Affiliation:
1. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, Japan
2. Department of Liberal Arts, The Open University of Japan, Chiba, Japan
3. Faculty of Science, Kyushu University, Fukuoka, Japan
4. Department of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo, Japan
5. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan
Abstract
ABSTRACT
Endosymbiotic bacteria of the genus
Wolbachia
represent the most successful symbiotic bacteria in the terrestrial ecosystem. The success of
Wolbachia
has been ascribed to its remarkable phenotypic effects on host reproduction, such as cytoplasmic incompatibility, whereby maternally inherited bacteria can spread in their host populations at the expense of their host's fitness. Meanwhile, recent theoretical as well as empirical studies have unveiled that weak and/or conditional positive fitness effects may significantly facilitate invasion and spread of
Wolbachia
infections in host populations. Here, we report a previously unrecognized nutritional aspect, the provision of riboflavin (vitamin B
2
), that potentially underpins the
Wolbachia
-mediated fitness benefit to insect hosts. A comparative genomic survey for synthetic capability of B vitamins revealed that only the synthesis pathway for riboflavin is highly conserved among diverse insect-associated
Wolbachia
strains, while the synthesis pathways for other B vitamins were either incomplete or absent. Molecular phylogenetic and genomic analyses of riboflavin synthesis genes from diverse
Wolbachia
strains revealed that, in general, their phylogenetic relationships are concordant with
Wolbachia
's genomic phylogeny, suggesting that the riboflavin synthesis genes have been stably maintained in the course of
Wolbachia
evolution. In rearing experiments with bedbugs (
Cimex lectularius
) on blood meals in which B vitamin contents were manipulated, we demonstrated that
Wolbachia
's riboflavin provisioning significantly contributes to growth, survival, and reproduction of the insect host. These results provide a physiological basis upon which
Wolbachia
-mediated positive fitness consequences are manifested and shed new light on the ecological and evolutionary relevance of
Wolbachia
infections.
IMPORTANCE
Conventionally,
Wolbachia
has been regarded as a parasitic bacterial endosymbiont that manipulates the host insect's reproduction in a selfish manner, which tends to affect a host's fitness negatively. Meanwhile, some theories predict that, at the same time,
Wolbachia
can directly affect the host's fitness positively, which may potentially reconcile the negative effect and facilitate spread and stability of the symbiotic association. Here we demonstrate, by using comparative genomic and experimental approaches, that among synthetic pathways for B vitamins, the synthetic pathway for riboflavin (vitamin B
2
) is exceptionally conserved among diverse insect-associated
Wolbachia
strains, and
Wolbachia
's riboflavin provisioning certainly contributes to growth, survival, and reproduction in an insect. These findings uncover a nutritional mechanism of a
Wolbachia
-mediated fitness benefit, which provides empirical evidence highlighting a “Jekyll and Hyde” aspect of
Wolbachia
infection.
Publisher
American Society for Microbiology
Cited by
109 articles.
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