Wolbachia as a bacteriocyte-associated nutritional mutualist

Takahiro Hosokawa, Ryuichi Koga, Yoshitomo Kikuchi, Xian Ying Meng, Takema Fukatsu

Research output: Contribution to journalArticle

329 Citations (Scopus)

Abstract

Many insects are dependent on bacterial symbionts that provide essential nutrients (ex. aphid-Buchnera and tsetse-Wiglesworthia associations), wherein the symbionts are harbored in specific cells called bacteriocytes that constitute a symbiotic organ bacteriome. Facultative and parasitic bacterial symbionts like Wolbachia have been regarded as evolutionarily distinct from such obligate nutritional mutualists. However, we discovered that, in the bedbug Cimex lectularius, Wolbachia resides in a bacteriome and appears to be an obligate nutritional mutualist. Two bacterial symbionts, a Wolbachia strain and an unnamed γ-proteobacterium, were identified from different strains of the bedbug. The Wolbachia symbiont was detected fromall of the insects examined whereas the γ-proteobacterium was found in a part of them. The Wolbachia symbiont was specifically localized in the bacteriomes and vertically transmitted via the somatic stemcell niche of germalia to oocytes, infecting the incipient symbiotic organ at an early stage of the embryogenesis. Elimination of the Wolbachia symbiont resulted in retarded growth and sterility of the host insect. These deficiencies were rescued by oral supplementation of B vitamins, confirming the essential nutritional role of the symbiont for the host. The estimated genome size of the Wolbachia symbiont was around 1.3 Mb, which was almost equivalent to the genome sizes of parasitic Wolbachia strains of other insects. These results indicate that bacteriocyte-associated nutritional mutualism can evolve from facultative and prevalent microbial associates like Wolbachia, highlighting a previously unknown aspect of the parasitism-mutualism evolutionary continuum.

Original languageEnglish
Pages (from-to)769-774
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume107
Issue number2
DOIs
Publication statusPublished - Feb 15 2010
Externally publishedYes

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Wolbachia
Bedbugs
Insects
Genome Size
Proteobacteria
Symbiosis
Buchnera
Vitamin B Complex
Aphids
Infertility
Oocytes
Embryonic Development

All Science Journal Classification (ASJC) codes

  • General

Cite this

Wolbachia as a bacteriocyte-associated nutritional mutualist. / Hosokawa, Takahiro; Koga, Ryuichi; Kikuchi, Yoshitomo; Meng, Xian Ying; Fukatsu, Takema.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 107, No. 2, 15.02.2010, p. 769-774.

Research output: Contribution to journalArticle

Hosokawa, Takahiro ; Koga, Ryuichi ; Kikuchi, Yoshitomo ; Meng, Xian Ying ; Fukatsu, Takema. / Wolbachia as a bacteriocyte-associated nutritional mutualist. In: Proceedings of the National Academy of Sciences of the United States of America. 2010 ; Vol. 107, No. 2. pp. 769-774.
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