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Activation of the Two-Component System LisRK Promotes Cell Adhesion and High Ampicillin Tolerance in Listeria monocytogenes

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Activation of the Two-Component System LisRK Promotes Cell Adhesion and High Ampicillin Tolerance in Listeria monocytogenes. / Aslan, Hüsnü; Petersen, Maiken Engelbrecht; De Berardinis, Alberto et al.

In: Frontiers in Microbiology, Vol. 12, 618174, 01.2021.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaperJournal articleResearchpeer-review

Harvard

Aslan, H, Petersen, ME, De Berardinis, A, Zacho Brunhede, M, Khan, N, Vergara, A, Kallipolitis, B & Meyer, RL 2021, 'Activation of the Two-Component System LisRK Promotes Cell Adhesion and High Ampicillin Tolerance in Listeria monocytogenes', Frontiers in Microbiology, vol. 12, 618174. https://doi.org/10.3389/fmicb.2021.618174

APA

Aslan, H., Petersen, M. E., De Berardinis, A., Zacho Brunhede, M., Khan, N., Vergara, A., Kallipolitis, B., & Meyer, R. L. (2021). Activation of the Two-Component System LisRK Promotes Cell Adhesion and High Ampicillin Tolerance in Listeria monocytogenes. Frontiers in Microbiology, 12, [618174]. https://doi.org/10.3389/fmicb.2021.618174

CBE

Aslan H, Petersen ME, De Berardinis A, Zacho Brunhede M, Khan N, Vergara A, Kallipolitis B, Meyer RL. 2021. Activation of the Two-Component System LisRK Promotes Cell Adhesion and High Ampicillin Tolerance in Listeria monocytogenes. Frontiers in Microbiology. 12:Article 618174. https://doi.org/10.3389/fmicb.2021.618174

MLA

Vancouver

Aslan H, Petersen ME, De Berardinis A, Zacho Brunhede M, Khan N, Vergara A et al. Activation of the Two-Component System LisRK Promotes Cell Adhesion and High Ampicillin Tolerance in Listeria monocytogenes. Frontiers in Microbiology. 2021 Jan;12. 618174. https://doi.org/10.3389/fmicb.2021.618174

Author

Bibtex

@article{9d688fce91874795aaf0472f2a2c53be,
title = "Activation of the Two-Component System LisRK Promotes Cell Adhesion and High Ampicillin Tolerance in Listeria monocytogenes",
abstract = "Listeria monocytogenes is a foodborne pathogen which can survive in harsh environmental conditions. It responds to external stimuli through an array of two-component systems (TCS) that sense external cues. Several TCS, including LisRK, have been linked to Listeria{\textquoteright}s ability to grow at slightly elevated antibiotic levels. The aim of this study was to determine if the TCS LisRK is also involved in acquiring the high antibiotic tolerance that is characteristic of persister cells. LisRK activates a response that leads to remodeling of the cell envelope, and we therefore hypothesized that activation of LisRK could also increase in the cells{\textquoteright} adhesiveness and initiate the first step in biofilm formation. We used a ΔlisR mutant to study antibiotic tolerance in the presence and absence of LisRK, and a GFP reporter strain to visualize the activation of LisRK in L. monocytogenes LO28 at a single-cell level. LisRK was activated in most cells in stationary phase cultures. Antimicrobial susceptibility tests showed that LisRK was required for the generation of ampicillin tolerance under these conditions. The wildtype strain tolerated exposure to ampicillin at 1,000 × inhibitory levels for 24 h, and the fraction of surviving cells was 20,000-fold higher in the wildtype strain compared to the ΔlisR mutant. The same protection was not offered to other antibiotics (vancomycin, gentamicin, tetracycline), and the mechanism for antibiotic tolerance is thus highly specific. Furthermore, quantification of bacterial attachment rates and attachment force also revealed that the absence of a functional LisRK rendered the cells less adhesive. Hence, LisRK TCS promotes multiple protective mechanisms simultaneously.",
keywords = "adhesion, antibiotic tolerance, LisRK, listeria monocytogenes, nanomechanics, persister, tcs, two-component systems",
author = "H{\"u}sn{\"u} Aslan and Petersen, {Maiken Engelbrecht} and {De Berardinis}, Alberto and {Zacho Brunhede}, Maja and Nasar Khan and Alberto Vergara and Birgitte Kallipolitis and Meyer, {Rikke Louise}",
year = "2021",
month = jan,
doi = "10.3389/fmicb.2021.618174",
language = "English",
volume = "12",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers Media S.A",

}

RIS

TY - JOUR

T1 - Activation of the Two-Component System LisRK Promotes Cell Adhesion and High Ampicillin Tolerance in Listeria monocytogenes

AU - Aslan, Hüsnü

AU - Petersen, Maiken Engelbrecht

AU - De Berardinis, Alberto

AU - Zacho Brunhede, Maja

AU - Khan, Nasar

AU - Vergara, Alberto

AU - Kallipolitis, Birgitte

AU - Meyer, Rikke Louise

PY - 2021/1

Y1 - 2021/1

N2 - Listeria monocytogenes is a foodborne pathogen which can survive in harsh environmental conditions. It responds to external stimuli through an array of two-component systems (TCS) that sense external cues. Several TCS, including LisRK, have been linked to Listeria’s ability to grow at slightly elevated antibiotic levels. The aim of this study was to determine if the TCS LisRK is also involved in acquiring the high antibiotic tolerance that is characteristic of persister cells. LisRK activates a response that leads to remodeling of the cell envelope, and we therefore hypothesized that activation of LisRK could also increase in the cells’ adhesiveness and initiate the first step in biofilm formation. We used a ΔlisR mutant to study antibiotic tolerance in the presence and absence of LisRK, and a GFP reporter strain to visualize the activation of LisRK in L. monocytogenes LO28 at a single-cell level. LisRK was activated in most cells in stationary phase cultures. Antimicrobial susceptibility tests showed that LisRK was required for the generation of ampicillin tolerance under these conditions. The wildtype strain tolerated exposure to ampicillin at 1,000 × inhibitory levels for 24 h, and the fraction of surviving cells was 20,000-fold higher in the wildtype strain compared to the ΔlisR mutant. The same protection was not offered to other antibiotics (vancomycin, gentamicin, tetracycline), and the mechanism for antibiotic tolerance is thus highly specific. Furthermore, quantification of bacterial attachment rates and attachment force also revealed that the absence of a functional LisRK rendered the cells less adhesive. Hence, LisRK TCS promotes multiple protective mechanisms simultaneously.

AB - Listeria monocytogenes is a foodborne pathogen which can survive in harsh environmental conditions. It responds to external stimuli through an array of two-component systems (TCS) that sense external cues. Several TCS, including LisRK, have been linked to Listeria’s ability to grow at slightly elevated antibiotic levels. The aim of this study was to determine if the TCS LisRK is also involved in acquiring the high antibiotic tolerance that is characteristic of persister cells. LisRK activates a response that leads to remodeling of the cell envelope, and we therefore hypothesized that activation of LisRK could also increase in the cells’ adhesiveness and initiate the first step in biofilm formation. We used a ΔlisR mutant to study antibiotic tolerance in the presence and absence of LisRK, and a GFP reporter strain to visualize the activation of LisRK in L. monocytogenes LO28 at a single-cell level. LisRK was activated in most cells in stationary phase cultures. Antimicrobial susceptibility tests showed that LisRK was required for the generation of ampicillin tolerance under these conditions. The wildtype strain tolerated exposure to ampicillin at 1,000 × inhibitory levels for 24 h, and the fraction of surviving cells was 20,000-fold higher in the wildtype strain compared to the ΔlisR mutant. The same protection was not offered to other antibiotics (vancomycin, gentamicin, tetracycline), and the mechanism for antibiotic tolerance is thus highly specific. Furthermore, quantification of bacterial attachment rates and attachment force also revealed that the absence of a functional LisRK rendered the cells less adhesive. Hence, LisRK TCS promotes multiple protective mechanisms simultaneously.

KW - adhesion

KW - antibiotic tolerance

KW - LisRK

KW - listeria monocytogenes

KW - nanomechanics

KW - persister

KW - tcs

KW - two-component systems

UR - http://www.scopus.com/inward/record.url?scp=85100974397&partnerID=8YFLogxK

U2 - 10.3389/fmicb.2021.618174

DO - 10.3389/fmicb.2021.618174

M3 - Journal article

C2 - 33584621

AN - SCOPUS:85100974397

VL - 12

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

M1 - 618174

ER -