Stringent Expression Control of Pathogenic R-body Production in Legume Symbiont <italic toggle="yes">Azorhizobium caulinodans</italic>

ABSTRACT R bodies are insoluble large polymers consisting of small proteins encoded by reb genes and are coiled into cylindrical structures in bacterial cells. They were first discovered in Caedibacter species, which are obligate endosymbionts of paramecia. Caedibacter confers a killer trait on the...

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Autores principales:	Jun-ichi Matsuoka, Fumiko Ishizuna, Keigo Kurumisawa, Kengo Morohashi, Tetsuhiro Ogawa, Makoto Hidaka, Katsuharu Saito, Tatsuhiro Ezawa, Toshihiro Aono
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	R body legume pathogenesis reb gene rhizobia symbiosis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b0924899dbc54f9a8814bbfd38ba7142
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spelling	oai:doaj.org-article:b0924899dbc54f9a8814bbfd38ba71422021-11-15T15:51:43ZStringent Expression Control of Pathogenic R-body Production in Legume Symbiont <italic toggle="yes">Azorhizobium caulinodans</italic>10.1128/mBio.00715-172150-7511https://doaj.org/article/b0924899dbc54f9a8814bbfd38ba71422017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00715-17https://doaj.org/toc/2150-7511ABSTRACT R bodies are insoluble large polymers consisting of small proteins encoded by reb genes and are coiled into cylindrical structures in bacterial cells. They were first discovered in Caedibacter species, which are obligate endosymbionts of paramecia. Caedibacter confers a killer trait on the host paramecia. R-body-producing symbionts are released from their host paramecia and kill symbiont-free paramecia after ingestion. The roles of R bodies have not been explained in bacteria other than Caedibacter. Azorhizobium caulinodans ORS571, a microsymbiont of the legume Sesbania rostrata, carries a reb operon containing four reb genes that are regulated by the repressor PraR. Herein, deletion of the praR gene resulted in R-body formation and death of host plant cells. The rebR gene in the reb operon encodes an activator. Three PraR binding sites and a RebR binding site are present in the promoter region of the reb operon. Expression analyses using strains with mutations within the PraR binding site and/or the RebR binding site revealed that PraR and RebR directly control the expression of the reb operon and that PraR dominantly represses reb expression. Furthermore, we found that the reb operon is highly expressed at low temperatures and that 2-oxoglutarate induces the expression of the reb operon by inhibiting PraR binding to the reb promoter. We conclude that R bodies are toxic not only in paramecium symbiosis but also in relationships between other bacteria and eukaryotic cells and that R-body formation is controlled by environmental factors. IMPORTANCE Caedibacter species, which are obligate endosymbiotic bacteria of paramecia, produce R bodies, and R-body-producing endosymbionts that are released from their hosts are pathogenic to symbiont-free paramecia. Besides Caedibacter species, R bodies have also been observed in a few free-living bacteria, but the significance of R-body production in these bacteria is still unknown. Recent advances in genome sequencing technologies revealed that many Gram-negative bacteria possess reb genes encoding R-body components, and interestingly, many of them are animal and plant pathogens. Azorhizobium caulinodans, a microsymbiont of the tropical legume Sesbania rostrata, also possesses reb genes. In this study, we demonstrate that A. caulinodans has ability to kill the host plant cells by producing R bodies, suggesting that pathogenicity conferred by an R body might be universal in bacteria possessing reb genes. Furthermore, we provide the first insight into the molecular mechanism underlying the expression of R-body production in response to environmental factors, such as temperature and 2-oxoglutarate.Jun-ichi MatsuokaFumiko IshizunaKeigo KurumisawaKengo MorohashiTetsuhiro OgawaMakoto HidakaKatsuharu SaitoTatsuhiro EzawaToshihiro AonoAmerican Society for MicrobiologyarticleR bodylegumepathogenesisreb generhizobiasymbiosisMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	R body legume pathogenesis reb gene rhizobia symbiosis Microbiology QR1-502
spellingShingle	R body legume pathogenesis reb gene rhizobia symbiosis Microbiology QR1-502 Jun-ichi Matsuoka Fumiko Ishizuna Keigo Kurumisawa Kengo Morohashi Tetsuhiro Ogawa Makoto Hidaka Katsuharu Saito Tatsuhiro Ezawa Toshihiro Aono Stringent Expression Control of Pathogenic R-body Production in Legume Symbiont <italic toggle="yes">Azorhizobium caulinodans</italic>
description	ABSTRACT R bodies are insoluble large polymers consisting of small proteins encoded by reb genes and are coiled into cylindrical structures in bacterial cells. They were first discovered in Caedibacter species, which are obligate endosymbionts of paramecia. Caedibacter confers a killer trait on the host paramecia. R-body-producing symbionts are released from their host paramecia and kill symbiont-free paramecia after ingestion. The roles of R bodies have not been explained in bacteria other than Caedibacter. Azorhizobium caulinodans ORS571, a microsymbiont of the legume Sesbania rostrata, carries a reb operon containing four reb genes that are regulated by the repressor PraR. Herein, deletion of the praR gene resulted in R-body formation and death of host plant cells. The rebR gene in the reb operon encodes an activator. Three PraR binding sites and a RebR binding site are present in the promoter region of the reb operon. Expression analyses using strains with mutations within the PraR binding site and/or the RebR binding site revealed that PraR and RebR directly control the expression of the reb operon and that PraR dominantly represses reb expression. Furthermore, we found that the reb operon is highly expressed at low temperatures and that 2-oxoglutarate induces the expression of the reb operon by inhibiting PraR binding to the reb promoter. We conclude that R bodies are toxic not only in paramecium symbiosis but also in relationships between other bacteria and eukaryotic cells and that R-body formation is controlled by environmental factors. IMPORTANCE Caedibacter species, which are obligate endosymbiotic bacteria of paramecia, produce R bodies, and R-body-producing endosymbionts that are released from their hosts are pathogenic to symbiont-free paramecia. Besides Caedibacter species, R bodies have also been observed in a few free-living bacteria, but the significance of R-body production in these bacteria is still unknown. Recent advances in genome sequencing technologies revealed that many Gram-negative bacteria possess reb genes encoding R-body components, and interestingly, many of them are animal and plant pathogens. Azorhizobium caulinodans, a microsymbiont of the tropical legume Sesbania rostrata, also possesses reb genes. In this study, we demonstrate that A. caulinodans has ability to kill the host plant cells by producing R bodies, suggesting that pathogenicity conferred by an R body might be universal in bacteria possessing reb genes. Furthermore, we provide the first insight into the molecular mechanism underlying the expression of R-body production in response to environmental factors, such as temperature and 2-oxoglutarate.
format	article
author	Jun-ichi Matsuoka Fumiko Ishizuna Keigo Kurumisawa Kengo Morohashi Tetsuhiro Ogawa Makoto Hidaka Katsuharu Saito Tatsuhiro Ezawa Toshihiro Aono
author_facet	Jun-ichi Matsuoka Fumiko Ishizuna Keigo Kurumisawa Kengo Morohashi Tetsuhiro Ogawa Makoto Hidaka Katsuharu Saito Tatsuhiro Ezawa Toshihiro Aono
author_sort	Jun-ichi Matsuoka
title	Stringent Expression Control of Pathogenic R-body Production in Legume Symbiont <italic toggle="yes">Azorhizobium caulinodans</italic>
title_short	Stringent Expression Control of Pathogenic R-body Production in Legume Symbiont <italic toggle="yes">Azorhizobium caulinodans</italic>
title_full	Stringent Expression Control of Pathogenic R-body Production in Legume Symbiont <italic toggle="yes">Azorhizobium caulinodans</italic>
title_fullStr	Stringent Expression Control of Pathogenic R-body Production in Legume Symbiont <italic toggle="yes">Azorhizobium caulinodans</italic>
title_full_unstemmed	Stringent Expression Control of Pathogenic R-body Production in Legume Symbiont <italic toggle="yes">Azorhizobium caulinodans</italic>
title_sort	stringent expression control of pathogenic r-body production in legume symbiont <italic toggle="yes">azorhizobium caulinodans</italic>
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/b0924899dbc54f9a8814bbfd38ba7142
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Stringent Expression Control of Pathogenic R-body Production in Legume Symbiont <italic toggle="yes">Azorhizobium caulinodans</italic>

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