The Global Transcriptional Regulator CodY Promotes Listeria monocytogenes Against Oxidative Stress

Abstract

Abstract: Objective: The purpose of this study was to explore the role of the global transcriptional regulator CodY of Listeria monocytogenes in oxidative stress. Methods: The tolerance of oxidative stress adaptation and the level of antioxidants (CAT, SOD and GSH) were compared between the wild-type strain EGDe and the isogenic CodY deletion strain EGDe?codY at a mid-logarithmic growth stage (OD600=0.65) under H2O2 stress. Genomic template stability (GTS) of the two strains was compared by random amplified polymorphic DNA (RAPD) method and the transcriptional expression of the genes which encode antioxidants and involving in SOS response were assessed by RT-qPCR. Results: (1)The MIC and MBC of EGDe?codY were about twice than that of EGDe under H2O2 stress, and the inhibition zone of EGDe?codY showed a significantly difference when the concentration of H2O2 was over 20 mmol/L(P ≤ 0.01); (2) The growth of EGDe?codY was completely inhibited by 200 mmol/L H2O2, while that of EGDe was slightly slowed down; (3) the catalase activity in both EGDe and EGDe?codY decreased, but the transcription levels of this enzyme had no differences in both strains. SOD activity did not change significantly, but its expression on mRNA level presented significant differences in those two strains (P ≤ 0.001). Notably, the general trend of transcription and concentration level of GSH in the two strains were almost same, which decreased firstly and then rose up slightly following H2O2 stress. Moreover, the transcription level of GSH in EGDe?codY was always lower than that in EGDe (P ≤ 0.01); (4) GTS of EGDe and EGDe?codY were 93.1% and 80.0% respectively. At the same time, the expressions of recA, lexA, recR, lmo1302, and lmo1975, which are important for SOS response, were significantly inhibited in EGDe?codY (P ≤ 0.001), while the expressions of recA, lmo1302 and lmo1975 in EGDe were activated. Conclusions: The deletion of CodY reduced bacterial oxidative tolerance, growth and the concentration of GSH. The stability of bacterial genomic DNA was also decreased, and the genes expression involving in SOS response were inhibited. These data showed that CodY plays an important role in response to oxidative stress in Listeria monocytogenes.

Key words: Listeria monocytogenes, CodY, oxidative stress, SOS response

CLC Number:

TS20

Shi-Yi YANG 罗勤. The Global Transcriptional Regulator CodY Promotes Listeria monocytogenes Against Oxidative Stress[J]. FOOD SCIENCE, 0, (): 0-0.

References

[ ] JUNTTILA J R , NIEMEL S I , HIRN J . Minimum growth temperatures of Listeria monocytogenes and non-haemolytic Listeria[J]. The Journal of Applied Bacteriology, 1988, 65(4):321-327. DOI:10.1111/j.1365-2672.1988.tb01898.x.
[ ] GANDHI M , CHIKINDAS M L. Listeria: A foodborne pathogen that knows how to survive[J]. International Journal of Food Microbiology, 2007, 113(1):1-15. DOI:10.1016/j.ijfoodmicro.2006.07.008.
[ ] In LEE S H, BARANCELLI G V, De CAMARGO T M, et al. Biofilm-producing ability of Listeria monocytogenes isolates from Brazilian cheese processing plants[J]. Food Research International, 2017, 91:88-91.DOI: 10.1016/j.foodres.2016.11.039.
[ ]刘昀阁，罗欣，董鹏程，等. 基于群体感应的单增李斯特菌生物膜形成与控制研究进展[J].食品科学，2019，40 (21): 303-310. DOI:10.7506/spkx1002-6630-20181114-166.
[ ] RíOS-CASTILLO A G, GONZáLEZ-RIVAS F, RODRíGUEZ-JEREZ J J. Bactericidal efficacy of hydrogen peroxide-based disinfectants against Gram-positive and Gram-negative bacteria on stainless steel surfaces[J]. Journal of Food Science, 2017,82(10):2351-2356. DOI: 10.1111/1750-3841.13790.
[ ] LINLEY E , DENYER S P , MCDONNELL G , et al. Use of hydrogen peroxide as a biocide: new consideration of its mechanisms of biocidal action[J]. Journal of Antimicrobial Chemotherapy, 2012, 67(7):1589-1596. DOI:10.1093/jac/dks129.
[ ] 周密, 唐毓祎, 王旭, 等. NaClO胁迫下单核细胞增生李斯特菌WaX12及其sigB基因缺失突变株抗氧化胁迫相关功能基因表达比较[J]. 食品科学, 2017, 38(10): 49-54. DOI:10.7506/spkx1002-6630-201710009.
[ ] CIRIMINNA R , ALBANESE L , MENEGUZZO F , et al. Hydrogen peroxide: A key chemical for today’s sustainable development[J]. ChemSusChem, 2016,9(24),3374-3381. DOI: 10.1002/cssc.201600895.
[ ] LAROSA V, REMACLE C. Insights into the respiratory chain and oxidative stress[J]. Bioscience Reports, 2018, 38:1-14. DOI:10.1042/bsr20171492.
[ ] OJHA D, PATIL K N. p-Coumaric acid inhibits the Listeria monocytogenes RecA protein functions and SOS response: An antimicrobial target[J]. Biochemical and Biophysical Research Communications, 2019, 517:655-661. DOI:10.1016/j.bbrc.2019.07.093.
[ ] WU S, YU P L, WHEELER D, et al. Transcriptomic study on persistence and survival of Listeria monocytogenes following lethal treatment with nisin[J]. Journal of Global Antimicrobial Resistance, 2018, 15:25-31. DOI:10.1016/j.jgar.2018.06.003.
[ ] BRINSMADE S R. CodY, a master integrator of metabolism and virulence in Gram-positive bacteria[J]. Current Genetics, 2016, 63(3):417-425. DOI:10.1007/s00294-016-0656-5.
[ ] den HENGST C D, van HIJUM S A, GEURTS J M, et al. The Lactococcus lactis CodY regulon: identification of a conserved cis-regulatory element[J]. The Journal of Biological Chemistry, 2005, 280(40):34332-34342. DOI:10.1074/jbc.M502349200.
[ ] BELITSKY B R, SONENSHEIN A L. Genetic and biochemical analysis of CodY-binding sites in Bacillus subtilis[J]. Journal of Bacteriology, 2008, 190(4):1224-1236. DOI:10.1128/JB.01780-07.
[ ] MAJERCZYK C D, DUNMAN P M, LUONG T T, et al. Direct targets of CodY in Staphylococcus aureus[J]. Journal of Bacteriology, 2010, 192(11):2861-2877. DOI:10.1128/JB.00220-10.
[ ] LOBEL L, HERSKOVITS A A. Systems level analyses reveal multiple regulatory activities of CodY controlling metabolism, motility and virulence in Listeria monocytogenes[J]. PLoS Genet, 2016, 12(2):e1005870. DOI:10.1371/journal.pgen.1005870.
[ ] WANG Y, HE H Y, LI H H, et al. The global regulator CodY responds to oxidative stress by the regulation of glutathione biosynthesis in Streptococcus thermophilus[J]. Journal of Dairy Science, 2017, 100(11):8768-8775. DOI: 10.3168/jds.2017-13007.
[ ] HAJAJ B, YESILKAYA H, SHAFEEQ S, et al. CodY regulates thiol peroxidase expression as part of the pneumococcal defense mechanism against H2O2 stress[J]. Frontiers in Cellular and Infection Microbiology, 2017, 7:210. DOI:10.3389/fcimb.2017.00210.
[ ] 张颖, 汤雨倩, 沈怡, 等. CodY在单核细胞增生李斯特菌运动和毒力方面的作用[J]. 中国生物工程杂志, 2017, 37(7):56-63. DOI:10.13523/j.cb.20170711.
[ ] WALLACE N, NEWTON E, ABRAMS E, et al. Metabolic determinants in Listeria monocytogenes anaerobic listeriolysin O production[J]. Archives of Microbiology,2017,199(6): 827-837. DOI:10.1007/s00203-017-1355-4.
[ ] LOBEL L, SIGAL N, BOROVOK I, et al. The metabolic regulator CodY links Listeria monocytogenes metabolism to virulence by directly activating the virulence regulatory gene prfA[J]. Molecular Microbiology, 2015, 95(4):624-644.DOI:10.1111/mmol/Li.12890.
[ ] GLASER P, FRANGEUL L, BUNCHRIESER C, et al. Comparative genomics of Listeria species[J]. Science, 2001, 294(5543): 849-852. DOI: 10.1126/science.1063447.
[ ] ATIENZAR F A, JHA A N. The random amplified polymorphic DNA (RAPD) assay and related techniques applied to genotoxicity and carcinogenesis studies: A critical review[J]. Reviews in Mutation Research, 2006, 613:76-102. DOI:10.1016/j.mrrev.2006.06.001.
[ ] BASTET L, TURCOTTE P, WADE J T, et al. Maestro of regulation: Riboswitches orchestrate gene expression at the levels of translation, transcription and mRNA decay[J]. RNA Biology, 2018,15(6):679-682. DOI:10.1038/s41467-020-15653-7.
[ ] IMLAY J A. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium[J]. Nature Reviews Microbiology, 2013, 11(7):443-454. DOI:10.1038/nrmicro3032.
[ ] CASANO L M , GóMEZ L D, LASCANO H R, et al. Inactivation and degradation of Cu/Zn-SOD by active oxygen species in wheat chloroplasts exposed to photooxidative stress[J]. Plant and Cell Physiology, 1997, 38(4):433-440. DOI:10.1093/oxfordjournals.pcp. a029186.
[ ] RABINOVICH L, SIGAL N, BOROVOK I, et al. Prophage excision activates Listeria competence genes that promote phagosomal escape and virulence[J]. Cell, 2012, 150(4):792-802. DOI:10.1016/j.cell.2012.06.036.
[ ] KALIA D, MEREY G, NAKAYAMA S, et al. Nucleotide, c-di-GMP, c-di-AMP, cGMP, cAMP, (p)ppGpp signaling in bacteria and implications in pathogenesis[J]. Chemical Society Reviews, 2013, 42(1):305-341. DOI:10.1039/c2cs35206k.
[ ] van der VEEN S, van SCHALKWIJK S, MOLENAAR D, et al, The SOS response of Listeria monocytogenes is involved in stress resistance and mutagenesis[J]. Microbiology, 2010, 156(2):374-384. DOI:10.1099/mic.0.035196-0.

[1]	ZHANG Qingyan, ZHAO Jun, ZHANG Zhe, CHEN Xiong, YAO Lan. Effect of Glucose on Vanillin Tolerance of Starmerella bacillaris [J]. FOOD SCIENCE, 2024, 45(4): 96-107.
[2]	LIU Fenfen, PU Shoucheng, ZHAO Wenliang, WANG Yiting, XUE Chen, XU Lishan. Hypoglycemic and Antioxidant Effects of Camellia nitidissima Flower on Type 2 Diabetic Mice [J]. FOOD SCIENCE, 2024, 45(3): 94-101.
[3]	ZHANG Le, CUI Jinna, LIU Wei, ZHU Mingda, LIU Zhanying. Research Progress on Tolerance Mechanism of Saccharomyces cerevisiae [J]. FOOD SCIENCE, 2024, 45(3): 317-325.
[4]	WANG Qing, JIN Shengzhu, LI Guangyao, LIN Changqing. Hypoglycemic and Hepatoprotective Effect of Angelica dahurica Polysaccharide in Type 2 Diabetic Rats [J]. FOOD SCIENCE, 2023, 44(7): 176-183.
[5]	QI Tingting, ZHANG Yimin, YANG Xiaoyin, LUO Xin, MAO Yanwei. Recent Progress in Research on the Effect of Oxidative Stress on Beef Color and Stability [J]. FOOD SCIENCE, 2023, 44(7): 260-266.
[6]	CAI Xixi, LI Chen, CHEN Xu, HUANG Yuannan, FU Caili, WANG Shaoyun. Protective Effect of Functional Peptides Derived from Crimson Snapper Scales on Oxidative Stress Damage in Caco-2 Cells [J]. FOOD SCIENCE, 2023, 44(7): 10-17.
[7]	DU Juan, CHEN Xin, LIU Kai, LIU Jialei, LUO Pengjie, LIANG Dong, BAI Yanhong. Highly Sensitive Colorimetric Detection of Listeria monocytogenes by Using Gold Nanoparticles Based on Magnetic Metal-Organic Framework Separation [J]. FOOD SCIENCE, 2023, 44(6): 360-367.
[8]	REN Junhe, ZENG Ping, CHEN Sirui, YI Lanhua. Inhibitory Effect of Antimicrobial Peptide zp37 on Listeria monocytogenes in Fruit Juice and Its Action Mechanism [J]. FOOD SCIENCE, 2023, 44(5): 29-37.
[9]	LIU Peng, HOU Zhixing, MAO Hongwei, LI Heng, GONG Jinsong, JIANG Min, XU Hongyu, XU Zhenghong, SHI Jinsong. Ameliorative Effect and Mechanism of Chitooligosaccharides on Hydrogen Peroxide-Induced Injury in Hepatic Cells [J]. FOOD SCIENCE, 2023, 44(5): 136-142.
[10]	LIN Zhiwei, WANG Shuai, WANG Yingchun, WU Zhanwen, LI Tao, LI Hongna, YANG Yange, YUAN Fei. Establishment of a Dual Enzymatic Recombinase Amplification Method for Rapid Detection of Foodborne Pathogens in Infant Formula Powder [J]. FOOD SCIENCE, 2023, 44(18): 347-354.
[11]	YIN Yanyan, ZHAO Yi, CHU Huicheng, LIANG Jinjie, HAN Xiaojia, CHEN Zujun, WANG Lingzhi. Protective Effect of Coix Seed Bioactive Peptide on Human Umbilical Vein Endothelial Cells Injured by High Glucose [J]. FOOD SCIENCE, 2023, 44(17): 79-85.
[12]	XU Qing, TAN Shuming, YU Lu, YUAN Meng, TAN Yunyun, ZHANG Liqun. Effect and Mechanism of Rosa roxburghii Fruit Polyphenols on Hypertension Induced by NG-Nitro-L-Arginine Methyl Ester in Mice [J]. FOOD SCIENCE, 2023, 44(17): 94-100.
[13]	LI Shouhan, GAO Wenfeng, CUI Zhijia. Renal Protective Effects of Lanzhou Lily (Lilium davidii var. unicolor) Polysaccharide and Aerobic Exercise in Streptozotocin-Induced Diabetic Rats [J]. FOOD SCIENCE, 2023, 44(15): 165-180.
[14]	JIA Qiansheng, ZUO Feng. Ameliorative Effect of Lactobacillus plantarum L15 on Excessive Exercise-Induced Skeletal Muscle Injury in Rats [J]. FOOD SCIENCE, 2023, 44(13): 79-87.
[15]	CAO Wenjing, LIU Shuang, LI Jiali, QIN Huishan, SU Yanmin, LIANG Chanhua, LI Wanying, ZENG Zhen, SONG Jiale. Tea Seed Saponin Combined with Aerobic Exercise Ameliorated Lipid Metabolism and Oxidative Stress in High-Fat Diet-Fed Mice [J]. FOOD SCIENCE, 2023, 44(11): 106-114.