Distinct Wolbachia localization patterns in oocytes of diverse host species reveal multiple strategies of maternal transmission

A broad array of endosymbionts radiate through host populations via vertical transmission, yet much remains unknown concerning the cellular basis, diversity and routes underlying this transmission strategy. Here we address these issues, by examining the cellular distributions of Wolbachia strains that diverged up to 50 million years ago in the oocytes of 18 divergent Drosophila species. This analysis revealed three Wolbachia distribution patterns: 1) a tight clustering at the posterior pole plasm (the site of germline formation); 2) a concentration at the posterior pole plasm, but with a significant bacteria population distributed throughout the oocyte; 3) and a distribution throughout the oocyte, with none or very few located at the posterior pole plasm. Examination of this latter class indicates Wolbachia accesses the posterior pole plasm during the interval between late oogenesis and the blastoderm formation. We also find that one Wolbachia strain in this class concentrates in the posterior somatic follicle cells that encompass the pole plasm of the developing oocyte. In contrast, strains in which Wolbachia concentrate at the posterior pole plasm generally exhibit no or few Wolbachia in the follicle cells associated with the pole plasm. Taken together, these studies suggest that for some Drosophila species, Wolbachia invade the germline from neighboring somatic follicle cells. Phylogenomic analysis indicates that closely related Wolbachia strains tend to exhibit similar patterns of posterior localization, suggesting that specific localization strategies are a function of Wolbachia-associated factors. Previous studies revealed that endosymbionts rely on one of two distinct routes of vertical transmission: continuous maintenance in the germline (germline-to-germline) or a more circuitous route via the soma (germline-to-soma-to-germline). Here we provide compelling evidence that Wolbachiastrains infecting Drosophila species maintain the diverse arrays of cellular mechanisms necessary for both of these distinct transmission routes. This characteristic may account for its ability to infect and spread globally through a vast range of host insect species.

众多内共生体（endosymbionts）通过垂直传播在宿主种群中广泛辐射演化，但目前对该传播策略背后的细胞基础、多样性与传播路径仍知之甚少。本研究针对这一问题展开探讨，对18个分化时长可达5000万年的果蝇（Drosophila）物种卵母细胞中，分化年代各异的沃尔巴克氏体（Wolbachia）菌株的细胞分布进行了分析。该分析揭示了三类沃尔巴克氏体分布模式：1）紧密聚集于后端极质（posterior pole plasm）——即生殖系形成的位点；2）虽主要聚集于后端极质，但仍有大量细菌分布于整个卵母细胞；3）均匀分布于整个卵母细胞，后端极质处几乎无或仅存在极少量菌体。对第三类分布模式的进一步研究表明，沃尔巴克氏体可在卵发生后期至囊胚层（blastoderm）形成的间期进入后端极质。本研究还发现，该类中的一株沃尔巴克氏体菌株会聚集于包裹发育中卵母细胞极质的后部体细胞滤泡细胞内。与之相反，那些主要聚集于后端极质的沃尔巴克氏体菌株，通常在极质相关的滤泡细胞中几乎不存在或仅含有少量菌体。综上，本研究结果表明，对于部分果蝇物种而言，沃尔巴克氏体可从邻近的体细胞滤泡细胞侵入生殖系。系统基因组学（phylogenomic）分析显示，亲缘关系相近的沃尔巴克氏体菌株往往呈现相似的后端定位模式，这提示特定的定位策略是沃尔巴克氏体相关因子作用的结果。既往研究表明，内共生体的垂直传播依赖两类截然不同的路径：一是在生殖系内持续维持（生殖系-生殖系路径），二是更为迂回的经由体细胞的路径（生殖系-体细胞-生殖系路径）。本研究提供了强有力的证据，证明感染果蝇的沃尔巴克氏体菌株具备实现这两类不同传播路径所需的多样化细胞机制。这一特性或许正是其能够在海量昆虫宿主物种中广泛传播并实现全球侵染的原因。