CLC number: S855.1
On-line Access: 2024-08-27
Received: 2023-10-17
Revision Accepted: 2024-05-08
Crosschecked: 2019-06-13
Cited: 0
Clicked: 3404
Ke He, Yong-Ping Xin, Ying Shan, Xian Zhang, Hou-Hui Song, Wei-Huan Fang. Phosphorylation residue T175 in RsbR protein is required for efficient induction of sigma B factor and survival of Listeria monocytogenes under acidic stress[J]. Journal of Zhejiang University Science B, 2019, 20(8): 660-669.
@article{title="Phosphorylation residue T175 in RsbR protein is required for efficient induction of sigma B factor and survival of Listeria monocytogenes under acidic stress",
author="Ke He, Yong-Ping Xin, Ying Shan, Xian Zhang, Hou-Hui Song, Wei-Huan Fang",
journal="Journal of Zhejiang University Science B",
volume="20",
number="8",
pages="660-669",
year="2019",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1800551"
}
%0 Journal Article
%T Phosphorylation residue T175 in RsbR protein is required for efficient induction of sigma B factor and survival of Listeria monocytogenes under acidic stress
%A Ke He
%A Yong-Ping Xin
%A Ying Shan
%A Xian Zhang
%A Hou-Hui Song
%A Wei-Huan Fang
%J Journal of Zhejiang University SCIENCE B
%V 20
%N 8
%P 660-669
%@ 1673-1581
%D 2019
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1800551
TY - JOUR
T1 - Phosphorylation residue T175 in RsbR protein is required for efficient induction of sigma B factor and survival of Listeria monocytogenes under acidic stress
A1 - Ke He
A1 - Yong-Ping Xin
A1 - Ying Shan
A1 - Xian Zhang
A1 - Hou-Hui Song
A1 - Wei-Huan Fang
J0 - Journal of Zhejiang University Science B
VL - 20
IS - 8
SP - 660
EP - 669
%@ 1673-1581
Y1 - 2019
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1800551
Abstract: Listeria monocytogenes is an important zoonotic foodborne pathogen that can tolerate a number of environmental stresses. rsbR, an upstream regulator of the sigma B (SigB) factor, is thought to sense environmental challenges and trigger the SigB pathway. In Bacillus subtilis, two phosphorylation sites in rsbR are involved in activating the SigB pathway and a feedback mechanism, respectively. In this study, the role of rsbR in L. monocytogenes under mild and severe stresses was investigated. Strains with genetic deletion (ΔrsbR), complementation (C-ΔrsbR), and phosphorylation site mutations in the rsbR (rsbR-T175A, rsbR-T209A, and rsbR-T175A-T209A) were constructed to evaluate the roles of these rsbR sequences in listerial growth and survival. SigB was examined at the transcriptional and translational levels. Deletion of rsbR reduced listerial growxth and survival in response to acidic stress. Substitution of the phosphorylation residue rsbR-T175A disabled rsbR complementation, while rsbR-T209A significantly upregulated SigB expression and listerial survival. Our results provide clear evidence that two phosphorylation sites of rsbR are functional in L. monocytogenes under acidic conditions, similar to the situation in B. subtilis.
[1]Chaturongakul S, Boor KJ, 2004. Rsbt and RsbV contribute to σB-dependent survival under environmental, energy, and intracellular stress conditions in Listeria monocytogenes. Appl Environ Microbiol, 70(9):5349-5356.
[2]Chen CC, Yudkin MD, Delumeau O, 2004. Phosphorylation and RsbX-dependent dephosphorylation of RsbR in the RsbR-RsBs complex of Bacillus subtilis. J Bacteriol, 186(20):6830-6836.
[3]Chen JS, Cheng CY, Xia Y, et al., 2011. Lmo0036, an ornithine and putrescine carbamoyltransferase in Listeria monocytogenes, participates in arginine deiminase and agmatine deiminase pathways and mediates acid tolerance. Microbiology, 157(11):3150-3161.
[4]Cotter PD, Gahan CGM, Hill C, 2000. Analysis of the role of the Listeria monocytogenes F0F1-ATPase operon in the acid tolerance response. Int J Food Microbiol, 60(2-3):137-146.
[5]Delumeau O, Chen CC, Murray JW, et al., 2006. High-molecular-weight complexes of RsbR and paralogues in the environmental signaling pathway of Bacillus subtilis. J Bacteriol, 188(22):7885-7892.
[6]Eymann C, Schulz S, Gronau K, et al., 2011. In vivo phosphorylation patterns of key stressosome proteins define a second feedback loop that limits activation of Bacillus subtilis σB. Mol Microbiol, 80(3):798-810.
[7]Gaidenko TA, Bie XM, Baldwin EP, et al., 2012. Two surfaces of a conserved interdomain linker differentially affect output from the RST sensing module of the Bacillus subtilis stressosome. J Bacteriol, 194(15):3913-3921.
[8]Hecker M, Pané-Farré J, Völker U, 2007. Sigb-dependent general stress response in bacillus subtilis and related Gram-positive bacteria. Annu Rev Microbiol, 61:215-236.
[9]Hecker M, Reder A, Fuchs S, et al., 2009. Physiological proteomics and stress/starvation responses in Bacillus subtilis and staphylococcus aureus. Res Microbiol, 160(4):245-258.
[10]Kim TJ, Gaidenko TA, Price CW, 2004a. A multicomponent protein complex mediates environmental stress signaling in Bacillus subtilis. J Mol Biol, 341(1):135-150.
[11]Kim TJ, Gaidenko TA, Price CW, 2004b. In vivo phosphorylation of partner switching regulators correlates with stress transmission in the environmental signaling pathway of Bacillus subtilis. J Bacteriol, 186(18):6124-6132.
[12]Liebal UW, Thomas M, Jon MW, et al., 2013. Simulations of stressosome activation emphasize allosteric interactions between RsbR and RsbT. BMC Syst Biol, 7:3.
[13]Livak KJ, Schmittgen TD, 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT. Methods, 25(4):402-408.
[14]Marles-Wright J, Grant T, Delumeau O, et al., 2008. Molecular architecture of the “stressosome,” a signal integration and transduction hub. Science, 322(5898):92-96.
[15]Martinez L, Reeves A, Haldenwang W, 2010. Stressosomes formed in Bacillus subtilis from the RsbR protein of Listeria monocytogenes allow σB activation following exposure to either physical or nutritional stress. J Bacteriol, 192(23):6279-6286.
[16]NicAogáin K, O'Byrne CP, 2016. The role of stress and stress adaptations in determining the fate of the bacterial pathogen Listeria monocytogenes in the food chain. Front Microbiol, 7:1865.
[17]O'Byrne CP, Karatzas KAG, 2008. Chapter 5: the role of sigma B (σB) in the stress adaptations of Listeria monocytogenes: overlaps between stress adaptation and virulence. Adv Appl Microbiol, 65:115-140.
[18]Okpo E, Leith J, Smith-Palmer A, et al., 2015. An outbreak of an unusual strain of Listeria monocytogenes infection in North-East Scotland. J Infect Public Health, 8(6):612-618.
[19]Pané-Farré J, Lewis RJ, Stülke J, 2005. The RsbRST stress module in bacteria: a signalling system that may interact with different output modules. J Mol Microbiol Biotechnol, 9:65-76.
[20]Price CW, 2011. General stress response in Bacillus subtilis and related Gram-positive bacteria. In: Storz G, Hengge R (Eds.), Bacterial Stress Responses, 2nd Ed. American Society of Microbiology (ASM) Press, Washington, DC, p.301-318.
[21]Shan Y, Liu ZQ, Li GW, et al., 2018. Nucleocapsid protein from porcine epidemic diarrhea virus isolates can antagonize interferon-λ production by blocking the nuclear factor-κB nuclear translocation. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 19(8):570-580.
[22]Shin JH, Brody MS, Price CW, 2010. Physical and antibiotic stresses require activation of the RsbU phosphatase to induce the general stress response in Listeria monocytogenes. Microbiology, 156:2660-2669.
[23]Varma JK, Samuel MC, Marcus R, et al., 2007. Listeria monocytogenes infection from foods prepared in a commercial establishment: a case-control study of potential sources of sporadic illness in the united states. Clin Inf Dis, 44(4):521-528.
[24]Xia Y, Xin YP, Li XL, et al., 2016. To modulate survival under secondary stress conditions, Listeria monocytogenes 10403S employs RsbX to downregulate σB activity in the poststress recovery stage or stationary phase. Appl Environ Microbiol, 82(4):1126-1135.
[25]Zhang ZC, Meng QL, Qiao J, et al., 2013. RsbV of Listeria monocytogenes contributes to regulation of environmental stress and virulence. Arch Microbiol, 195(2):113-120.
[26]Zhou YS, Gu YX, Qi BZ, et al., 2017. Porcine circovirus type 2 capsid protein induces unfolded protein response with subsequent activation of apoptosis. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 18(4):316-323.
Open peer comments: Debate/Discuss/Question/Opinion
<1>