Riboflavin Provisioning Underlies <italic toggle="yes">Wolbachia</italic>'s Fitness Contribution to Its Insect Host

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 inherite...

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Autores principales:	Minoru Moriyama, Naruo Nikoh, Takahiro Hosokawa, Takema Fukatsu
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6aa0fae4e4a845d4befe5be02b943870
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spelling	oai:doaj.org-article:6aa0fae4e4a845d4befe5be02b9438702021-11-15T15:41:24ZRiboflavin Provisioning Underlies <italic toggle="yes">Wolbachia</italic>'s Fitness Contribution to Its Insect Host10.1128/mBio.01732-152150-7511https://doaj.org/article/6aa0fae4e4a845d4befe5be02b9438702015-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01732-15https://doaj.org/toc/2150-7511ABSTRACT 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 B2), 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 B2) 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.Minoru MoriyamaNaruo NikohTakahiro HosokawaTakema FukatsuAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 6 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Minoru Moriyama Naruo Nikoh Takahiro Hosokawa Takema Fukatsu Riboflavin Provisioning Underlies <italic toggle="yes">Wolbachia</italic>'s Fitness Contribution to Its Insect Host
description	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 B2), 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 B2) 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.
format	article
author	Minoru Moriyama Naruo Nikoh Takahiro Hosokawa Takema Fukatsu
author_facet	Minoru Moriyama Naruo Nikoh Takahiro Hosokawa Takema Fukatsu
author_sort	Minoru Moriyama
title	Riboflavin Provisioning Underlies <italic toggle="yes">Wolbachia</italic>'s Fitness Contribution to Its Insect Host
title_short	Riboflavin Provisioning Underlies <italic toggle="yes">Wolbachia</italic>'s Fitness Contribution to Its Insect Host
title_full	Riboflavin Provisioning Underlies <italic toggle="yes">Wolbachia</italic>'s Fitness Contribution to Its Insect Host
title_fullStr	Riboflavin Provisioning Underlies <italic toggle="yes">Wolbachia</italic>'s Fitness Contribution to Its Insect Host
title_full_unstemmed	Riboflavin Provisioning Underlies <italic toggle="yes">Wolbachia</italic>'s Fitness Contribution to Its Insect Host
title_sort	riboflavin provisioning underlies <italic toggle="yes">wolbachia</italic>'s fitness contribution to its insect host
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/6aa0fae4e4a845d4befe5be02b943870
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Riboflavin Provisioning Underlies <italic toggle="yes">Wolbachia</italic>'s Fitness Contribution to Its Insect Host

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