Evolutionary origin of insect–Wolbachia nutritional mutualism

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 111; no. 28; pp. 10257 - 10262
• Main Authors: Nikoh, Naruo, Hosokawa, Takahiro, Moriyama, Minoru, Oshima, Kenshiro, Hattori, Masahira, Fukatsu, Takema
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 15.07.2014; National Acad Sciences
• Subjects: Animals; bacteria; Base Sequence; Bedbugs - metabolism; Bedbugs - microbiology; Biological Sciences; Biotin; Biotin - biosynthesis; Biotin - genetics; blood meal; Cimex lectularius; Endosymbionts; Evolution; Feeding Behavior - physiology; Genes, Bacterial - physiology; genetic background; Genome, Bacterial - physiology; Genomes; Horizontal gene transfer; hosts; Insect genetics; Insects; microsymbionts; Molecular Sequence Data; multigene family; Mutualism; Nutrition; operon; Operons; reproduction; Rickettsia; Symbiosis; Symbiosis - physiology; Vitamin B; Vitamin B Complex - biosynthesis; Vitamin B Complex - genetics; Vitamins; Wolbachia; Wolbachia - genetics; Wolbachia - metabolism
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.1409284111

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 w Cle, 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 w Cle, 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 w Cle-infected and w Cle-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 w Cle-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.