The tripartite associations between bacteriophage, Wolbachia, and arthropods.
The tripartite associations between bacteriophage, Wolbachia, and arthropods.
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DOI：
10.1371/journal.ppat.0020043
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发表时间：
2006-05
期刊：
影响因子：
6.7
通讯作者：
Wernegreen JJ
中科院分区：
文献类型：
--
作者：
Bordenstein SR;Marshall ML;Fry AJ;Kim U;Wernegreen JJ
通过在全球范围内操纵节肢动物的繁殖，可遗传的内共生沃尔巴克氏菌已经蔓延到大流行的水平。关于细胞质不亲和(CI)的微生物基础，除了细菌密度和感染精子囊的百分比与不亲和强度有关外，人们知之甚少。最近发现的沃尔巴克氏菌温和噬菌体(WO-B)含有Ankyrin编码基因和毒力因子，这导致了关于WO-B噬菌体诱导CI的争论日益激烈。然而，目前的假设还没有考虑到裂解噬菌体和溶原噬菌体对细菌适合性和表型可能具有的单独作用。在这里，我们描述了一套定量方法来表征噬菌体密度及其与细菌密度和CI的关系。在A、B超群寄生黄蜂的雄蜂中，我们计数了WO-B噬菌体和Wolbachia噬菌体的基因组拷贝数和CI外显率。我们报告了几个发现：(1)正如CI的细菌密度模型所预期的那样，感染A的男性CI强度的可变性与细菌密度呈正相关；(2)正如活动性裂解感染所预期的那样，噬菌体和细菌密度呈显著负相关；(3)在A感染的男性中，CI强度和噬菌体密度呈负相关；类似地，表达不完全CI的男性的噬菌体密度显著高于表达完全CI的男性。超微结构分析表明，大约12%的沃尔巴克氏菌含有噬菌体颗粒，这些颗粒的聚集可能发生在沃尔巴克氏菌细胞外。观察到大约16%的沃尔巴克氏细胞与精子细胞尾部之间存在物理相互作用。这些结果支持沃尔巴克氏菌中低至中等频率的裂解发育，以及噬菌体和沃尔巴克氏菌之间总体上的负密度关系。这一发现激发了一种新的CI噬菌体密度模型，在该模型中，裂解噬菌体抑制了沃尔巴克氏菌的密度，从而抑制了生殖寄生。我们的结论是，噬菌体、沃尔巴克氏菌和节肢动物形成了一个三方共生关系，其中所有三个都是理解这种广泛存在的内共生的生物学所不可或缺的。阐明溶源性和溶原性噬菌体发育在沃尔巴克氏菌生物学中的作用将有效地构建对这一研究主题的探讨。母系遗传的共生细菌广泛存在于陆生无脊椎动物中。这种细菌会感染生殖组织的细胞，并对宿主的进化和发育产生重要影响。通常，这些遗传的共生体与宿主建立了有益的关系，但一些物种也可以自私地改变无脊椎动物的繁殖，以增加种群中受感染的雌性动物的数量(细菌的传播性)。细菌介导的扭曲，如杀雄、雌性化、孤雌生殖诱导和细胞质不亲和性，统称为“生殖寄生”。在这篇文章中，研究人员表明，生物圈中最常见的生殖寄生虫(沃尔巴克氏菌)与寄生黄蜂宿主之间的联系受到一个可移动的元件--沃尔巴克氏菌的温带噬菌体的影响。与最近关于WO-B噬菌体可能诱导生殖寄生的报道不同，作者的定量和超微结构分析表明，裂解噬菌体WO-B是致命的，因此与Wolbachia密度和生殖寄生减少有关。基于这些数据，作者提出了一个噬菌体密度模型，在该模型中，裂解噬菌体的发育特定地导致生殖独占的减少，而不是诱导。这项研究是首次发现裂解噬菌体与专性胞内细菌的密度和表型成反比。
By manipulating arthropod reproduction worldwide, the heritable endosymbiont Wolbachia has spread to pandemic levels. Little is known about the microbial basis of cytoplasmic incompatibility (CI) except that bacterial densities and percentages of infected sperm cysts associate with incompatibility strength. The recent discovery of a temperate bacteriophage (WO-B) of Wolbachia containing ankyrin-encoding genes and virulence factors has led to intensifying debate that bacteriophage WO-B induces CI. However, current hypotheses have not considered the separate roles that lytic and lysogenic phage might have on bacterial fitness and phenotype. Here we describe a set of quantitative approaches to characterize phage densities and its associations with bacterial densities and CI. We enumerated genome copy number of phage WO-B and Wolbachia and CI penetrance in supergroup A- and B-infected males of the parasitoid wasp Nasonia vitripennis. We report several findings: (1) variability in CI strength for A-infected males is positively associated with bacterial densities, as expected under the bacterial density model of CI, (2) phage and bacterial densities have a significant inverse association, as expected for an active lytic infection, and (3) CI strength and phage densities are inversely related in A-infected males; similarly, males expressing incomplete CI have significantly higher phage densities than males expressing complete CI. Ultrastructural analyses indicate that approximately 12% of the A Wolbachia have phage particles, and aggregations of these particles can putatively occur outside the Wolbachia cell. Physical interactions were observed between approximately 16% of the Wolbachia cells and spermatid tails. The results support a low to moderate frequency of lytic development in Wolbachia and an overall negative density relationship between bacteriophage and Wolbachia. The findings motivate a novel phage density model of CI in which lytic phage repress Wolbachia densities and therefore reproductive parasitism. We conclude that phage, Wolbachia, and arthropods form a tripartite symbiotic association in which all three are integral to understanding the biology of this widespread endosymbiosis. Clarifying the roles of lytic and lysogenic phage development in Wolbachia biology will effectively structure inquiries into this research topic. Symbiotic bacteria that are maternally inherited are widespread in terrestrial invertebrates. Such bacteria infect the cells of reproductive tissues and can have important evolutionary and developmental effects on the host. Often these inherited symbionts develop beneficial relationships with their hosts, but some species can also selfishly alter invertebrate reproduction to increase the numbers of infected females (the transmitting sex of the bacteria) in the population. Bacterial-mediated distortions such as male-killing, feminization, parthenogenesis induction, and cytoplasmic incompatibility are collectively known as “reproductive parasitism.” In this article, the investigators show that the associations between the most common reproductive parasite in the biosphere (Wolbachia) and a parasitic wasp host are affected by a mobile element—a temperate bacteriophage of Wolbachia. In contrast to recent reports that suggest bacteriophage WO-B may induce reproductive parasitism, the authors' quantitative and ultrastructural analyses indicate that lytic phage WO-B are lethal and therefore associate with a reduction in both Wolbachia densities and reproductive parasitism. Based on these data, the authors propose a phage density model in which lytic phage development specifically leads to a reduction, rather than induction, of reproductive parisitism. The study is among the first investigations to show that lytic bacteriophage inversely associate with the densities and phenotype of an obligate intracellular bacterium.