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AEM Accepts, published online ahead of print on 31 August 2007
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Appl. Environ. Microbiol. doi:10.1128/AEM.01131-07
Copyright (c) 2007, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

Bacterial endosymbiont of the slender pigeon louse Columbicola columbae allied to endosymbionts of grain weevils and tsetse flies

Takema Fukatsu*, Ryuichi Koga, Wendy A. Smith, Kohjiiro Tanaka, Naruo Nikoh, Kayoko Sasaki-Fukatsu, Kazunori Yoshizawa, Colin Dale, and Dale H. Clayton

Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan; Department of Biology, University of Utah, UT84106, USA; Division of Natural Sciences, University of the Air, Chiba 261-8586, Japan; Department of Ecology and Systematics, Hokkaido University, Sapporo 060-8589, Japan

* To whom correspondence should be addressed. Email: t-fukatsu{at}aist.go.jp.


   Abstract

The current study focuses on a symbiotic bacterium found in the slender pigeon louse Columbicola columbae (Insecta: Phthiraptera). Molecular phylogenetic analyses indicated that the symbiont belongs to the {gamma}-subdivision of the class Proteobacteria and is allied to Sodalis glossinidius, the secondary symbiont of the tsetse flies Glossina spp., and also to the primary symbiont of the grain weevils Sitophilus spp. Relative rate tests revealed that the symbiont of C. columbae exhibits accelerated molecular evolution in comparison with the tsetse symbiont and the weevil symbiont. Whole mount in situ hybridization was used to localize the symbiont and determine infection dynamics during host development. In 1st and 2nd instar nymphs, the symbionts were localized in the cytoplasm of oval bacteriocytes that formed small aggregates on the both sides of the body cavity. In 3rd instar nymphs, the bacteriocytes migrated to the central body and were finally located in the anterior region of the lateral oviducts, forming conspicuous tissue formations called ovarial ampullae. In adult females, the symbionts were transmitted from the ovarial ampullae to developing oocytes in the ovarioles. In adult males, the bacteriocytes often disappeared without migration. Diagnostic PCR survey of insects collected from Japan, USA, Australia and Argentina detected 96.5% (109/113) infection, with a few uninfected male insects. This study provides the first microbial characterization of a bacteriocyte-associated symbiont from a chewing louse. Possible biological roles of the symbiont are discussed in relation to the host nutritional physiology associated with the feather-feeding lifestyle.




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