Department of Liberal Arts, The Open University of Japan, Chiba 261-8586, Japan;
Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan; and.
Proc Natl Acad Sci U S A. 2014 Jul 15;111(28):10257-62. doi: 10.1073/pnas.1409284111. Epub 2014 Jun 30.
Obligate insect-bacterium nutritional mutualism is among the most sophisticated forms of symbiosis, wherein the host and the symbiont are integrated into a coherent biological entity and unable to survive without the partnership. Originally, however, such obligate symbiotic bacteria must have been derived from free-living bacteria. How highly specialized obligate mutualisms have arisen from less specialized associations is of interest. Here we address this evolutionary issue by focusing on an exceptional insect-Wolbachia nutritional mutualism. Although Wolbachia endosymbionts are ubiquitously found in diverse insects and generally regarded as facultative/parasitic associates for their insect hosts, a Wolbachia strain associated with the bedbug Cimex lectularius, designated as wCle, was shown to be essential for host's growth and reproduction via provisioning of B vitamins. We determined the 1,250,060-bp genome of wCle, which was generally similar to the genomes of insect-associated facultative Wolbachia strains, except for the presence of an operon encoding the complete biotin synthetic pathway that was acquired via lateral gene transfer presumably from a coinfecting endosymbiont Cardinium or Rickettsia. Nutritional and physiological experiments, in which wCle-infected and wCle-cured bedbugs of the same genetic background were fed on B-vitamin-manipulated blood meals via an artificial feeding system, demonstrated that wCle certainly synthesizes biotin, and the wCle-provisioned biotin significantly contributes to the host fitness. These findings strongly suggest that acquisition of a single gene cluster consisting of biotin synthesis genes underlies the bedbug-Wolbachia nutritional mutualism, uncovering an evolutionary transition from facultative symbiosis to obligate mutualism facilitated by lateral gene transfer in an endosymbiont lineage.
专性昆虫-细菌营养互惠共生是最复杂的共生形式之一，其中宿主和共生体整合为一个连贯的生物实体，如果没有伙伴关系，它们就无法生存。然而，最初这种专性共生细菌必须是从自由生活的细菌中衍生而来的。高度特化的专性互惠共生是如何从较少特化的共生关系中产生的，这是一个有趣的问题。在这里，我们通过关注一种特殊的昆虫-沃尔巴克氏体营养互惠共生关系来解决这个进化问题。尽管沃尔巴克氏体内共生菌广泛存在于各种昆虫中，通常被认为是它们昆虫宿主的兼性/寄生伙伴，但与臭虫 Cimex lectularius 相关的沃尔巴克氏体菌株 wCle 被证明是宿主生长和繁殖所必需的，因为它为宿主提供了 B 族维生素。我们确定了 wCle 的 1,250,060-bp 基因组，它与昆虫相关的兼性沃尔巴克氏体菌株的基因组大致相似，除了存在一个编码完整生物素合成途径的操纵子，该途径是通过水平基因转移从共生的内共生体 Cardinium 或 Rickettsia 获得的。营养和生理实验表明，在同一个遗传背景下，感染了 wCle 和治愈了 wCle 的臭虫通过人工喂养系统以 B 族维生素处理过的血液为食，wCle 肯定合成生物素，而且 wCle 提供的生物素显著有助于宿主的适应度。这些发现强烈表明，一个由生物素合成基因组成的单基因簇的获得是臭虫-沃尔巴克氏体营养互惠共生的基础，揭示了在共生体谱系中，水平基因转移促进了从兼性共生到专性互惠共生的进化转变。
