Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery

ABSTRACT Pathogenic bacteria need high-affinity zinc uptake systems to counteract the nutritional immunity exerted by infected hosts. However, our understanding of zinc homeostasis in mutualistic systems such as the rhizobium-legume symbiosis is limited. Here, we show that the conserved high-affinit...

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Autores principales:	Pan Zhang, Biliang Zhang, Jian Jiao, Shi-Qi Dai, Wen-Xin Chen, Chang-Fu Tian
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Sinorhizobium soybean zinc nodulation compatibility Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a3806ce18b69471086b62904753537f1
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spelling	oai:doaj.org-article:a3806ce18b69471086b62904753537f12021-11-15T15:56:58ZModulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery10.1128/mBio.03193-192150-7511https://doaj.org/article/a3806ce18b69471086b62904753537f12020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.03193-19https://doaj.org/toc/2150-7511ABSTRACT Pathogenic bacteria need high-affinity zinc uptake systems to counteract the nutritional immunity exerted by infected hosts. However, our understanding of zinc homeostasis in mutualistic systems such as the rhizobium-legume symbiosis is limited. Here, we show that the conserved high-affinity zinc transporter ZnuABC and accessory transporter proteins (Zip1, Zip2, and c06450) made cumulative contributions to nodulation of the broad-host-range strain Sinorhizobium fredii CCBAU45436. Zur acted as a zinc-dependent repressor for the znuC-znuB-zur operon, znuA, and c06450 by binding to the associated Zur box, but did not regulate zip1 and zip2. ZnuABC was the major zinc transporter. Combined mutants lacking znuA and one of the three accessory genes had more severe defects in nodulation and growth under zinc starvation conditions than the znuA mutant, though rhizoplane colonization by these mutants was not impaired. In contrast to the elite strain CCBAU45436, more drastic symbiotic defects were observed for the znuA mutants of other Sinorhizobium strains, which lack at least one of the three accessory genes in their genomes and are characterized by their limited host range and geographical distribution. The znu-derived mutants showed a higher expression level of nod genes involved in Nod factor biosynthesis and a reduced expression of genes encoding a type three secretion system and its effector NopP, which can interfere with the host immune system. Application of exogenous zinc restored the nodulation ability of these znu-derived mutants. Therefore, the conserved ZnuABC and accessory components in the zinc starvation machinery play an important role in modulating symbiotic compatibility. IMPORTANCE The rhizobium-legume symbiosis contributes around 65% of biological nitrogen fixation in agriculture systems and is critical for sustainable agriculture by reducing the amount of chemical nitrogen fertilizer being used. Rhizobial inocula have been commercialized for more than 100 years, but the efficiency of inoculation can vary among legume cultivars, field sites, and years. These long-lasting challenging problems impede the establishment of a sustainable agriculture, particularly in developing countries. Here, we report that rhizobial zinc starvation machinery containing a conserved high-affinity zinc transporter and accessory components makes cumulative contributions to modulating rhizobial symbiotic compatibility. This work highlights a critical role of largely unexplored nutritional immunity in the rhizobium-legume symbiosis, which makes zinc starvation machinery an attractive target for improving rhizobial symbiotic compatibility.Pan ZhangBiliang ZhangJian JiaoShi-Qi DaiWen-Xin ChenChang-Fu TianAmerican Society for MicrobiologyarticleSinorhizobiumsoybeanzincnodulationcompatibilityMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Sinorhizobium soybean zinc nodulation compatibility Microbiology QR1-502
spellingShingle	Sinorhizobium soybean zinc nodulation compatibility Microbiology QR1-502 Pan Zhang Biliang Zhang Jian Jiao Shi-Qi Dai Wen-Xin Chen Chang-Fu Tian Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery
description	ABSTRACT Pathogenic bacteria need high-affinity zinc uptake systems to counteract the nutritional immunity exerted by infected hosts. However, our understanding of zinc homeostasis in mutualistic systems such as the rhizobium-legume symbiosis is limited. Here, we show that the conserved high-affinity zinc transporter ZnuABC and accessory transporter proteins (Zip1, Zip2, and c06450) made cumulative contributions to nodulation of the broad-host-range strain Sinorhizobium fredii CCBAU45436. Zur acted as a zinc-dependent repressor for the znuC-znuB-zur operon, znuA, and c06450 by binding to the associated Zur box, but did not regulate zip1 and zip2. ZnuABC was the major zinc transporter. Combined mutants lacking znuA and one of the three accessory genes had more severe defects in nodulation and growth under zinc starvation conditions than the znuA mutant, though rhizoplane colonization by these mutants was not impaired. In contrast to the elite strain CCBAU45436, more drastic symbiotic defects were observed for the znuA mutants of other Sinorhizobium strains, which lack at least one of the three accessory genes in their genomes and are characterized by their limited host range and geographical distribution. The znu-derived mutants showed a higher expression level of nod genes involved in Nod factor biosynthesis and a reduced expression of genes encoding a type three secretion system and its effector NopP, which can interfere with the host immune system. Application of exogenous zinc restored the nodulation ability of these znu-derived mutants. Therefore, the conserved ZnuABC and accessory components in the zinc starvation machinery play an important role in modulating symbiotic compatibility. IMPORTANCE The rhizobium-legume symbiosis contributes around 65% of biological nitrogen fixation in agriculture systems and is critical for sustainable agriculture by reducing the amount of chemical nitrogen fertilizer being used. Rhizobial inocula have been commercialized for more than 100 years, but the efficiency of inoculation can vary among legume cultivars, field sites, and years. These long-lasting challenging problems impede the establishment of a sustainable agriculture, particularly in developing countries. Here, we report that rhizobial zinc starvation machinery containing a conserved high-affinity zinc transporter and accessory components makes cumulative contributions to modulating rhizobial symbiotic compatibility. This work highlights a critical role of largely unexplored nutritional immunity in the rhizobium-legume symbiosis, which makes zinc starvation machinery an attractive target for improving rhizobial symbiotic compatibility.
format	article
author	Pan Zhang Biliang Zhang Jian Jiao Shi-Qi Dai Wen-Xin Chen Chang-Fu Tian
author_facet	Pan Zhang Biliang Zhang Jian Jiao Shi-Qi Dai Wen-Xin Chen Chang-Fu Tian
author_sort	Pan Zhang
title	Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery
title_short	Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery
title_full	Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery
title_fullStr	Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery
title_full_unstemmed	Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery
title_sort	modulation of symbiotic compatibility by rhizobial zinc starvation machinery
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/a3806ce18b69471086b62904753537f1
work_keys_str_mv	AT panzhang modulationofsymbioticcompatibilitybyrhizobialzincstarvationmachinery AT biliangzhang modulationofsymbioticcompatibilitybyrhizobialzincstarvationmachinery AT jianjiao modulationofsymbioticcompatibilitybyrhizobialzincstarvationmachinery AT shiqidai modulationofsymbioticcompatibilitybyrhizobialzincstarvationmachinery AT wenxinchen modulationofsymbioticcompatibilitybyrhizobialzincstarvationmachinery AT changfutian modulationofsymbioticcompatibilitybyrhizobialzincstarvationmachinery
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Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery

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