title: Evolutionary origin of insect-Wolbachia nutritional mutualism.
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 wCle 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.
authors: Department of Liberal Arts, The Open University of Japan, Chiba 261-8586, Japan;
authors: Naruo
authors: N
authors: Nikoh
authors: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan; and.
authors: Takahiro
authors: T
authors: Hosokawa
authors: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan; and.
authors: Minoru
authors: M
authors: Moriyama
authors: Center for Omics and Bioinformatics, Graduate School of Frontier Sciences, University of Tokyo, Kashiwa 277-8561, Japan.
authors: Kenshiro
authors: K
authors: Oshima
authors: Center for Omics and Bioinformatics, Graduate School of Frontier Sciences, University of Tokyo, Kashiwa 277-8561, Japan.
authors: Masahira
authors: M
authors: Hattori
authors: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan; and t-fukatsu@aist.go.jp.
authors: Takema
authors: T
authors: Fukatsu
mesh_terms: D000818:Animals; D001483:Base Sequence; D001511:Bedbugs / Q000378:metabolism / Q000382:microbiology; D001710:Biotin / Q000096:biosynthesis / Q000235:genetics; D005247:Feeding Behavior / Q000502:physiology*; D005798:Genes, Bacterial / Q000502:physiology*; D016680:Genome, Bacterial / Q000502:physiology*; D008969:Molecular Sequence Data; D013559:Symbiosis / Q000502:physiology*; D014803:Vitamin B Complex / Q000096:biosynthesis / Q000235:genetics; D020577:Wolbachia / Q000235:genetics / Q000378:metabolism
chemical_list: D014803:Vitamin B Complex; D001710:Biotin