These results provide a physiological basis upon which Wolbachia-mediated positive fitness consequences are manifested and shed new light on the ecological and evolutionary relevance of Wolbachia infections. Conventionally, Wolbachia has been regarded as a parasitic bacterial endosymbiont that manipulates the host insect’s reproduction in a selfish manner, which tends to affect a host’s fitness negatively. Meanwhile, some theories predict that, at the same time, Wolbachia can directly affect the host’s fitness positively, which may potentially reconcile the negative effect and facilitate spread and stability of the symbiotic association. Here we demonstrate, by using comparative genomic and experimental approaches, that among synthetic pathways for B vitamins, the synthetic pathway for riboflavin (vitamin B2) is exceptionally conserved among diverse insect-associated Wolbachia strains, and Wolbachia’s riboflavin provisioning certainly contributes to growth, survival, and reproduction in an insect. These findings uncover a nutritional mechanism of a Wolbachia-mediated fitness benefit, which provides empirical evidence highlighting a “Jekyll and Hyde” aspect of Wolbachia infection.