Cross-Phosphorylation between AgrC Histidine Kinase and the Noncognate Response Regulator Lmo1172 in <i>Listeria monocytogenes</i> under Benzalkonium Chloride Stress

Benzalkonium chloride (BC) is widely used for disinfection in the food industry. However, <i>Listeria monocytogenes</i> strains with resistance to BC have been reported recently. In <i>L. monocytogenes</i>, the Agr communication system consists of a membrane-bound peptidase A...

Full description

Bibliographic Details
Main Authors: Tao Yu, Xiaojie Jiang, Xiaobo Xu, Ping Xu, Shuxing Qiu, Junlei Yin, David P. Hamilton, Xiaobing Jiang
Format: Article
Language:English
Published: MDPI AG 2024-02-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/12/2/392
_version_ 1797297444920229888
author Tao Yu
Xiaojie Jiang
Xiaobo Xu
Ping Xu
Shuxing Qiu
Junlei Yin
David P. Hamilton
Xiaobing Jiang
author_facet Tao Yu
Xiaojie Jiang
Xiaobo Xu
Ping Xu
Shuxing Qiu
Junlei Yin
David P. Hamilton
Xiaobing Jiang
author_sort Tao Yu
collection DOAJ
description Benzalkonium chloride (BC) is widely used for disinfection in the food industry. However, <i>Listeria monocytogenes</i> strains with resistance to BC have been reported recently. In <i>L. monocytogenes</i>, the Agr communication system consists of a membrane-bound peptidase AgrB, a precursor peptide AgrD, a histidine kinase (HK) AgrC, and a response regulator (RR) AgrA. Our previous study showed that the <i>agr</i> genes are significantly upregulated by BC adaptation. This study aimed to investigate the role of the Agr system in BC resistance in <i>L. monocytogenes</i>. Our results showed that the Agr system was involved in BC resistance. However, a direct interaction between BC and AgrC was not observed, nor between BC and AgrA. These results indicated that BC could induce the Agr system via an indirect action. Both AgrBD and AgrC were required for growth under BC stress. Nevertheless, when exposed to BC, the gene deletion mutant ∆<i>agrA</i> strain exhibited better growth performance than its parental strain. The RR Lmo1172 played a role in BC resistance in the ∆<i>agrA</i> strain, suggesting that Lmo1172 may be an alternative to AgrA in the phosphotransfer pathway. Phosphorylation of Lmo1172 by AgrC was observed in vitro. The cognate HK Lmo1173 of Lmo1172 was not involved in BC stress, regardless of whether it was as the wild-type or the ∆<i>agrA</i> mutant strain. Our evidence suggests that the HK AgrC cross-phosphorylates its noncognate RR Lmo1172 to cope with BC stress when the cognate RR AgrA is absent. In vivo, further studies will be required to detect phosphotransfer of AgrC/AgrA and AgrC/Lmo1172.
first_indexed 2024-03-07T22:21:20Z
format Article
id doaj.art-ed9d17cc192442b0b20a42de0a4b061d
institution Directory Open Access Journal
issn 2076-2607
language English
last_indexed 2024-03-07T22:21:20Z
publishDate 2024-02-01
publisher MDPI AG
record_format Article
series Microorganisms
spelling doaj.art-ed9d17cc192442b0b20a42de0a4b061d2024-02-23T15:28:24ZengMDPI AGMicroorganisms2076-26072024-02-0112239210.3390/microorganisms12020392Cross-Phosphorylation between AgrC Histidine Kinase and the Noncognate Response Regulator Lmo1172 in <i>Listeria monocytogenes</i> under Benzalkonium Chloride StressTao Yu0Xiaojie Jiang1Xiaobo Xu2Ping Xu3Shuxing Qiu4Junlei Yin5David P. Hamilton6Xiaobing Jiang7School of Biological Engineering, Xinxiang University, Xinxiang 453003, ChinaSchool of Biological Engineering, Xinxiang University, Xinxiang 453003, ChinaSchool of Biological Engineering, Xinxiang University, Xinxiang 453003, ChinaSchool of Biological Engineering, Xinxiang University, Xinxiang 453003, ChinaKey Laboratory of Biomedicine and Health Risk Warning of Xinxiang City, Medical College, Xinxiang University, Xinxiang 453003, ChinaKey Laboratory of Biomedicine and Health Risk Warning of Xinxiang City, Medical College, Xinxiang University, Xinxiang 453003, ChinaAustralian Rivers Institute, Griffith University, Brisbane, QLD 4111, AustraliaHenan Engineering Laboratory for Bioconversion Technology of Functional Microbes, College of Life Sciences, Henan Normal University, Xinxiang 453007, ChinaBenzalkonium chloride (BC) is widely used for disinfection in the food industry. However, <i>Listeria monocytogenes</i> strains with resistance to BC have been reported recently. In <i>L. monocytogenes</i>, the Agr communication system consists of a membrane-bound peptidase AgrB, a precursor peptide AgrD, a histidine kinase (HK) AgrC, and a response regulator (RR) AgrA. Our previous study showed that the <i>agr</i> genes are significantly upregulated by BC adaptation. This study aimed to investigate the role of the Agr system in BC resistance in <i>L. monocytogenes</i>. Our results showed that the Agr system was involved in BC resistance. However, a direct interaction between BC and AgrC was not observed, nor between BC and AgrA. These results indicated that BC could induce the Agr system via an indirect action. Both AgrBD and AgrC were required for growth under BC stress. Nevertheless, when exposed to BC, the gene deletion mutant ∆<i>agrA</i> strain exhibited better growth performance than its parental strain. The RR Lmo1172 played a role in BC resistance in the ∆<i>agrA</i> strain, suggesting that Lmo1172 may be an alternative to AgrA in the phosphotransfer pathway. Phosphorylation of Lmo1172 by AgrC was observed in vitro. The cognate HK Lmo1173 of Lmo1172 was not involved in BC stress, regardless of whether it was as the wild-type or the ∆<i>agrA</i> mutant strain. Our evidence suggests that the HK AgrC cross-phosphorylates its noncognate RR Lmo1172 to cope with BC stress when the cognate RR AgrA is absent. In vivo, further studies will be required to detect phosphotransfer of AgrC/AgrA and AgrC/Lmo1172.https://www.mdpi.com/2076-2607/12/2/392<i>Listeria monocytogenes</i>AgrCLmo1172crosstalkbenzalkonium chloride
spellingShingle Tao Yu
Xiaojie Jiang
Xiaobo Xu
Ping Xu
Shuxing Qiu
Junlei Yin
David P. Hamilton
Xiaobing Jiang
Cross-Phosphorylation between AgrC Histidine Kinase and the Noncognate Response Regulator Lmo1172 in <i>Listeria monocytogenes</i> under Benzalkonium Chloride Stress
Microorganisms
<i>Listeria monocytogenes</i>
AgrC
Lmo1172
crosstalk
benzalkonium chloride
title Cross-Phosphorylation between AgrC Histidine Kinase and the Noncognate Response Regulator Lmo1172 in <i>Listeria monocytogenes</i> under Benzalkonium Chloride Stress
title_full Cross-Phosphorylation between AgrC Histidine Kinase and the Noncognate Response Regulator Lmo1172 in <i>Listeria monocytogenes</i> under Benzalkonium Chloride Stress
title_fullStr Cross-Phosphorylation between AgrC Histidine Kinase and the Noncognate Response Regulator Lmo1172 in <i>Listeria monocytogenes</i> under Benzalkonium Chloride Stress
title_full_unstemmed Cross-Phosphorylation between AgrC Histidine Kinase and the Noncognate Response Regulator Lmo1172 in <i>Listeria monocytogenes</i> under Benzalkonium Chloride Stress
title_short Cross-Phosphorylation between AgrC Histidine Kinase and the Noncognate Response Regulator Lmo1172 in <i>Listeria monocytogenes</i> under Benzalkonium Chloride Stress
title_sort cross phosphorylation between agrc histidine kinase and the noncognate response regulator lmo1172 in i listeria monocytogenes i under benzalkonium chloride stress
topic <i>Listeria monocytogenes</i>
AgrC
Lmo1172
crosstalk
benzalkonium chloride
url https://www.mdpi.com/2076-2607/12/2/392
work_keys_str_mv AT taoyu crossphosphorylationbetweenagrchistidinekinaseandthenoncognateresponseregulatorlmo1172inilisteriamonocytogenesiunderbenzalkoniumchloridestress
AT xiaojiejiang crossphosphorylationbetweenagrchistidinekinaseandthenoncognateresponseregulatorlmo1172inilisteriamonocytogenesiunderbenzalkoniumchloridestress
AT xiaoboxu crossphosphorylationbetweenagrchistidinekinaseandthenoncognateresponseregulatorlmo1172inilisteriamonocytogenesiunderbenzalkoniumchloridestress
AT pingxu crossphosphorylationbetweenagrchistidinekinaseandthenoncognateresponseregulatorlmo1172inilisteriamonocytogenesiunderbenzalkoniumchloridestress
AT shuxingqiu crossphosphorylationbetweenagrchistidinekinaseandthenoncognateresponseregulatorlmo1172inilisteriamonocytogenesiunderbenzalkoniumchloridestress
AT junleiyin crossphosphorylationbetweenagrchistidinekinaseandthenoncognateresponseregulatorlmo1172inilisteriamonocytogenesiunderbenzalkoniumchloridestress
AT davidphamilton crossphosphorylationbetweenagrchistidinekinaseandthenoncognateresponseregulatorlmo1172inilisteriamonocytogenesiunderbenzalkoniumchloridestress
AT xiaobingjiang crossphosphorylationbetweenagrchistidinekinaseandthenoncognateresponseregulatorlmo1172inilisteriamonocytogenesiunderbenzalkoniumchloridestress