Department of Entomology, University of California Riverside.
Department of Biology, Indiana University, Bloomington.
Genome Biol Evol. 2018 Feb 1;10(2):434-451. doi: 10.1093/gbe/evy012.
The bacterial endosymbiont Wolbachia manipulates arthropod reproduction to facilitate its maternal spread through host populations. The most common manipulation is cytoplasmic incompatibility (CI): Wolbachia-infected males produce modified sperm that cause embryonic mortality, unless rescued by embryos harboring the same Wolbachia. The genes underlying CI, cifA and cifB, were recently identified in the eukaryotic association module of Wolbachia's prophage WO. Here, we use transcriptomic and genomic approaches to address three important evolutionary facets of the cif genes. First, we assess whether or not cifA and cifB comprise a classic toxin-antitoxin operon in wMel and show that the two genes exhibit striking, transcriptional differences across host development. They can produce a bicistronic message despite a predicted hairpin termination element in their intergenic region. Second, cifA and cifB strongly coevolve across the diversity of phage WO. Third, we provide new domain and functional predictions across homologs within Wolbachia, and show that amino acid sequences vary substantially across the genus. Finally, we investigate conservation of cifA and cifB and find frequent degradation and loss of the genes in strains that no longer induce CI. Taken together, we demonstrate that cifA and cifB exhibit complex transcriptional regulation in wMel, provide functional annotations that broaden the potential mechanisms of CI induction, and report recurrent erosion of cifA and cifB in non-CI strains, thus expanding our understanding of the most widespread form of reproductive parasitism.
细菌共生体沃尔巴克氏体操纵节肢动物的生殖，以促进其在宿主种群中的母系传播。最常见的操纵形式是细胞质不兼容（CI）：感染沃尔巴克氏体的雄性产生的精子会导致胚胎死亡，除非胚胎携带相同的沃尔巴克氏体才能得到拯救。CI 的相关基因 cifA 和 cifB 最近在沃尔巴克氏体噬菌体 WO 的真核共生模块中被鉴定出来。在这里，我们使用转录组学和基因组学方法来研究 cif 基因的三个重要进化方面。首先，我们评估 cifA 和 cifB 是否构成 wMel 中的经典毒素-抗毒素操纵子，并表明这两个基因在宿主发育过程中表现出明显的转录差异。尽管它们的基因间区存在预测的发夹终止元件，但它们可以产生双顺反子消息。其次，cifA 和 cifB 在噬菌体 WO 的多样性中强烈协同进化。第三，我们在沃尔巴克氏体中提供了同源物的新结构域和功能预测，并表明氨基酸序列在属内有很大差异。最后，我们研究了 cifA 和 cifB 的保守性，发现不再诱导 CI 的菌株中经常出现基因降解和丢失。总之，我们证明了 cifA 和 cifB 在 wMel 中表现出复杂的转录调控，提供了扩展 CI 诱导潜在机制的功能注释，并报告了非 CI 菌株中 cifA 和 cifB 的频繁侵蚀，从而扩展了我们对最广泛的生殖寄生形式的理解。
