Characterization of a Regulatory Network of Peptide Antibiotic Detoxification Modules in Lactobacillus casei BL23

Abstract

ABSTRACT Two-component systems (TCS) are major signal transduction pathways that allow bacteria to detect and respond to environmental and intracellular changes. A group of TCS has been shown to be involved in the response against antimicrobial peptides (AMPs). These TCS are characterized by the possession of intramembrane-sensing histidine kinases, and they are usually associated with ABC transporters of the peptide-7 exporter family (Pep7E). Lactobacillus casei BL23 encodes two TCS belonging to this group (TCS09 and TCS12) that are located next to two ABC transporters (ABC09 and ABC12), as well as a third Pep7E ABC transporter not genetically associated with any TCS (orphan ABC). This study addressed the involvement of modules TCS09/ABC09 and TCS12/ABC12 in AMP resistance. Results showed that both systems contribute to L. casei resistance to AMPs, and that each TCS constitutes a functional unit with its corresponding ABC transporter. Analysis of transcriptional levels showed that module 09 is required for the induction of ABC09 expression in response to nisin. In contrast, module 12 controls a wider regulon that encompasses the orphan ABC, the dlt operon ( d -alanylation of teichoid acids), and the mprF gene ( l -lysinylation of phospholipids), thereby controlling properties of the cell envelope. Furthermore, the characterization of a dltA mutant showed that Dlt plays a major role in AMP resistance in L. casei . This is the first report on the regulation of the response of L. casei to AMPs, giving insight into its ability to adapt to the challenging environments that it encounters as a probiotic microorganism.

Autoren

Ainhoa Revilla-Guarinos
Susanne Gebhard
Cristina Alcántara
Anna Staroń
Thorsten Mascher
Manuel Zúñiga

DOI

10.1128/aem.00178-13

eISSN

1098-5336

ISSN

0099-2240

Ausgabe der Veröffentlichung

10

Zeitschrift

Applied and Environmental Microbiology

Sprache

en

Paginierung

3160 - 3170

Datum der Veröffentlichung

2013

Status

Published

Herausgeber

American Society for Microbiology

Herausgeber URL

http://dx.doi.org/10.1128/aem.00178-13

Datum der Datenerfassung

2022

Titel

Characterization of a Regulatory Network of Peptide Antibiotic Detoxification Modules in Lactobacillus casei BL23

Ausgabe der Zeitschrift

79

Datenquelle: Crossref

Abstract

Two-component systems (TCS) are major signal transduction pathways that allow bacteria to detect and respond to environmental and intracellular changes. A group of TCS has been shown to be involved in the response against antimicrobial peptides (AMPs). These TCS are characterized by the possession of intramembrane-sensing histidine kinases, and they are usually associated with ABC transporters of the peptide-7 exporter family (Pep7E). Lactobacillus casei BL23 encodes two TCS belonging to this group (TCS09 and TCS12) that are located next to two ABC transporters (ABC09 and ABC12), as well as a third Pep7E ABC transporter not genetically associated with any TCS (orphan ABC). This study addressed the involvement of modules TCS09/ABC09 and TCS12/ABC12 in AMP resistance. Results showed that both systems contribute to L. casei resistance to AMPs, and that each TCS constitutes a functional unit with its corresponding ABC transporter. Analysis of transcriptional levels showed that module 09 is required for the induction of ABC09 expression in response to nisin. In contrast, module 12 controls a wider regulon that encompasses the orphan ABC, the dlt operon (d-alanylation of teichoid acids), and the mprF gene (l-lysinylation of phospholipids), thereby controlling properties of the cell envelope. Furthermore, the characterization of a dltA mutant showed that Dlt plays a major role in AMP resistance in L. casei. This is the first report on the regulation of the response of L. casei to AMPs, giving insight into its ability to adapt to the challenging environments that it encounters as a probiotic microorganism.

Addresses

Departamento de Biotecnología, Consejo Superior de Investigaciones Científicas, Paterna, Valencia, Spain.

Autoren

Ainhoa Revilla-Guarinos
Susanne Gebhard
Cristina Alcántara
Anna Staron
Thorsten Mascher
Manuel Zúñiga

DOI

10.1128/aem.00178-13

eISSN

1098-5336

Externe Identifier

PubMed Identifier: 23455349
PubMed Central ID: PMC3685250

Open access

false

ISSN

0099-2240

Ausgabe der Veröffentlichung

10

Zeitschrift

Applied and environmental microbiology

Schlüsselwörter

Escherichia coli
Bacitracin
Nisin
Antimicrobial Cationic Peptides
Bacterial Proteins
Microbial Sensitivity Tests
Adaptation, Physiological
Drug Resistance, Bacterial
Species Specificity
Transcription, Genetic
Gene Expression Regulation, Bacterial
Binding Sites
Consensus Sequence
Genome, Bacterial
Operon
Regulon
Promoter Regions, Genetic
Genetic Pleiotropy
Lacticaseibacillus casei

Sprache

eng

Medium

Print-Electronic

Online publication date

2013

Paginierung

3160 - 3170

Datum der Veröffentlichung

2013

Status

Published

Datum der Datenerfassung

2013

Titel

Characterization of a regulatory network of peptide antibiotic detoxification modules in Lactobacillus casei BL23.

Sub types

Research Support, Non-U.S. Gov't
research-article
Journal Article

Ausgabe der Zeitschrift

79

Files

https://aem.asm.org/content/aem/79/10/3160.full.pdf https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23455349/pdf/?tool=EBI https://europepmc.org/articles/PMC3685250?pdf=render

Datenquelle: Europe PubMed Central

Abstract

Two-component systems (TCS) are major signal transduction pathways that allow bacteria to detect and respond to environmental and intracellular changes. A group of TCS has been shown to be involved in the response against antimicrobial peptides (AMPs). These TCS are characterized by the possession of intramembrane-sensing histidine kinases, and they are usually associated with ABC transporters of the peptide-7 exporter family (Pep7E). Lactobacillus casei BL23 encodes two TCS belonging to this group (TCS09 and TCS12) that are located next to two ABC transporters (ABC09 and ABC12), as well as a third Pep7E ABC transporter not genetically associated with any TCS (orphan ABC). This study addressed the involvement of modules TCS09/ABC09 and TCS12/ABC12 in AMP resistance. Results showed that both systems contribute to L. casei resistance to AMPs, and that each TCS constitutes a functional unit with its corresponding ABC transporter. Analysis of transcriptional levels showed that module 09 is required for the induction of ABC09 expression in response to nisin. In contrast, module 12 controls a wider regulon that encompasses the orphan ABC, the dlt operon (d-alanylation of teichoid acids), and the mprF gene (l-lysinylation of phospholipids), thereby controlling properties of the cell envelope. Furthermore, the characterization of a dltA mutant showed that Dlt plays a major role in AMP resistance in L. casei. This is the first report on the regulation of the response of L. casei to AMPs, giving insight into its ability to adapt to the challenging environments that it encounters as a probiotic microorganism.

Autoren

Ainhoa Revilla-Guarinos
Susanne Gebhard
Cristina Alcántara
Anna Staron
Thorsten Mascher
Manuel Zúñiga

Autoren-URL

https://www.ncbi.nlm.nih.gov/pubmed/23455349

DOI

10.1128/AEM.00178-13

eISSN

1098-5336

Externe Identifier

PubMed Central ID: PMC3685250

Ausgabe der Veröffentlichung

10

Zeitschrift

Appl Environ Microbiol

Schlüsselwörter

Adaptation, Physiological
Antimicrobial Cationic Peptides
Bacitracin
Bacterial Proteins
Binding Sites
Consensus Sequence
Drug Resistance, Bacterial
Escherichia coli
Gene Expression Regulation, Bacterial
Genetic Pleiotropy
Genome, Bacterial
Lacticaseibacillus casei
Microbial Sensitivity Tests
Nisin
Operon
Promoter Regions, Genetic
Regulon
Species Specificity
Transcription, Genetic

Sprache

eng

Country

United States

Paginierung

3160 - 3170

PII

AEM.00178-13

Datum der Veröffentlichung

2013

Status

Published

Datum, an dem der Datensatz öffentlich gemacht wurde

2013

Titel

Characterization of a regulatory network of peptide antibiotic detoxification modules in Lactobacillus casei BL23.

Sub types

Journal Article
Research Support, Non-U.S. Gov't

Ausgabe der Zeitschrift

79

Datenquelle: PubMed

Characterization of a Regulatory Network of Peptide Antibiotic Detoxification Modules in Lactobacillus casei BL23

Files

Werkzeuge