A Small Regulatory RNA Controls Cell Wall Biosynthesis and Antibiotic Resistance

ABSTRACT Small regulatory RNAs play an important role in the adaptation to changing conditions. Here, we describe a differentially expressed small regulatory RNA (sRNA) that affects various cellular processes in the plant pathogen Agrobacterium tumefaciens. Using a combination of bioinformatic predi...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Jessica Borgmann, Sina Schäkermann, Julia Elisabeth Bandow, Franz Narberhaus
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2018
Materias:
Acceso en línea:https://doaj.org/article/c3a881bc08ea427a8b73de6902df30b5
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:c3a881bc08ea427a8b73de6902df30b5
record_format dspace
spelling oai:doaj.org-article:c3a881bc08ea427a8b73de6902df30b52021-11-15T15:52:19ZA Small Regulatory RNA Controls Cell Wall Biosynthesis and Antibiotic Resistance10.1128/mBio.02100-182150-7511https://doaj.org/article/c3a881bc08ea427a8b73de6902df30b52018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02100-18https://doaj.org/toc/2150-7511ABSTRACT Small regulatory RNAs play an important role in the adaptation to changing conditions. Here, we describe a differentially expressed small regulatory RNA (sRNA) that affects various cellular processes in the plant pathogen Agrobacterium tumefaciens. Using a combination of bioinformatic predictions and comparative proteomics, we identified nine targets, most of which are positively regulated by the sRNA. According to these targets, we named the sRNA PmaR for peptidoglycan biosynthesis, motility, and ampicillin resistance regulator. Agrobacterium spp. are long known to be naturally resistant to high ampicillin concentrations, and we can now explain this phenotype by the positive PmaR-mediated regulation of the beta-lactamase gene ampC. Structure probing revealed a spoon-like structure of the sRNA, with a single-stranded loop that is engaged in target interaction in vivo and in vitro. Several riboregulators have been implicated in antibiotic resistance mechanisms, such as uptake and efflux transporters, but PmaR represents the first example of an sRNA that directly controls the expression of an antibiotic resistance gene. IMPORTANCE The alphaproteobacterium Agrobacterium tumefaciens is able to infect various eudicots causing crown gall tumor formation. Based on its unique ability of interkingdom gene transfer, Agrobacterium serves as a crucial biotechnological tool for genetic manipulation of plant cells. The presence of hundreds of putative sRNAs in this organism suggests a considerable impact of riboregulation on A. tumefaciens physiology. Here, we characterized the biological function of the sRNA PmaR that controls various processes crucial for growth, motility, and virulence. Among the genes directly targeted by PmaR is ampC coding for a beta-lactamase that confers ampicillin resistance, suggesting that the sRNA is crucial for fitness in the competitive microbial composition of the rhizosphere.Jessica BorgmannSina SchäkermannJulia Elisabeth BandowFranz NarberhausAmerican Society for Microbiologyarticleantibiotic resistancegene regulationplant-microbe interactionposttranscriptional controlregulatory RNAMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution DOAJ
collection DOAJ
language EN
topic antibiotic resistance
gene regulation
plant-microbe interaction
posttranscriptional control
regulatory RNA
Microbiology
QR1-502
spellingShingle antibiotic resistance
gene regulation
plant-microbe interaction
posttranscriptional control
regulatory RNA
Microbiology
QR1-502
Jessica Borgmann
Sina Schäkermann
Julia Elisabeth Bandow
Franz Narberhaus
A Small Regulatory RNA Controls Cell Wall Biosynthesis and Antibiotic Resistance
description ABSTRACT Small regulatory RNAs play an important role in the adaptation to changing conditions. Here, we describe a differentially expressed small regulatory RNA (sRNA) that affects various cellular processes in the plant pathogen Agrobacterium tumefaciens. Using a combination of bioinformatic predictions and comparative proteomics, we identified nine targets, most of which are positively regulated by the sRNA. According to these targets, we named the sRNA PmaR for peptidoglycan biosynthesis, motility, and ampicillin resistance regulator. Agrobacterium spp. are long known to be naturally resistant to high ampicillin concentrations, and we can now explain this phenotype by the positive PmaR-mediated regulation of the beta-lactamase gene ampC. Structure probing revealed a spoon-like structure of the sRNA, with a single-stranded loop that is engaged in target interaction in vivo and in vitro. Several riboregulators have been implicated in antibiotic resistance mechanisms, such as uptake and efflux transporters, but PmaR represents the first example of an sRNA that directly controls the expression of an antibiotic resistance gene. IMPORTANCE The alphaproteobacterium Agrobacterium tumefaciens is able to infect various eudicots causing crown gall tumor formation. Based on its unique ability of interkingdom gene transfer, Agrobacterium serves as a crucial biotechnological tool for genetic manipulation of plant cells. The presence of hundreds of putative sRNAs in this organism suggests a considerable impact of riboregulation on A. tumefaciens physiology. Here, we characterized the biological function of the sRNA PmaR that controls various processes crucial for growth, motility, and virulence. Among the genes directly targeted by PmaR is ampC coding for a beta-lactamase that confers ampicillin resistance, suggesting that the sRNA is crucial for fitness in the competitive microbial composition of the rhizosphere.
format article
author Jessica Borgmann
Sina Schäkermann
Julia Elisabeth Bandow
Franz Narberhaus
author_facet Jessica Borgmann
Sina Schäkermann
Julia Elisabeth Bandow
Franz Narberhaus
author_sort Jessica Borgmann
title A Small Regulatory RNA Controls Cell Wall Biosynthesis and Antibiotic Resistance
title_short A Small Regulatory RNA Controls Cell Wall Biosynthesis and Antibiotic Resistance
title_full A Small Regulatory RNA Controls Cell Wall Biosynthesis and Antibiotic Resistance
title_fullStr A Small Regulatory RNA Controls Cell Wall Biosynthesis and Antibiotic Resistance
title_full_unstemmed A Small Regulatory RNA Controls Cell Wall Biosynthesis and Antibiotic Resistance
title_sort small regulatory rna controls cell wall biosynthesis and antibiotic resistance
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/c3a881bc08ea427a8b73de6902df30b5
work_keys_str_mv AT jessicaborgmann asmallregulatoryrnacontrolscellwallbiosynthesisandantibioticresistance
AT sinaschakermann asmallregulatoryrnacontrolscellwallbiosynthesisandantibioticresistance
AT juliaelisabethbandow asmallregulatoryrnacontrolscellwallbiosynthesisandantibioticresistance
AT franznarberhaus asmallregulatoryrnacontrolscellwallbiosynthesisandantibioticresistance
AT jessicaborgmann smallregulatoryrnacontrolscellwallbiosynthesisandantibioticresistance
AT sinaschakermann smallregulatoryrnacontrolscellwallbiosynthesisandantibioticresistance
AT juliaelisabethbandow smallregulatoryrnacontrolscellwallbiosynthesisandantibioticresistance
AT franznarberhaus smallregulatoryrnacontrolscellwallbiosynthesisandantibioticresistance
_version_ 1718427302408224768