Evolutionary origin of insect-Wolbachia nutritional mutualism

Naruo Nikoh, Takahiro Hosokawa, Minoru Moriyama, Kenshiro Oshima, Masahira Hattori, Takema Fukatsu

Research output: Contribution to journalArticle

115 Citations (Scopus)

Abstract

Obligate insect-bacterium nutritional mutualism is among the most sophisticated forms of symbiosis, wherein the host and the symbiont are integrated into a coherent biological entity and unable to survive without the partnership. Originally, however, such obligate symbiotic bacteria must have been derived from free-living bacteria. How highly specialized obligate mutualisms have arisen from less specialized associations is of interest. Here we address this evolutionary issue by focusing on an exceptional insect-Wolbachia nutritional mutualism. Although Wolbachia endosymbionts are ubiquitously found in diverse insects and generally regarded as facultative/parasitic associates for their insect hosts, a Wolbachia strain associated with the bedbug Cimex lectularius, designated as wCle, was shown to be essential for host's growth and reproduction via provisioning of B vitamins. We determined the 1,250,060-bp genome of wCle, which was generally similar to the genomes of insect-associated facultative Wolbachia strains, except for the presence of an operon encoding the complete biotin synthetic pathway that was acquired via lateral gene transfer presumably from a coinfecting endosymbiont Cardinium or Rickettsia. Nutritional and physiological experiments, in which wCle-infected and wCle-cured bedbugs of the same genetic background were fed on B-vitamin-manipulated blood meals via an artificial feeding system, demonstrated that w Cle certainly synthesizes biotin, and the wCle-provisioned biotin significantly contributes to the host fitness. These findings strongly suggest that acquisition of a single gene cluster consisting of biotin synthesis genes underlies the bedbug-Wolbachia nutritional mutualism, uncovering an evolutionary transition from facultative symbiosis to obligate mutualism facilitated by lateral gene transfer in an endosymbiont lineage.

Original languageEnglish
Pages (from-to)10257-10262
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number28
DOIs
Publication statusPublished - Jul 15 2014

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Wolbachia
Symbiosis
Bedbugs
Insects
Biotin
Horizontal Gene Transfer
Vitamin B Complex
Bacteria
Insect Genome
Rickettsia
Nutritional Support
Operon
Multigene Family
Reproduction
Meals
Genome
Growth
Genes

All Science Journal Classification (ASJC) codes

  • General

Cite this

Evolutionary origin of insect-Wolbachia nutritional mutualism. / Nikoh, Naruo; Hosokawa, Takahiro; Moriyama, Minoru; Oshima, Kenshiro; Hattori, Masahira; Fukatsu, Takema.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, No. 28, 15.07.2014, p. 10257-10262.

Research output: Contribution to journalArticle

Nikoh, Naruo ; Hosokawa, Takahiro ; Moriyama, Minoru ; Oshima, Kenshiro ; Hattori, Masahira ; Fukatsu, Takema. / Evolutionary origin of insect-Wolbachia nutritional mutualism. In: Proceedings of the National Academy of Sciences of the United States of America. 2014 ; Vol. 111, No. 28. pp. 10257-10262.
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