Department of Biology, West Virginia University, Morgantown, West Virginia, USA.
mBio. 2012 Feb 14;3(1). doi: 10.1128/mBio.00240-11. Print 2012.
Ancient endosymbionts have been associated with extreme genome structural stability with little differentiation in gene inventory between sister species. Tsetse flies (Diptera: Glossinidae) harbor an obligate endosymbiont, Wigglesworthia, which has coevolved with the Glossina radiation. We report on the ~720-kb Wigglesworthia genome and its associated plasmid from Glossina morsitans morsitans and compare them to those of the symbiont from Glossina brevipalpis. While there was overall high synteny between the two genomes, a large inversion was noted. Furthermore, symbiont transcriptional analyses demonstrated host tissue and development-specific gene expression supporting robust transcriptional regulation in Wigglesworthia, an unprecedented observation in other obligate mutualist endosymbionts. Expression and immunohistochemistry confirmed the role of flagella during the vertical transmission process from mother to intrauterine progeny. The expression of nutrient provisioning genes (thiC and hemH) suggests that Wigglesworthia may function in dietary supplementation tailored toward host development. Furthermore, despite extensive conservation, unique genes were identified within both symbiont genomes that may result in distinct metabolomes impacting host physiology. One of these differences involves the chorismate, phenylalanine, and folate biosynthetic pathways, which are uniquely present in Wigglesworthia morsitans. Interestingly, African trypanosomes are auxotrophs for phenylalanine and folate and salvage both exogenously. It is possible that W. morsitans contributes to the higher parasite susceptibility of its host species.
Genomic stasis has historically been associated with obligate endosymbionts and their sister species. Here we characterize the Wigglesworthia genome of the tsetse fly species Glossina morsitans and compare it to its sister genome within G. brevipalpis. The similarity and variation between the genomes enabled specific hypotheses regarding functional biology. Expression analyses indicate significant levels of transcriptional regulation and support development- and tissue-specific functional roles for the symbiosis previously not observed in obligate mutualist symbionts. Retention of the genetically expensive flagella within these small genomes was demonstrated to be significant in symbiont transmission and tailored to the unique tsetse fly reproductive biology. Distinctions in metabolomes were also observed. We speculate an additional role for Wigglesworthia symbiosis where infections with pathogenic trypanosomes may depend upon symbiont species-specific metabolic products and thus influence the vector competence traits of different tsetse fly host species.
古老的内共生体与姐妹物种之间的基因库差异很小，具有极端的基因组结构稳定性相关。舌蝇（双翅目：丽蝇科）携带一种专性内共生菌，Wigglesworthia，它与 Glossina 辐射共同进化。我们报告了来自 Glossina morsitans morsitans 的约 720kb 的 Wigglesworthia 基因组及其相关质粒，并将其与来自 Glossina brevipalpis 的共生菌进行了比较。尽管两个基因组之间存在总体高度的同线性，但注意到了一个大的倒位。此外，共生体转录分析表明，基因表达具有宿主组织和发育特异性，支持 Wigglesworthia 中强大的转录调控，这是其他强制性互惠共生内共生体中前所未有的观察结果。表达和免疫组织化学证实了鞭毛在从母体到子宫内后代的垂直传播过程中的作用。营养供应基因（thiC 和 hemH）的表达表明，Wigglesworthia 可能在针对宿主发育的饮食补充中发挥作用。此外，尽管存在广泛的保守性，但在两个共生体基因组中都鉴定到了独特的基因，这可能导致影响宿主生理学的不同代谢组。其中一个差异涉及到芳香族氨基酸、苯丙氨酸和叶酸生物合成途径，这些途径仅存在于 Wigglesworthia morsitans 中。有趣的是，非洲锥虫是苯丙氨酸和叶酸的营养缺陷型，并且可以外源性地回收这两种物质。有可能是 W. morsitans 导致了其宿主物种更高的寄生虫易感性。
基因组静止性在历史上与专性内共生体及其姐妹物种有关。在这里，我们描述了舌蝇物种 Glossina morsitans 的 Wigglesworthia 基因组，并将其与 G. brevipalpis 中的姐妹基因组进行了比较。基因组之间的相似性和差异使我们能够针对共生关系提出特定的功能生物学假设。表达分析表明，转录调控水平显著，支持共生关系以前在强制性互惠共生体中没有观察到的发育和组织特异性功能作用。在这些小基因组中保留遗传上昂贵的鞭毛在共生体传播中具有重要意义，并针对舌蝇独特的生殖生物学进行了调整。还观察到代谢组的差异。我们推测 Wigglesworthia 共生关系的另一个作用是，感染致病性锥虫可能依赖于共生体物种特异性的代谢产物，从而影响不同舌蝇宿主物种的媒介能力特征。
