STM1827在鼠伤寒沙门菌生物被膜形成及环境应激中的调控作用

doi:10.11843/j.issn.0366-6964.2023.12.030

Abstract

Abstract: The aim was to study the regulation of the c-di-GMP pathway metabolic gene STM1827 on the biofilm of Salmonella Typhimurium and its related biological functions. Firstly, we analyzed the effect of STM1827 on the content of c-di-GMP by measuring the level of c-di-GMP; Further analyzed the effect of STM1827 on biofilm formation through experiments such as biofilm and motility; Finally, the effects of STM1827 on the adaptability of Salmonella Typhimurium to environmental stress were analyzed through experiments such as oxygen stress and disinfectant stress. The results showed that the intracellular c-di-GMP level of the mutant strain 269ΔSTM1827 was 33.16% higher than that of wild strain. In terms of biofilm formation, compared with the wild strain, the mutant strain 269ΔSTM1827 had a 2.19-fold increase in the ability of biofilm formation, a 1.3-fold increase in the content of biofilm related extracellular polysaccharide, and a significant increase in the expression of extracellular polysaccharide synthesis genes (P<0.000 1). In terms of motility, the motility of 269ΔSTM1827 was decreased by 13%, and the expression of flagella-related genes was significantly decreased (P<0.05). And STM1827 gene mutant enhanced the adaptive ability of Salmonella Typhimurium under oxygen stress and disinfectant stress. The study showed that STM1827 can degrade c-di-GMP, inhibit the formation of biofilm by inhibiting the synthesis of extracellular polysaccharide and promoting bacterial motility, and ultimately lead to the decrease of bacterial tolerance under oxygen and disinfectant stress. This study provides a theoretical basis for the screening of salmonellosis targets and the development of prevention and control measures.

Key words: Salmonella Typhimurium, c-di-GMP, STM1827, biofilm, motility, adapting

CLC Number:

LI Lili, CHEN Kaifeng, CHEN Bing, ZHOU Zhouping, WANG Nanwei, QU Xiaoyun, XU Chenggang, LIAO Ming, ZHANG Jianmin. Regulatory Role of STM1827 in the Biofilm Formation and Environmental Stress of Salmonella Typhimurium[J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(12): 5207-5217.

References

[1] 张临, 卢芳, 付恒峰, 等. 鼠伤寒沙门菌BaeSR对氟喹诺酮类药物耐药性的调控机制[J]. 畜牧兽医学报, 2022, 53(3):894-903.ZHANG L, LU F, FU H F, et al. Regulation mechanism of BaeSR on fluoroquinolones resistance in Salmonella Typhimurium[J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(3):894-903. (in Chinese)
[2] POPA G L, POPA M I. Salmonella spp. infection-a continuous threat worldwide[J]. Germs, 2020, 11(1):88-96.
[3] 曹莉, 武周慧, 程如楠, 等. 鼠伤寒沙门菌mgtC基因生物学功能的研究[J]. 北京农学院学报, 2022, 37(2):66-71.CAO L, WU Z H, CHENG R N, et al. On the biological characteristics of mgtC gene deletion strain of Salmonella Typhimurium[J]. Journal of Beijing University of Agriculture, 2022, 37(2):66-71. (in Chinese)
[4] 费霞, 田一辰, 黄山, 等. tolB和tolR基因缺失对鼠伤寒沙门菌生物学功能的影响[J]. 中国兽医科学, 2022, 52(11):1422-1429.FEI X, TIAN Y C, HUANG S, et al. Effect of tolB and tolR gene deletions on biological functions of Salmonella Typhimurium[J]. Chinese Veterinary Science, 2022, 52(11):1422-1429. (in Chinese)
[5] WANG Y N, LIU Y, LYU N, et al. The temporal dynamics of antimicrobial-resistant Salmonella enterica and predominant serovars in China[J]. Natl Sci Rev, 2023, 10(3):nwac269.
[6] CHEN K F, GAO Y, LI L L, et al. Increased drug resistance and biofilm formation ability in ST34-type Salmonella Typhimurium exhibiting multicellular behavior in China[J]. Front Microbiol, 2022, 13:876500.
[7] WINTER S E, THIENNIMITR P, WINTER M G, et al. Gut inflammation provides a respiratory electron acceptor for Salmonella[J]. Nature, 2010, 467(7314):426-429.
[8] ZENG M Y, INOHARA N, NUÑEZ G. Mechanisms of inflammation-driven bacterial dysbiosis in the gut[J]. Mucosal Immunol, 2017, 10(1):18-26.
[9] 苏洋洋, 黄骏, 吴白, 等. 鼠伤寒沙门菌rpoN基因缺失株构建及生物学特性研究[J]. 畜牧兽医学报, 2016, 47(4):771-778.SU Y Y, HUANG J, WU B, et al. Construction and biological characterization of rpoN gene deletion mutants of Salmonella Typhimurium[J]. Acta Veterinaria et Zootechnica Sinica, 2016, 47(4):771-778. (in Chinese)
[10] 曹莉, 程如楠, 武周慧, 等. 鼠伤寒沙门菌sapC基因缺失株的构建及生物学特性分析[J]. 畜牧兽医学报, 2022, 53(7):2282-2289. CAO L, CHENG R N, WU Z H, et al. Construction and biological characteristics of sapC gene deletion strain of Salmonella Typhimurium[J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(7):2282-2289. (in Chinese)
[11] 旷年玲, 左丽, 吕兴帮, 等. 生物被膜形成对大肠杆菌致病性的影响[J]. 现代畜牧兽医, 2022(9):82-86.KUANG N L, ZUO L, LV X B, et al. Effect of biofilm formation on pathogenicity of Escherichia coli[J]. Modern Journal of Animal Husbandry and Veterinary Medicine, 2022(9):82-86. (in Chinese)
[12] SISTI F, HA D G, O'TOOLE G A, et al. Cyclic-di-GMP signalling regulates motility and biofilm formation in Bordetella bronchiseptica[J]. Microbiology (Reading), 2013, 159(Pt 5):869-879.
[13] 霍卫萍, 刘智猛, 陈韦, 等. 铜绿假单胞菌二鸟苷酸环化酶SiaD突变体的功能研究[J]. 微生物学报, 2022, 62(10):3997-4007. HUO W P, LIU Z M, CHEN W, et al. Functions of mutants of diguanylate cyclase SiaD from Pseudomonas aeruginosa[J]. Acta Microbiologica Sinica, 2022, 62(10):3997-4007. (in Chinese)
[14] RÖMLING U. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae[J]. Cell Mol Life Sci, 2005, 62(11):1234-1246.
[15] AHMAD I, WIGREN E, LE GUYON S, et al. The EAL-like protein STM1697 regulates virulence phenotypes, motility and biofilm formation in Salmonella Typhimurium[J]. Mol Microbiol, 2013, 90(6):1216-1232.
[16] SIMM R, REMMINGHORST U, AHMAD I, et al. A role for the EAL-like protein STM1344 in regulation of CsgD expression and motility in Salmonella enterica serovar Typhimurium[J]. J Bacteriol, 2009, 191(12):3928-3937.
[17] SIMM R, MORR M, KADER A, et al. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility[J]. Mol Microbiol, 2004, 53(4):1123-1134.
[18] DATSENKO K A, WANNER B L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products[J]. Proc Natl Acad Sci U S A, 2000, 97(12):6640-6645.
[19] GÓMEZ-BALTAZAR A, VÁZQUEZ-GARCIDUENAS M S, LARSEN J, et al. Comparative stress response to food preservation conditions of ST19 and ST213 genotypes of Salmonella enterica serotype Typhimurium[J]. Food Microbiol, 2019, 82:303-315.
[20] ZHANG Z Q, DU W N, WANG M, et al. Contribution of the colicin receptor CirA to biofilm formation, antibotic resistance, and pathogenicity of Salmonella Enteritidis[J]. J Basic Microbiol, 2020, 60(1):72-81.
[21] DRESSAIRE C, MOREIRA R N, BARAHONA S, et al. BolA is a transcriptional switch that turns off motility and turns on biofilm development[J]. mBio, 2015, 6(1):e02352-14.
[22] SIMM R, LUSCH A, KADER A, et al. Role of EAL-containing proteins in multicellular behavior of Salmonella enterica serovar Typhimurium[J]. J Bacteriol, 2007, 189(9):3613-3623.
[23] 张家莉, 段世宇, 令狐远凤, 等. 鼠伤寒沙门菌ompA基因缺失株的构建及生物学特性的分析[J]. 中国动物传染病学报, 2022, 30(6):27-33. ZHANG J L, DUAN S Y, LINGHU Y F, et al. Construction of ompA gene deletion Strain of Salmonella Typhimurium and analysis of its biological characteristics[J]. Chinese Journal of Animal Infectious Diseases, 2022, 30(6):27-33. (in Chinese)
[24] FOUNOU L L, FOUNOU R C, ESSACK S Y. Antibiotic resistance in the food chain:a developing country-perspective[J]. Front Microbiol, 2016, 7:1881.
[25] PENESYAN A, GILLINGS M, PAULSEN I T. Antibiotic discovery:combatting bacterial resistance in cells and in biofilm communities[J]. Molecules, 2015, 20(4):5286-5298.
[26] KUMAR A, ALAM A, RANI M, et al. Biofilms:survival and defense strategy for pathogens[J]. Int J Med Microbiol, 2017, 307(8):481-489.
[27] DULA S, AJAYEOBA T A, IJABADENIYI O A. Bacterial biofilm formation on stainless steel in the food processing environment and its health implications[J]. Folia Microbiol (Praha), 2021, 66(3):293-302.
[28] 王帅涛, 高倩倩, 成娟丽, 等. 铜绿假单胞菌生物被膜组成及其受群体感应系统和c-di-GMP调控的研究进展[J]. 微生物学报, 2021, 61(5):1106-1122.WANG S T, GAO Q Q, CHENG J L, et al. Regulation of Pseudomonas aeruginosa biofilms by quorum sensing systems and c-di-GMP[J]. Acta Microbiologica Sinica, 2021, 61(5):1106-1122. (in Chinese)
[29] WHITNEY J C, COLVIN K M, MARMONT L S, et al. Structure of the cytoplasmic region of PelD, a degenerate diguanylate cyclase receptor that regulates exopolysaccharide production in Pseudomonas aeruginosa[J]. J Biol Chem, 2012, 287(28):23582-23593.
[30] ALY M A, REIMHULT E, KNEIFEL W, et al. Characterization of biofilm formation by Cronobacter spp. isolates of different food origin under model conditions[J]. J Food Prot, 2019, 82(1):65-77.
[31] KARATAN E, WATNICK P. Signals, regulatory networks, and materials that build and break bacterial biofilms[J]. Microbiol Mol Biol Rev, 2009, 73(2):310-347.
[32] 赵文瑾, 尚道涵, 谢来工, 等. 铜绿假单胞菌环二鸟苷酸代谢及其调控生物膜形成研究进展[J]. 中国病原生物学杂志, 2022, 17(12):1468-1474.ZHAO W J, SHANG D H, XIE L G, et al. Research progress on C-di-GMP metabolism and its regulation of biofilm formation in Pseudomonas aeruginosa[J]. Journal of Pathogen Biology, 2022, 17(12):1468-1474. (in Chinese)
[33] VENKATESAN N, PERUMAL G, DOBLE M. Bacterial resistance in biofilm-associated bacteria[J]. Future Microbiol, 2015, 10(11):1743-1750.
[34] CHIN K C J, TAYLOR T D, HEBRARD M, et al. Transcriptomic study of Salmonella enterica subspecies enterica serovar Typhi biofilm[J]. BMC Genomics, 2017, 18(1):836.
[35] 季春辉, 郭蕴, 王立霞, 等. sRNA rli82分子特征及其对单核细胞增生李斯特菌环境应激和生物被膜形成的调控作用[J]. 农业生物技术学报, 2022, 30(5):990-998.JI C H, GUO Y, WANG L X, et al. Molecular characterization of sRNA rli82 and its regulation roles in environmental stress and biofilm formation in Listeria monocytogenes[J]. Journal of Agricultural Biotechnology, 2022, 30(5):990-998. (in Chinese)
[36] 郭蕴, 季春辉, 王立霞, 等. sRNA rli106在单核细胞增生李斯特菌环境应激及生物被膜形成中的调控作用研究[J]. 中国预防兽医学报, 2022, 44(3):277-283.GUO Y, JI C H, WANG L X, et al. The regulatory roles of sRNA rli106 in adaptability of Listeria monocytogenes to environmental stress and biofilm formation[J]. Chinese Journal of Preventive Veterinary Medicine, 2022, 44(3):277-283. (in Chinese)

Regulatory Role of STM1827 in the Biofilm Formation and Environmental Stress of Salmonella Typhimurium

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	HE Qifu, GAO Feng, WU Shenghui, ZHANG Yong, QUAN Fusheng. Advances in Ion Channels Involved in the Regulation of Mammalian Sperm Motility [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(7): 2708-2722.
[2]	HAN Xiuyuan, ZHAO Liang, WANG Chuang, QI Meiyu, YAO Yuchang. Nicotinic Acid Enhances Low Temperature Preservation of Sheep Sperm by Reducing Oxidative Stress Levels [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(5): 1979-1989.
[3]	QIN Lei, WU Huimin, XU Qiqi, CHEN Wanzhao, WANG Dong, LI Hongbo, XIA Panpan, LIU Zepeng, XIA Lining. Effect of Exogenous Drug-Resistant Salmonella Typhimurium on Intestinal Flora in Healthy Mice [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(5): 2158-2169.
[4]	JIANG Zenghai, TENG Lin, HE Anwen, LIU Yanyan, YUE Min, HE Qigai. Genomic Analysis of Salmonella Typhimurium Isolates and Salmonella Serotype 4, [5], 12: i:- Isolates from Pig-borne Food Chain [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(3): 1199-1209.
[5]	HAO Ruochen, TANG Minjia, LIU Guangliang, ZHANG Yan, MUHAMMAD Shoaib, SHANG Ruofeng, CAO Zongxi, PU Wanxia. Distribution and Genotyping of Major Enterobacteriaceae Bacteria in Milk Sources and Dairy Farm Environment of Hainan Province [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(12): 5184-5197.
[6]	WU Zhouhui, WANG Yu, DU Heng, WANG Zhiwen, XIAO Shuang, WU Jinliang, WANG Zhen. Analysis of the Antibacterial Sensitization Activity of Tirapazamine against Multi-Drug Resistant Salmonella [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(10): 4362-4371.
[7]	MAO Yanni, CHANG Jiawei, LI Na, WANG Xin, KANG Xinyun, MA Qiang, MA Liang, WANG Guiqin. Transcriptome Differential Expression Analysis of Staphylococcus aureus in Biofilm State and Planktonic State [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(8): 2697-2707.
[8]	CAO Li, CHENG Runan, WU Zhouhui, WANG Jiawei, WANG Yu, ZHANG Yonghong, WU Qingmin, WANG Zhen. Construction and Biological Characteristics of sapC Gene Deletion Strain of Salmonella Typhimurium [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(7): 2282-2289.
[9]	LI Hui, XIONG Jing, MEI Cui, WANG Shiyuan, ZHOU Yang, LI Xiaofen, FU Guihua, ZHANG Yang, CHENG Peng, HE Yuzhang, CHEN Hongwei. The Safety and Stability of the Antimicrobial Peptide CRAMP and Its Role in Eradicating Pseudomonas aeruginosa Biofilms [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(5): 1576-1586.
[10]	ZHANG Lin, LU Fang, FU Hengfeng, JIANG Xidi, WEI Qiling, QI Caili, GAO Haixia, LI Lin. Regulation Mechanism of BaeSR on Fluoroquinolones Resistance in Salmonella Typhimurium [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(3): 894-903.
[11]	HE Lüqin, YAN Xuefeng, WEN Xintian, CAO Sanjie, HUANG Xiaobo, WU Rui, ZHAO Qin, WEN Yiping. Construction and Biological Characteristic of Glaesserella parasuis Strain with qseB, qseC Double Gene Deletion [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(2): 529-537.
[12]	JIANG Kai, ZHAO Pengyu, WANG Tianshuo, YU Siwen, BI Lan, XIAO Jiawei, HE Xianjing, GUO Donghua. Analysis of Biological Characteristics of Fusobacterium necrophorum 43K OMP Genes Mutant Strain [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(11): 4019-4026.
[13]	HOU Bo,WANG Chenyan,ZHOU Lunjiang. The Roles and Regulatory Mechanisms of Toxin-antitoxin System in Bacterial Biofilm Formation [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(10): 3326-3334.
[14]	HE Yirong, ZHANG Yijie, YANG Wei, CHEN Xiaocong, ZHANG Jiaxiang, CHEN Peifu. Isolation, Identification and Biological Properties of a Lytic Phage against Salmonella Typhimurium [J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(3): 763-771.
[15]	XIONG Xianrong, ZHANG Yan, XIONG Yan, MIN Xingyu, WU Jinbo, HAO Zhenyu, ZHANG He, LI Jian. The Establishment of X, Y Sperm Sorting System in Yak by Flow Cytometer [J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(2): 399-407.