Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster To Maintain Sinorhizobium-Legume Mutualism
ABSTRACT 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 la...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-02-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.02900-21 |
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| author | Ke-Han Liu Biliang Zhang Bo-Sen Yang Wen-Tao Shi Yu-Fei Li Yin Wang Pan Zhang Jian Jiao Chang-Fu Tian |
| author_facet | Ke-Han Liu Biliang Zhang Bo-Sen Yang Wen-Tao Shi Yu-Fei Li Yin Wang Pan Zhang Jian Jiao Chang-Fu Tian |
| author_sort | Ke-Han Liu |
| collection | DOAJ |
| description | ABSTRACT 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. IMPORTANCE Iron is a public good explored by both eukaryotes and prokaryotes. The abundant ferric form is insoluble under neutral and basic pH conditions, and many bacteria secrete siderophores forming soluble ferric siderophore complexes, which can be then taken up by specific receptors and transporters. Siderophore biosynthesis and uptake machineries can be horizontally transferred among bacteria in nature. Despite increasing attention on the importance of siderophores in host-microbiota interactions, the regulatory integration process of transferred siderophore biosynthesis and transport genes is poorly understood in an evolutionary context. By focusing on the mutualistic rhizobium-legume symbiosis, here, we report how a naturally synthetic foreign siderophore gene cluster was integrated with the rhizobial indigenous regulation cascade, which is essential for maintaining mutualistic interactions. |
| first_indexed | 2024-12-24T00:45:55Z |
| format | Article |
| id | doaj.art-cea098f100f045449af8313778430f11 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-24T00:45:55Z |
| publishDate | 2022-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-cea098f100f045449af8313778430f112022-12-21T17:23:49ZengAmerican Society for MicrobiologymBio2150-75112022-02-0113110.1128/mbio.02900-21Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster To Maintain Sinorhizobium-Legume MutualismKe-Han Liu0Biliang Zhang1Bo-Sen Yang2Wen-Tao Shi3Yu-Fei Li4Yin Wang5Pan Zhang6Jian Jiao7Chang-Fu Tian8State Key Laboratory of Agrobiotechnology, and College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agrobiotechnology, and College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agrobiotechnology, and College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agrobiotechnology, and College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agrobiotechnology, and College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agrobiotechnology, and College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agrobiotechnology, and College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agrobiotechnology, and College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agrobiotechnology, and College of Biological Sciences, China Agricultural University, Beijing, ChinaABSTRACT 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. IMPORTANCE Iron is a public good explored by both eukaryotes and prokaryotes. The abundant ferric form is insoluble under neutral and basic pH conditions, and many bacteria secrete siderophores forming soluble ferric siderophore complexes, which can be then taken up by specific receptors and transporters. Siderophore biosynthesis and uptake machineries can be horizontally transferred among bacteria in nature. Despite increasing attention on the importance of siderophores in host-microbiota interactions, the regulatory integration process of transferred siderophore biosynthesis and transport genes is poorly understood in an evolutionary context. By focusing on the mutualistic rhizobium-legume symbiosis, here, we report how a naturally synthetic foreign siderophore gene cluster was integrated with the rhizobial indigenous regulation cascade, which is essential for maintaining mutualistic interactions.https://journals.asm.org/doi/10.1128/mbio.02900-21horizontal gene transferpetrobactinsoybeansymbiosis |
| spellingShingle | Ke-Han Liu Biliang Zhang Bo-Sen Yang Wen-Tao Shi Yu-Fei Li Yin Wang Pan Zhang Jian Jiao Chang-Fu Tian Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster To Maintain Sinorhizobium-Legume Mutualism mBio horizontal gene transfer petrobactin soybean symbiosis |
| 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 | horizontal gene transfer petrobactin soybean symbiosis |
| url | https://journals.asm.org/doi/10.1128/mbio.02900-21 |
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