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Applied and Environmental Microbiology, July 2008, p. 4175-4184, Vol. 74, No. 13
0099-2240/08/$08.00+0     doi:10.1128/AEM.00250-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Infection Dynamics of Coexisting Beta- and Gammaproteobacteria in the Nested Endosymbiotic System of Mealybugs{triangledown}

Marie Kono,1,2 Ryuichi Koga,1 Masakazu Shimada,2 and Takema Fukatsu1,2*

Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan,1 Department of General Systems Studies, Graduate School of Arts and Sciences, University of Tokyo, Tokyo, Japan2

Received 28 January 2008/ Accepted 28 April 2008

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 β-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 β-endosymbiont cells were present in the cytoplasm of the bacteriocytes, and the {gamma}-endosymbiont cells were located in the β-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 β-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 β-endosymbiont populations in male development. Possible mechanisms underlying the uncoupled regulation of the β- and {gamma}-endosymbiont populations are discussed in relation to the establishment and evolution of this unique prokaryote-prokaryote endosymbiotic system.

* Corresponding author. Mailing address: Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan. Phone: 81-29-861-6087. Fax: 81-29-861-6080. E-mail: t-fukatsu{at}aist.go.jp

{triangledown} Published ahead of print on 9 May 2008.

Applied and Environmental Microbiology, July 2008, p. 4175-4184, Vol. 74, No. 13
0099-2240/08/$08.00+0     doi:10.1128/AEM.00250-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.





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