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Sinorhizobium meliloti Functions Required for Resistance to Antimicrobial NCR Peptides and Bacteroid Differentiation

Legumes of the Medicago genus have a symbiotic relationship with the bacterium Sinorhizobium meliloti and develop root nodules housing large numbers of intracellular symbionts. Members of the nodule-specific cysteine-rich peptide (NCR) family induce the endosymbionts into a terminal differentiated s...

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Autores principales: Nicoud, Quentin, Barrière, Quentin, Busset, Nicolas, Dendene, Sara, Travin, Dmitrii, Bourge, Mickaël, Le Bars, Romain, Boulogne, Claire, Lecroël, Marie, Jenei, Sándor, Kereszt, Atilla, Kondorosi, Eva, Biondi, Emanuele G., Timchenko, Tatiana, Alunni, Benoît, Mergaert, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8406287/
https://www.ncbi.nlm.nih.gov/pubmed/34311575
http://dx.doi.org/10.1128/mBio.00895-21
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author Nicoud, Quentin
Barrière, Quentin
Busset, Nicolas
Dendene, Sara
Travin, Dmitrii
Bourge, Mickaël
Le Bars, Romain
Boulogne, Claire
Lecroël, Marie
Jenei, Sándor
Kereszt, Atilla
Kondorosi, Eva
Biondi, Emanuele G.
Timchenko, Tatiana
Alunni, Benoît
Mergaert, Peter
author_facet Nicoud, Quentin
Barrière, Quentin
Busset, Nicolas
Dendene, Sara
Travin, Dmitrii
Bourge, Mickaël
Le Bars, Romain
Boulogne, Claire
Lecroël, Marie
Jenei, Sándor
Kereszt, Atilla
Kondorosi, Eva
Biondi, Emanuele G.
Timchenko, Tatiana
Alunni, Benoît
Mergaert, Peter
author_sort Nicoud, Quentin
collection PubMed
description Legumes of the Medicago genus have a symbiotic relationship with the bacterium Sinorhizobium meliloti and develop root nodules housing large numbers of intracellular symbionts. Members of the nodule-specific cysteine-rich peptide (NCR) family induce the endosymbionts into a terminal differentiated state. Individual cationic NCRs are antimicrobial peptides that have the capacity to kill the symbiont, but the nodule cell environment prevents killing. Moreover, the bacterial broad-specificity peptide uptake transporter BacA and exopolysaccharides contribute to protect the endosymbionts against the toxic activity of NCRs. Here, we show that other S. meliloti functions participate in the protection of the endosymbionts; these include an additional broad-specificity peptide uptake transporter encoded by the yejABEF genes and lipopolysaccharide modifications mediated by lpsB and lpxXL, as well as rpoH1, encoding a stress sigma factor. Strains with mutations in these genes show a strain-specific increased sensitivity profile against a panel of NCRs and form nodules in which bacteroid differentiation is affected. The lpsB mutant nodule bacteria do not differentiate, the lpxXL and rpoH1 mutants form some seemingly fully differentiated bacteroids, although most of the nodule bacteria are undifferentiated, while the yejABEF mutants form hypertrophied but nitrogen-fixing bacteroids. The nodule bacteria of all the mutants have a strongly enhanced membrane permeability, which is dependent on the transport of NCRs to the endosymbionts. Our results suggest that S. meliloti relies on a suite of functions, including peptide transporters, the bacterial envelope structures, and stress response regulators, to resist the aggressive assault of NCR peptides in the nodule cells.
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spelling pubmed-84062872021-09-09 Sinorhizobium meliloti Functions Required for Resistance to Antimicrobial NCR Peptides and Bacteroid Differentiation Nicoud, Quentin Barrière, Quentin Busset, Nicolas Dendene, Sara Travin, Dmitrii Bourge, Mickaël Le Bars, Romain Boulogne, Claire Lecroël, Marie Jenei, Sándor Kereszt, Atilla Kondorosi, Eva Biondi, Emanuele G. Timchenko, Tatiana Alunni, Benoît Mergaert, Peter mBio Research Article Legumes of the Medicago genus have a symbiotic relationship with the bacterium Sinorhizobium meliloti and develop root nodules housing large numbers of intracellular symbionts. Members of the nodule-specific cysteine-rich peptide (NCR) family induce the endosymbionts into a terminal differentiated state. Individual cationic NCRs are antimicrobial peptides that have the capacity to kill the symbiont, but the nodule cell environment prevents killing. Moreover, the bacterial broad-specificity peptide uptake transporter BacA and exopolysaccharides contribute to protect the endosymbionts against the toxic activity of NCRs. Here, we show that other S. meliloti functions participate in the protection of the endosymbionts; these include an additional broad-specificity peptide uptake transporter encoded by the yejABEF genes and lipopolysaccharide modifications mediated by lpsB and lpxXL, as well as rpoH1, encoding a stress sigma factor. Strains with mutations in these genes show a strain-specific increased sensitivity profile against a panel of NCRs and form nodules in which bacteroid differentiation is affected. The lpsB mutant nodule bacteria do not differentiate, the lpxXL and rpoH1 mutants form some seemingly fully differentiated bacteroids, although most of the nodule bacteria are undifferentiated, while the yejABEF mutants form hypertrophied but nitrogen-fixing bacteroids. The nodule bacteria of all the mutants have a strongly enhanced membrane permeability, which is dependent on the transport of NCRs to the endosymbionts. Our results suggest that S. meliloti relies on a suite of functions, including peptide transporters, the bacterial envelope structures, and stress response regulators, to resist the aggressive assault of NCR peptides in the nodule cells. American Society for Microbiology 2021-07-27 /pmc/articles/PMC8406287/ /pubmed/34311575 http://dx.doi.org/10.1128/mBio.00895-21 Text en Copyright © 2021 Nicoud 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
Nicoud, Quentin
Barrière, Quentin
Busset, Nicolas
Dendene, Sara
Travin, Dmitrii
Bourge, Mickaël
Le Bars, Romain
Boulogne, Claire
Lecroël, Marie
Jenei, Sándor
Kereszt, Atilla
Kondorosi, Eva
Biondi, Emanuele G.
Timchenko, Tatiana
Alunni, Benoît
Mergaert, Peter
Sinorhizobium meliloti Functions Required for Resistance to Antimicrobial NCR Peptides and Bacteroid Differentiation
title Sinorhizobium meliloti Functions Required for Resistance to Antimicrobial NCR Peptides and Bacteroid Differentiation
title_full Sinorhizobium meliloti Functions Required for Resistance to Antimicrobial NCR Peptides and Bacteroid Differentiation
title_fullStr Sinorhizobium meliloti Functions Required for Resistance to Antimicrobial NCR Peptides and Bacteroid Differentiation
title_full_unstemmed Sinorhizobium meliloti Functions Required for Resistance to Antimicrobial NCR Peptides and Bacteroid Differentiation
title_short Sinorhizobium meliloti Functions Required for Resistance to Antimicrobial NCR Peptides and Bacteroid Differentiation
title_sort sinorhizobium meliloti functions required for resistance to antimicrobial ncr peptides and bacteroid differentiation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8406287/
https://www.ncbi.nlm.nih.gov/pubmed/34311575
http://dx.doi.org/10.1128/mBio.00895-21
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