Pervasive RNA Regulation of Metabolism Enhances the Root Colonization Ability of Nitrogen-Fixing Symbiotic α-Rhizobia
ABSTRACT The rhizosphere and rhizoplane are nutrient-rich but selective environments for the root microbiome. Here, we deciphered a posttranscriptional network regulated by the homologous trans-small RNAs (sRNAs) AbcR1 and AbcR2, which rewire the metabolism of the nitrogen-fixing α-rhizobium Sinorhi...
Ausführliche Beschreibung
Autor*in: |
Natalia I. García-Tomsig [verfasserIn] Marta Robledo [verfasserIn] George C. diCenzo [verfasserIn] Alessio Mengoni [verfasserIn] Vicenta Millán [verfasserIn] Alexandra Peregrina [verfasserIn] Alejandro Uceta [verfasserIn] José I. Jiménez-Zurdo [verfasserIn] |
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E-Artikel |
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Sprache: |
Englisch |
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2022 |
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Übergeordnetes Werk: |
In: mBio - American Society for Microbiology, 2010, 13(2022), 1 |
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Übergeordnetes Werk: |
volume:13 ; year:2022 ; number:1 |
Links: |
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DOI / URN: |
10.1128/mbio.03576-21 |
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Katalog-ID: |
DOAJ013733427 |
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520 | |a ABSTRACT The rhizosphere and rhizoplane are nutrient-rich but selective environments for the root microbiome. Here, we deciphered a posttranscriptional network regulated by the homologous trans-small RNAs (sRNAs) AbcR1 and AbcR2, which rewire the metabolism of the nitrogen-fixing α-rhizobium Sinorhizobium meliloti during preinfection stages of symbiosis with its legume host alfalfa. The LysR-type regulator LsrB, which transduces the cell redox state, is indispensable for AbcR1 expression in actively dividing bacteria, whereas the stress-induced transcription of AbcR2 depends on the alternative σ factor RpoH1. MS2 affinity purification coupled with RNA sequencing unveiled exceptionally large and overlapping AbcR1/2 mRNA interactomes, jointly representing ⁓6% of the S. meliloti protein-coding genes. Most mRNAs encode transport/metabolic proteins whose translation is silenced by base pairing to two distinct anti-Shine Dalgarno motifs that function independently in both sRNAs. A metabolic model-aided analysis of the targetomes predicted changes in AbcR1/2 expression driven by shifts in carbon/nitrogen sources, which were confirmed experimentally. Low AbcR1/2 levels in some defined media anticipated overexpression growth phenotypes linked to the silencing of specific mRNAs. As a proof of principle, we confirmed AbcR1/2-mediated downregulation of the l-amino acid AapQ permease. AbcR1/2 interactomes are well represented in rhizosphere-related S. meliloti transcriptomic signatures. Remarkably, a lack of AbcR1 specifically compromised the ability of S. meliloti to colonize the root rhizoplane. The AbcR1 regulon likely ranks the utilization of available substrates to optimize metabolism, thus conferring on S. meliloti an advantage for efficient rhizosphere/rhizoplane colonization. AbcR1 regulation is predicted to be conserved in related α-rhizobia, which opens unprecedented possibilities for engineering highly competitive biofertilizers. IMPORTANCE Nitrogen-fixing root nodule symbioses between rhizobia and legume plants provide more than half of the combined nitrogen incorporated annually into terrestrial ecosystems, rendering plant growth independent of environmentally unfriendly chemical fertilizers. The success of symbiosis depends primarily on the capacity of rhizobia to establish competitive populations in soil and rhizosphere environments. Here, we provide insights into the regulation and architecture of an extensive RNA posttranscriptional network that fine-tunes the metabolism of the alfalfa symbiont S. meliloti, thereby enhancing the ability of this beneficial bacterium to colonize nutrient-rich but extremely selective niches, such as the rhizosphere of its host plant. This pervasive RNA regulation of metabolism is a major adaptive mechanism, predicted to operate in diverse rhizobial species. Because RNA regulation relies on modifiable base-pairing interactions, our findings open unexplored avenues for engineering the legumes rhizobiome within sustainable agricultural practices. | ||
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10.1128/mbio.03576-21 doi (DE-627)DOAJ013733427 (DE-599)DOAJabc6c4de55e74ccf9881d66363a54117 DE-627 ger DE-627 rakwb eng QR1-502 Natalia I. García-Tomsig verfasserin aut Pervasive RNA Regulation of Metabolism Enhances the Root Colonization Ability of Nitrogen-Fixing Symbiotic α-Rhizobia 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT The rhizosphere and rhizoplane are nutrient-rich but selective environments for the root microbiome. Here, we deciphered a posttranscriptional network regulated by the homologous trans-small RNAs (sRNAs) AbcR1 and AbcR2, which rewire the metabolism of the nitrogen-fixing α-rhizobium Sinorhizobium meliloti during preinfection stages of symbiosis with its legume host alfalfa. The LysR-type regulator LsrB, which transduces the cell redox state, is indispensable for AbcR1 expression in actively dividing bacteria, whereas the stress-induced transcription of AbcR2 depends on the alternative σ factor RpoH1. MS2 affinity purification coupled with RNA sequencing unveiled exceptionally large and overlapping AbcR1/2 mRNA interactomes, jointly representing ⁓6% of the S. meliloti protein-coding genes. Most mRNAs encode transport/metabolic proteins whose translation is silenced by base pairing to two distinct anti-Shine Dalgarno motifs that function independently in both sRNAs. A metabolic model-aided analysis of the targetomes predicted changes in AbcR1/2 expression driven by shifts in carbon/nitrogen sources, which were confirmed experimentally. Low AbcR1/2 levels in some defined media anticipated overexpression growth phenotypes linked to the silencing of specific mRNAs. As a proof of principle, we confirmed AbcR1/2-mediated downregulation of the l-amino acid AapQ permease. AbcR1/2 interactomes are well represented in rhizosphere-related S. meliloti transcriptomic signatures. Remarkably, a lack of AbcR1 specifically compromised the ability of S. meliloti to colonize the root rhizoplane. The AbcR1 regulon likely ranks the utilization of available substrates to optimize metabolism, thus conferring on S. meliloti an advantage for efficient rhizosphere/rhizoplane colonization. AbcR1 regulation is predicted to be conserved in related α-rhizobia, which opens unprecedented possibilities for engineering highly competitive biofertilizers. IMPORTANCE Nitrogen-fixing root nodule symbioses between rhizobia and legume plants provide more than half of the combined nitrogen incorporated annually into terrestrial ecosystems, rendering plant growth independent of environmentally unfriendly chemical fertilizers. The success of symbiosis depends primarily on the capacity of rhizobia to establish competitive populations in soil and rhizosphere environments. Here, we provide insights into the regulation and architecture of an extensive RNA posttranscriptional network that fine-tunes the metabolism of the alfalfa symbiont S. meliloti, thereby enhancing the ability of this beneficial bacterium to colonize nutrient-rich but extremely selective niches, such as the rhizosphere of its host plant. This pervasive RNA regulation of metabolism is a major adaptive mechanism, predicted to operate in diverse rhizobial species. Because RNA regulation relies on modifiable base-pairing interactions, our findings open unexplored avenues for engineering the legumes rhizobiome within sustainable agricultural practices. Sinorhizobium meliloti alphaproteobacteria noncoding RNA riboregulation Microbiology Marta Robledo verfasserin aut George C. diCenzo verfasserin aut Alessio Mengoni verfasserin aut Vicenta Millán verfasserin aut Alexandra Peregrina verfasserin aut Alejandro Uceta verfasserin aut José I. Jiménez-Zurdo verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 1 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:1 https://doi.org/10.1128/mbio.03576-21 kostenfrei https://doaj.org/article/abc6c4de55e74ccf9881d66363a54117 kostenfrei https://journals.asm.org/doi/10.1128/mbio.03576-21 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 1 |
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10.1128/mbio.03576-21 doi (DE-627)DOAJ013733427 (DE-599)DOAJabc6c4de55e74ccf9881d66363a54117 DE-627 ger DE-627 rakwb eng QR1-502 Natalia I. García-Tomsig verfasserin aut Pervasive RNA Regulation of Metabolism Enhances the Root Colonization Ability of Nitrogen-Fixing Symbiotic α-Rhizobia 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT The rhizosphere and rhizoplane are nutrient-rich but selective environments for the root microbiome. Here, we deciphered a posttranscriptional network regulated by the homologous trans-small RNAs (sRNAs) AbcR1 and AbcR2, which rewire the metabolism of the nitrogen-fixing α-rhizobium Sinorhizobium meliloti during preinfection stages of symbiosis with its legume host alfalfa. The LysR-type regulator LsrB, which transduces the cell redox state, is indispensable for AbcR1 expression in actively dividing bacteria, whereas the stress-induced transcription of AbcR2 depends on the alternative σ factor RpoH1. MS2 affinity purification coupled with RNA sequencing unveiled exceptionally large and overlapping AbcR1/2 mRNA interactomes, jointly representing ⁓6% of the S. meliloti protein-coding genes. Most mRNAs encode transport/metabolic proteins whose translation is silenced by base pairing to two distinct anti-Shine Dalgarno motifs that function independently in both sRNAs. A metabolic model-aided analysis of the targetomes predicted changes in AbcR1/2 expression driven by shifts in carbon/nitrogen sources, which were confirmed experimentally. Low AbcR1/2 levels in some defined media anticipated overexpression growth phenotypes linked to the silencing of specific mRNAs. As a proof of principle, we confirmed AbcR1/2-mediated downregulation of the l-amino acid AapQ permease. AbcR1/2 interactomes are well represented in rhizosphere-related S. meliloti transcriptomic signatures. Remarkably, a lack of AbcR1 specifically compromised the ability of S. meliloti to colonize the root rhizoplane. The AbcR1 regulon likely ranks the utilization of available substrates to optimize metabolism, thus conferring on S. meliloti an advantage for efficient rhizosphere/rhizoplane colonization. AbcR1 regulation is predicted to be conserved in related α-rhizobia, which opens unprecedented possibilities for engineering highly competitive biofertilizers. IMPORTANCE Nitrogen-fixing root nodule symbioses between rhizobia and legume plants provide more than half of the combined nitrogen incorporated annually into terrestrial ecosystems, rendering plant growth independent of environmentally unfriendly chemical fertilizers. The success of symbiosis depends primarily on the capacity of rhizobia to establish competitive populations in soil and rhizosphere environments. Here, we provide insights into the regulation and architecture of an extensive RNA posttranscriptional network that fine-tunes the metabolism of the alfalfa symbiont S. meliloti, thereby enhancing the ability of this beneficial bacterium to colonize nutrient-rich but extremely selective niches, such as the rhizosphere of its host plant. This pervasive RNA regulation of metabolism is a major adaptive mechanism, predicted to operate in diverse rhizobial species. Because RNA regulation relies on modifiable base-pairing interactions, our findings open unexplored avenues for engineering the legumes rhizobiome within sustainable agricultural practices. Sinorhizobium meliloti alphaproteobacteria noncoding RNA riboregulation Microbiology Marta Robledo verfasserin aut George C. diCenzo verfasserin aut Alessio Mengoni verfasserin aut Vicenta Millán verfasserin aut Alexandra Peregrina verfasserin aut Alejandro Uceta verfasserin aut José I. Jiménez-Zurdo verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 1 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:1 https://doi.org/10.1128/mbio.03576-21 kostenfrei https://doaj.org/article/abc6c4de55e74ccf9881d66363a54117 kostenfrei https://journals.asm.org/doi/10.1128/mbio.03576-21 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 1 |
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10.1128/mbio.03576-21 doi (DE-627)DOAJ013733427 (DE-599)DOAJabc6c4de55e74ccf9881d66363a54117 DE-627 ger DE-627 rakwb eng QR1-502 Natalia I. García-Tomsig verfasserin aut Pervasive RNA Regulation of Metabolism Enhances the Root Colonization Ability of Nitrogen-Fixing Symbiotic α-Rhizobia 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT The rhizosphere and rhizoplane are nutrient-rich but selective environments for the root microbiome. Here, we deciphered a posttranscriptional network regulated by the homologous trans-small RNAs (sRNAs) AbcR1 and AbcR2, which rewire the metabolism of the nitrogen-fixing α-rhizobium Sinorhizobium meliloti during preinfection stages of symbiosis with its legume host alfalfa. The LysR-type regulator LsrB, which transduces the cell redox state, is indispensable for AbcR1 expression in actively dividing bacteria, whereas the stress-induced transcription of AbcR2 depends on the alternative σ factor RpoH1. MS2 affinity purification coupled with RNA sequencing unveiled exceptionally large and overlapping AbcR1/2 mRNA interactomes, jointly representing ⁓6% of the S. meliloti protein-coding genes. Most mRNAs encode transport/metabolic proteins whose translation is silenced by base pairing to two distinct anti-Shine Dalgarno motifs that function independently in both sRNAs. A metabolic model-aided analysis of the targetomes predicted changes in AbcR1/2 expression driven by shifts in carbon/nitrogen sources, which were confirmed experimentally. Low AbcR1/2 levels in some defined media anticipated overexpression growth phenotypes linked to the silencing of specific mRNAs. As a proof of principle, we confirmed AbcR1/2-mediated downregulation of the l-amino acid AapQ permease. AbcR1/2 interactomes are well represented in rhizosphere-related S. meliloti transcriptomic signatures. Remarkably, a lack of AbcR1 specifically compromised the ability of S. meliloti to colonize the root rhizoplane. The AbcR1 regulon likely ranks the utilization of available substrates to optimize metabolism, thus conferring on S. meliloti an advantage for efficient rhizosphere/rhizoplane colonization. AbcR1 regulation is predicted to be conserved in related α-rhizobia, which opens unprecedented possibilities for engineering highly competitive biofertilizers. IMPORTANCE Nitrogen-fixing root nodule symbioses between rhizobia and legume plants provide more than half of the combined nitrogen incorporated annually into terrestrial ecosystems, rendering plant growth independent of environmentally unfriendly chemical fertilizers. The success of symbiosis depends primarily on the capacity of rhizobia to establish competitive populations in soil and rhizosphere environments. Here, we provide insights into the regulation and architecture of an extensive RNA posttranscriptional network that fine-tunes the metabolism of the alfalfa symbiont S. meliloti, thereby enhancing the ability of this beneficial bacterium to colonize nutrient-rich but extremely selective niches, such as the rhizosphere of its host plant. This pervasive RNA regulation of metabolism is a major adaptive mechanism, predicted to operate in diverse rhizobial species. Because RNA regulation relies on modifiable base-pairing interactions, our findings open unexplored avenues for engineering the legumes rhizobiome within sustainable agricultural practices. Sinorhizobium meliloti alphaproteobacteria noncoding RNA riboregulation Microbiology Marta Robledo verfasserin aut George C. diCenzo verfasserin aut Alessio Mengoni verfasserin aut Vicenta Millán verfasserin aut Alexandra Peregrina verfasserin aut Alejandro Uceta verfasserin aut José I. Jiménez-Zurdo verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 1 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:1 https://doi.org/10.1128/mbio.03576-21 kostenfrei https://doaj.org/article/abc6c4de55e74ccf9881d66363a54117 kostenfrei https://journals.asm.org/doi/10.1128/mbio.03576-21 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 1 |
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10.1128/mbio.03576-21 doi (DE-627)DOAJ013733427 (DE-599)DOAJabc6c4de55e74ccf9881d66363a54117 DE-627 ger DE-627 rakwb eng QR1-502 Natalia I. García-Tomsig verfasserin aut Pervasive RNA Regulation of Metabolism Enhances the Root Colonization Ability of Nitrogen-Fixing Symbiotic α-Rhizobia 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT The rhizosphere and rhizoplane are nutrient-rich but selective environments for the root microbiome. Here, we deciphered a posttranscriptional network regulated by the homologous trans-small RNAs (sRNAs) AbcR1 and AbcR2, which rewire the metabolism of the nitrogen-fixing α-rhizobium Sinorhizobium meliloti during preinfection stages of symbiosis with its legume host alfalfa. The LysR-type regulator LsrB, which transduces the cell redox state, is indispensable for AbcR1 expression in actively dividing bacteria, whereas the stress-induced transcription of AbcR2 depends on the alternative σ factor RpoH1. MS2 affinity purification coupled with RNA sequencing unveiled exceptionally large and overlapping AbcR1/2 mRNA interactomes, jointly representing ⁓6% of the S. meliloti protein-coding genes. Most mRNAs encode transport/metabolic proteins whose translation is silenced by base pairing to two distinct anti-Shine Dalgarno motifs that function independently in both sRNAs. A metabolic model-aided analysis of the targetomes predicted changes in AbcR1/2 expression driven by shifts in carbon/nitrogen sources, which were confirmed experimentally. Low AbcR1/2 levels in some defined media anticipated overexpression growth phenotypes linked to the silencing of specific mRNAs. As a proof of principle, we confirmed AbcR1/2-mediated downregulation of the l-amino acid AapQ permease. AbcR1/2 interactomes are well represented in rhizosphere-related S. meliloti transcriptomic signatures. Remarkably, a lack of AbcR1 specifically compromised the ability of S. meliloti to colonize the root rhizoplane. The AbcR1 regulon likely ranks the utilization of available substrates to optimize metabolism, thus conferring on S. meliloti an advantage for efficient rhizosphere/rhizoplane colonization. AbcR1 regulation is predicted to be conserved in related α-rhizobia, which opens unprecedented possibilities for engineering highly competitive biofertilizers. IMPORTANCE Nitrogen-fixing root nodule symbioses between rhizobia and legume plants provide more than half of the combined nitrogen incorporated annually into terrestrial ecosystems, rendering plant growth independent of environmentally unfriendly chemical fertilizers. The success of symbiosis depends primarily on the capacity of rhizobia to establish competitive populations in soil and rhizosphere environments. Here, we provide insights into the regulation and architecture of an extensive RNA posttranscriptional network that fine-tunes the metabolism of the alfalfa symbiont S. meliloti, thereby enhancing the ability of this beneficial bacterium to colonize nutrient-rich but extremely selective niches, such as the rhizosphere of its host plant. This pervasive RNA regulation of metabolism is a major adaptive mechanism, predicted to operate in diverse rhizobial species. Because RNA regulation relies on modifiable base-pairing interactions, our findings open unexplored avenues for engineering the legumes rhizobiome within sustainable agricultural practices. Sinorhizobium meliloti alphaproteobacteria noncoding RNA riboregulation Microbiology Marta Robledo verfasserin aut George C. diCenzo verfasserin aut Alessio Mengoni verfasserin aut Vicenta Millán verfasserin aut Alexandra Peregrina verfasserin aut Alejandro Uceta verfasserin aut José I. Jiménez-Zurdo verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 1 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:1 https://doi.org/10.1128/mbio.03576-21 kostenfrei https://doaj.org/article/abc6c4de55e74ccf9881d66363a54117 kostenfrei https://journals.asm.org/doi/10.1128/mbio.03576-21 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 1 |
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10.1128/mbio.03576-21 doi (DE-627)DOAJ013733427 (DE-599)DOAJabc6c4de55e74ccf9881d66363a54117 DE-627 ger DE-627 rakwb eng QR1-502 Natalia I. García-Tomsig verfasserin aut Pervasive RNA Regulation of Metabolism Enhances the Root Colonization Ability of Nitrogen-Fixing Symbiotic α-Rhizobia 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT The rhizosphere and rhizoplane are nutrient-rich but selective environments for the root microbiome. Here, we deciphered a posttranscriptional network regulated by the homologous trans-small RNAs (sRNAs) AbcR1 and AbcR2, which rewire the metabolism of the nitrogen-fixing α-rhizobium Sinorhizobium meliloti during preinfection stages of symbiosis with its legume host alfalfa. The LysR-type regulator LsrB, which transduces the cell redox state, is indispensable for AbcR1 expression in actively dividing bacteria, whereas the stress-induced transcription of AbcR2 depends on the alternative σ factor RpoH1. MS2 affinity purification coupled with RNA sequencing unveiled exceptionally large and overlapping AbcR1/2 mRNA interactomes, jointly representing ⁓6% of the S. meliloti protein-coding genes. Most mRNAs encode transport/metabolic proteins whose translation is silenced by base pairing to two distinct anti-Shine Dalgarno motifs that function independently in both sRNAs. A metabolic model-aided analysis of the targetomes predicted changes in AbcR1/2 expression driven by shifts in carbon/nitrogen sources, which were confirmed experimentally. Low AbcR1/2 levels in some defined media anticipated overexpression growth phenotypes linked to the silencing of specific mRNAs. As a proof of principle, we confirmed AbcR1/2-mediated downregulation of the l-amino acid AapQ permease. AbcR1/2 interactomes are well represented in rhizosphere-related S. meliloti transcriptomic signatures. Remarkably, a lack of AbcR1 specifically compromised the ability of S. meliloti to colonize the root rhizoplane. The AbcR1 regulon likely ranks the utilization of available substrates to optimize metabolism, thus conferring on S. meliloti an advantage for efficient rhizosphere/rhizoplane colonization. AbcR1 regulation is predicted to be conserved in related α-rhizobia, which opens unprecedented possibilities for engineering highly competitive biofertilizers. IMPORTANCE Nitrogen-fixing root nodule symbioses between rhizobia and legume plants provide more than half of the combined nitrogen incorporated annually into terrestrial ecosystems, rendering plant growth independent of environmentally unfriendly chemical fertilizers. The success of symbiosis depends primarily on the capacity of rhizobia to establish competitive populations in soil and rhizosphere environments. Here, we provide insights into the regulation and architecture of an extensive RNA posttranscriptional network that fine-tunes the metabolism of the alfalfa symbiont S. meliloti, thereby enhancing the ability of this beneficial bacterium to colonize nutrient-rich but extremely selective niches, such as the rhizosphere of its host plant. This pervasive RNA regulation of metabolism is a major adaptive mechanism, predicted to operate in diverse rhizobial species. Because RNA regulation relies on modifiable base-pairing interactions, our findings open unexplored avenues for engineering the legumes rhizobiome within sustainable agricultural practices. Sinorhizobium meliloti alphaproteobacteria noncoding RNA riboregulation Microbiology Marta Robledo verfasserin aut George C. diCenzo verfasserin aut Alessio Mengoni verfasserin aut Vicenta Millán verfasserin aut Alexandra Peregrina verfasserin aut Alejandro Uceta verfasserin aut José I. Jiménez-Zurdo verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 1 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:1 https://doi.org/10.1128/mbio.03576-21 kostenfrei https://doaj.org/article/abc6c4de55e74ccf9881d66363a54117 kostenfrei https://journals.asm.org/doi/10.1128/mbio.03576-21 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 1 |
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QR1-502 Pervasive RNA Regulation of Metabolism Enhances the Root Colonization Ability of Nitrogen-Fixing Symbiotic α-Rhizobia Sinorhizobium meliloti alphaproteobacteria noncoding RNA riboregulation |
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Pervasive RNA Regulation of Metabolism Enhances the Root Colonization Ability of Nitrogen-Fixing Symbiotic α-Rhizobia |
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pervasive rna regulation of metabolism enhances the root colonization ability of nitrogen-fixing symbiotic α-rhizobia |
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Pervasive RNA Regulation of Metabolism Enhances the Root Colonization Ability of Nitrogen-Fixing Symbiotic α-Rhizobia |
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ABSTRACT The rhizosphere and rhizoplane are nutrient-rich but selective environments for the root microbiome. Here, we deciphered a posttranscriptional network regulated by the homologous trans-small RNAs (sRNAs) AbcR1 and AbcR2, which rewire the metabolism of the nitrogen-fixing α-rhizobium Sinorhizobium meliloti during preinfection stages of symbiosis with its legume host alfalfa. The LysR-type regulator LsrB, which transduces the cell redox state, is indispensable for AbcR1 expression in actively dividing bacteria, whereas the stress-induced transcription of AbcR2 depends on the alternative σ factor RpoH1. MS2 affinity purification coupled with RNA sequencing unveiled exceptionally large and overlapping AbcR1/2 mRNA interactomes, jointly representing ⁓6% of the S. meliloti protein-coding genes. Most mRNAs encode transport/metabolic proteins whose translation is silenced by base pairing to two distinct anti-Shine Dalgarno motifs that function independently in both sRNAs. A metabolic model-aided analysis of the targetomes predicted changes in AbcR1/2 expression driven by shifts in carbon/nitrogen sources, which were confirmed experimentally. Low AbcR1/2 levels in some defined media anticipated overexpression growth phenotypes linked to the silencing of specific mRNAs. As a proof of principle, we confirmed AbcR1/2-mediated downregulation of the l-amino acid AapQ permease. AbcR1/2 interactomes are well represented in rhizosphere-related S. meliloti transcriptomic signatures. Remarkably, a lack of AbcR1 specifically compromised the ability of S. meliloti to colonize the root rhizoplane. The AbcR1 regulon likely ranks the utilization of available substrates to optimize metabolism, thus conferring on S. meliloti an advantage for efficient rhizosphere/rhizoplane colonization. AbcR1 regulation is predicted to be conserved in related α-rhizobia, which opens unprecedented possibilities for engineering highly competitive biofertilizers. IMPORTANCE Nitrogen-fixing root nodule symbioses between rhizobia and legume plants provide more than half of the combined nitrogen incorporated annually into terrestrial ecosystems, rendering plant growth independent of environmentally unfriendly chemical fertilizers. The success of symbiosis depends primarily on the capacity of rhizobia to establish competitive populations in soil and rhizosphere environments. Here, we provide insights into the regulation and architecture of an extensive RNA posttranscriptional network that fine-tunes the metabolism of the alfalfa symbiont S. meliloti, thereby enhancing the ability of this beneficial bacterium to colonize nutrient-rich but extremely selective niches, such as the rhizosphere of its host plant. This pervasive RNA regulation of metabolism is a major adaptive mechanism, predicted to operate in diverse rhizobial species. Because RNA regulation relies on modifiable base-pairing interactions, our findings open unexplored avenues for engineering the legumes rhizobiome within sustainable agricultural practices. |
abstractGer |
ABSTRACT The rhizosphere and rhizoplane are nutrient-rich but selective environments for the root microbiome. Here, we deciphered a posttranscriptional network regulated by the homologous trans-small RNAs (sRNAs) AbcR1 and AbcR2, which rewire the metabolism of the nitrogen-fixing α-rhizobium Sinorhizobium meliloti during preinfection stages of symbiosis with its legume host alfalfa. The LysR-type regulator LsrB, which transduces the cell redox state, is indispensable for AbcR1 expression in actively dividing bacteria, whereas the stress-induced transcription of AbcR2 depends on the alternative σ factor RpoH1. MS2 affinity purification coupled with RNA sequencing unveiled exceptionally large and overlapping AbcR1/2 mRNA interactomes, jointly representing ⁓6% of the S. meliloti protein-coding genes. Most mRNAs encode transport/metabolic proteins whose translation is silenced by base pairing to two distinct anti-Shine Dalgarno motifs that function independently in both sRNAs. A metabolic model-aided analysis of the targetomes predicted changes in AbcR1/2 expression driven by shifts in carbon/nitrogen sources, which were confirmed experimentally. Low AbcR1/2 levels in some defined media anticipated overexpression growth phenotypes linked to the silencing of specific mRNAs. As a proof of principle, we confirmed AbcR1/2-mediated downregulation of the l-amino acid AapQ permease. AbcR1/2 interactomes are well represented in rhizosphere-related S. meliloti transcriptomic signatures. Remarkably, a lack of AbcR1 specifically compromised the ability of S. meliloti to colonize the root rhizoplane. The AbcR1 regulon likely ranks the utilization of available substrates to optimize metabolism, thus conferring on S. meliloti an advantage for efficient rhizosphere/rhizoplane colonization. AbcR1 regulation is predicted to be conserved in related α-rhizobia, which opens unprecedented possibilities for engineering highly competitive biofertilizers. IMPORTANCE Nitrogen-fixing root nodule symbioses between rhizobia and legume plants provide more than half of the combined nitrogen incorporated annually into terrestrial ecosystems, rendering plant growth independent of environmentally unfriendly chemical fertilizers. The success of symbiosis depends primarily on the capacity of rhizobia to establish competitive populations in soil and rhizosphere environments. Here, we provide insights into the regulation and architecture of an extensive RNA posttranscriptional network that fine-tunes the metabolism of the alfalfa symbiont S. meliloti, thereby enhancing the ability of this beneficial bacterium to colonize nutrient-rich but extremely selective niches, such as the rhizosphere of its host plant. This pervasive RNA regulation of metabolism is a major adaptive mechanism, predicted to operate in diverse rhizobial species. Because RNA regulation relies on modifiable base-pairing interactions, our findings open unexplored avenues for engineering the legumes rhizobiome within sustainable agricultural practices. |
abstract_unstemmed |
ABSTRACT The rhizosphere and rhizoplane are nutrient-rich but selective environments for the root microbiome. Here, we deciphered a posttranscriptional network regulated by the homologous trans-small RNAs (sRNAs) AbcR1 and AbcR2, which rewire the metabolism of the nitrogen-fixing α-rhizobium Sinorhizobium meliloti during preinfection stages of symbiosis with its legume host alfalfa. The LysR-type regulator LsrB, which transduces the cell redox state, is indispensable for AbcR1 expression in actively dividing bacteria, whereas the stress-induced transcription of AbcR2 depends on the alternative σ factor RpoH1. MS2 affinity purification coupled with RNA sequencing unveiled exceptionally large and overlapping AbcR1/2 mRNA interactomes, jointly representing ⁓6% of the S. meliloti protein-coding genes. Most mRNAs encode transport/metabolic proteins whose translation is silenced by base pairing to two distinct anti-Shine Dalgarno motifs that function independently in both sRNAs. A metabolic model-aided analysis of the targetomes predicted changes in AbcR1/2 expression driven by shifts in carbon/nitrogen sources, which were confirmed experimentally. Low AbcR1/2 levels in some defined media anticipated overexpression growth phenotypes linked to the silencing of specific mRNAs. As a proof of principle, we confirmed AbcR1/2-mediated downregulation of the l-amino acid AapQ permease. AbcR1/2 interactomes are well represented in rhizosphere-related S. meliloti transcriptomic signatures. Remarkably, a lack of AbcR1 specifically compromised the ability of S. meliloti to colonize the root rhizoplane. The AbcR1 regulon likely ranks the utilization of available substrates to optimize metabolism, thus conferring on S. meliloti an advantage for efficient rhizosphere/rhizoplane colonization. AbcR1 regulation is predicted to be conserved in related α-rhizobia, which opens unprecedented possibilities for engineering highly competitive biofertilizers. IMPORTANCE Nitrogen-fixing root nodule symbioses between rhizobia and legume plants provide more than half of the combined nitrogen incorporated annually into terrestrial ecosystems, rendering plant growth independent of environmentally unfriendly chemical fertilizers. The success of symbiosis depends primarily on the capacity of rhizobia to establish competitive populations in soil and rhizosphere environments. Here, we provide insights into the regulation and architecture of an extensive RNA posttranscriptional network that fine-tunes the metabolism of the alfalfa symbiont S. meliloti, thereby enhancing the ability of this beneficial bacterium to colonize nutrient-rich but extremely selective niches, such as the rhizosphere of its host plant. This pervasive RNA regulation of metabolism is a major adaptive mechanism, predicted to operate in diverse rhizobial species. Because RNA regulation relies on modifiable base-pairing interactions, our findings open unexplored avenues for engineering the legumes rhizobiome within sustainable agricultural practices. |
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Pervasive RNA Regulation of Metabolism Enhances the Root Colonization Ability of Nitrogen-Fixing Symbiotic α-Rhizobia |
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