Infection dynamics of coexisting beta- and gammaproteobacteria in the nested endosymbiotic system of mealybugs

Infection dynamics of coexisting beta- and gammaproteobacteria in the nested endosymbiotic system of mealybugs
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DOI:
10.1128/aem.00250-08
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发表时间:
2008-07-01
影响因子:
4.4
通讯作者:
Fukatsu, Takema
Fukatsu, Takema
中科院分区:
生物学2区
文献类型:
--
作者:
Kono, Marie;Koga, Ryuichi;Fukatsu, Takema

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本文研究了粉孢细菌克朗恩平球菌和康斯托克假球菌发育过程中内共生细菌的感染动态。分子系统发育分析鉴定出每个粉蚧种的β变形菌和γ变形菌。前一种细菌与其他粉虫的β -内共生体,即“Candidatus Tremblaya princeps”有关,并在β变形菌门中形成了紧密的分支。同时,后者与其他粉孢菌的γ -内共生体有亲缘关系,但在γ变形菌门中属于不同的分支。全安装原位杂交证实了粉蚧内共生系统中奇特的巢状结构:β -内共生细胞存在于细菌细胞的细胞质中,γ -内共生细胞位于β -内共生细胞中。在若虫和雌虫的发育中,一个由许多细菌细胞组成的大的椭圆形细菌群存在于腹部,其中是内共生体的避难所。在雄性发育过程中,细菌群在预蛹和蛹中逐渐退化,在成年雄性中几乎无法辨认。在退化过程中,γ -内共生体比β -内共生体消失得更快。定量PCR分析表明:(1)雌虫发育阶段内共生体的种群动态反映了昆虫的繁殖活动;(2)雌虫和雄虫发育阶段内共生体的种群动态存在显著差异;(3)雄虫发育阶段内共生体种群数量急剧减少;(4)γ -内共生体种群数量在雄虫发育阶段下降速度快于β -内共生体种群数量。本文讨论了β -和γ -内共生种群不耦合调控的可能机制,并讨论了这种独特的原核-原核内共生系统的建立和进化。
We investigated the infection dynamics of endosymbiotic bacteria in the developmental course of the mealybugs Planococcus kraunhiae and Pseudococcus comstocki. Molecular phylogenetic analyses identified a betaproteobacterium and a gammaproteobacterium from each of the mealybug species. The former bacterium was related to the beta-endosymbionts of other mealybugs, i.e., "Candidatus Tremblaya princeps," and formed a compact clade in the Betaproteobacteria. Meanwhile, the latter bacterium was related to the gamma-endosymbionts of other mealybugs but belonged to distinct clades in the Gammaproteobacteria. Whole-mount in situ hybridization confirmed the peculiar nested formation in the endosymbiotic system of the mealybugs: the beta-endosymbiont cells were present in the cytoplasm of the bacteriocytes, and the gamma-endosymbiont cells were located in the beta-endosymbiont cells. In nymphal and female development, a large oval bacteriome consisting of a number of bacteriocytes was present in the abdomen, wherein the endosymbionts were harbored. In male development, strikingly, the bacteriome progressively degenerated in prepupae and pupae and became almost unrecognizable in adult males. In the degeneration process, the gamma-endosymbionts disappeared more rapidly than the beta-endosymbionts did. Quantitative PCR analyses revealed that (i) the population dynamics of the endosymbionts in female development reflected the reproductive activity of the insects, (ii) the population dynamics of the endosymbionts were strikingly different between female development and male development, (iii) the endosymbiont populations drastically decreased in male development, and (iv) the gamma-endosymbiont populations decreased more rapidly than the beta-endosymbiont populations in male development. Possible mechanisms underlying the uncoupled regulation of the beta- and gamma-endosymbiont populations are discussed in relation to the establishment and evolution of this unique prokaryote-prokaryote endosymbiotic system.