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Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster To Maintain Sinorhizobium-Legume Mutualism

Iron homeostasis is strictly regulated in cellular organisms. The Rhizobiales order enriched with symbiotic and pathogenic bacteria has evolved a lineage-specific regulator, RirA, responding to iron fluctuations. However, the regulatory role of RirA in bacterium-host interactions remains largely unk...

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Autores principales: Liu, Ke-Han, Zhang, Biliang, Yang, Bo-Sen, Shi, Wen-Tao, Li, Yu-Fei, Wang, Yin, Zhang, Pan, Jiao, Jian, Tian, Chang-Fu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8822346/
https://www.ncbi.nlm.nih.gov/pubmed/35130720
http://dx.doi.org/10.1128/mbio.02900-21
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author Liu, Ke-Han
Zhang, Biliang
Yang, Bo-Sen
Shi, Wen-Tao
Li, Yu-Fei
Wang, Yin
Zhang, Pan
Jiao, Jian
Tian, Chang-Fu
author_facet Liu, Ke-Han
Zhang, Biliang
Yang, Bo-Sen
Shi, Wen-Tao
Li, Yu-Fei
Wang, Yin
Zhang, Pan
Jiao, Jian
Tian, Chang-Fu
author_sort Liu, Ke-Han
collection PubMed
description Iron homeostasis is strictly regulated in cellular organisms. The Rhizobiales order enriched with symbiotic and pathogenic bacteria has evolved a lineage-specific regulator, RirA, responding to iron fluctuations. However, the regulatory role of RirA in bacterium-host interactions remains largely unknown. Here, we report that RirA is essential for mutualistic interactions of Sinorhizobium fredii with its legume hosts by repressing a gene cluster directing biosynthesis and transport of petrobactin siderophore. Genes encoding an inner membrane ABC transporter (fat) and the biosynthetic machinery (asb) of petrobactin siderophore are sporadically distributed in Gram-positive and Gram-negative bacteria. An outer membrane siderophore receptor gene (fprA) was naturally assembled with asb and fat, forming a long polycistron in S. fredii. An indigenous regulation cascade harboring an inner membrane protease (RseP), a sigma factor (FecI), and its anti-sigma protein (FecR) were involved in direct activation of the fprA-asb-fat polycistron. Operons harboring fecI and fprA-asb-fat, and those encoding the indigenous TonB-ExbB-ExbD complex delivering energy to the outer membrane transport activity, were directly repressed by RirA under iron-replete conditions. The rirA deletion led to upregulation of these operons and iron overload in nodules, impaired intracellular persistence, and symbiotic nitrogen fixation of rhizobia. Mutualistic defects of the rirA mutant can be rescued by blocking activities of this naturally “synthetic” circuit for siderophore biosynthesis and transport. These findings not only are significant for understanding iron homeostasis of mutualistic interactions but also provide insights into assembly and integration of foreign machineries for biosynthesis and transport of siderophores, horizontal transfer of which is selected in microbiota.
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spelling pubmed-88223462022-02-17 Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster To Maintain Sinorhizobium-Legume Mutualism Liu, Ke-Han Zhang, Biliang Yang, Bo-Sen Shi, Wen-Tao Li, Yu-Fei Wang, Yin Zhang, Pan Jiao, Jian Tian, Chang-Fu mBio Research Article Iron homeostasis is strictly regulated in cellular organisms. The Rhizobiales order enriched with symbiotic and pathogenic bacteria has evolved a lineage-specific regulator, RirA, responding to iron fluctuations. However, the regulatory role of RirA in bacterium-host interactions remains largely unknown. Here, we report that RirA is essential for mutualistic interactions of Sinorhizobium fredii with its legume hosts by repressing a gene cluster directing biosynthesis and transport of petrobactin siderophore. Genes encoding an inner membrane ABC transporter (fat) and the biosynthetic machinery (asb) of petrobactin siderophore are sporadically distributed in Gram-positive and Gram-negative bacteria. An outer membrane siderophore receptor gene (fprA) was naturally assembled with asb and fat, forming a long polycistron in S. fredii. An indigenous regulation cascade harboring an inner membrane protease (RseP), a sigma factor (FecI), and its anti-sigma protein (FecR) were involved in direct activation of the fprA-asb-fat polycistron. Operons harboring fecI and fprA-asb-fat, and those encoding the indigenous TonB-ExbB-ExbD complex delivering energy to the outer membrane transport activity, were directly repressed by RirA under iron-replete conditions. The rirA deletion led to upregulation of these operons and iron overload in nodules, impaired intracellular persistence, and symbiotic nitrogen fixation of rhizobia. Mutualistic defects of the rirA mutant can be rescued by blocking activities of this naturally “synthetic” circuit for siderophore biosynthesis and transport. These findings not only are significant for understanding iron homeostasis of mutualistic interactions but also provide insights into assembly and integration of foreign machineries for biosynthesis and transport of siderophores, horizontal transfer of which is selected in microbiota. American Society for Microbiology 2022-02-08 /pmc/articles/PMC8822346/ /pubmed/35130720 http://dx.doi.org/10.1128/mbio.02900-21 Text en Copyright © 2022 Liu et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Liu, Ke-Han
Zhang, Biliang
Yang, Bo-Sen
Shi, Wen-Tao
Li, Yu-Fei
Wang, Yin
Zhang, Pan
Jiao, Jian
Tian, Chang-Fu
Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster To Maintain Sinorhizobium-Legume Mutualism
title Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster To Maintain Sinorhizobium-Legume Mutualism
title_full Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster To Maintain Sinorhizobium-Legume Mutualism
title_fullStr Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster To Maintain Sinorhizobium-Legume Mutualism
title_full_unstemmed Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster To Maintain Sinorhizobium-Legume Mutualism
title_short Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster To Maintain Sinorhizobium-Legume Mutualism
title_sort rhizobiales-specific rira represses a naturally “synthetic” foreign siderophore gene cluster to maintain sinorhizobium-legume mutualism
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8822346/
https://www.ncbi.nlm.nih.gov/pubmed/35130720
http://dx.doi.org/10.1128/mbio.02900-21
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