Cooperative Interaction between Acid and Copper Resistance in Escherichia coli
2
조회
0
다운로드
0
인용
0
참고문헌
키워드
초록
The persistence of pathogenic Escherichia coli under acidic conditions poses a serious risk to food safety, especially in acidic foods such as kimchi. To identify the bacterial factors required for acid resistance, transcriptomic analysis was conducted on an acid-resistant enterotoxigenic E. coli strain and the genes with significant changes in their expression under acidic pH were selected as putative resistance factors against acid stress. These genes included those associated with a glutamatedependent acid resistance (GDAR) system and copper resistance. E. coli strains lacking GadA, GadB, or YbaST, the components of the GDAR system, exhibited significantly attenuated growth and survival under acidic stress conditions. Accordantly, the inhibition of the GDAR system by 3- mercaptopropionic acid and aminooxyacetic acid abolished bacterial adaptation and survival under acidic conditions, indicating the indispensable role of a GDAR system in acid resistance. Intriguingly, the lack of cueR encoding a transcriptional regulator for copper resistance genes markedly impaired bacterial resistance to acid stress as well as copper. Conversely, the absence of YbaST severely compromised bacterial resistance against copper, suggesting an interplay between acid and copper resistance. These results suggest that a GDAR system can be a promising target for developing control measures to prevent E. coli resistance to acid and copper treatments.
Abstract
The persistence of pathogenic Escherichia coli under acidic conditions poses a serious risk to food safety, especially in acidic foods such as kimchi. To identify the bacterial factors required for acid resistance, transcriptomic analysis was conducted on an acid-resistant enterotoxigenic E. coli strain and the genes with significant changes in their expression under acidic pH were selected as putative resistance factors against acid stress. These genes included those associated with a glutamatedependent acid resistance (GDAR) system and copper resistance. E. coli strains lacking GadA, GadB, or YbaST, the components of the GDAR system, exhibited significantly attenuated growth and survival under acidic stress conditions. Accordantly, the inhibition of the GDAR system by 3- mercaptopropionic acid and aminooxyacetic acid abolished bacterial adaptation and survival under acidic conditions, indicating the indispensable role of a GDAR system in acid resistance. Intriguingly, the lack of cueR encoding a transcriptional regulator for copper resistance genes markedly impaired bacterial resistance to acid stress as well as copper. Conversely, the absence of YbaST severely compromised bacterial resistance against copper, suggesting an interplay between acid and copper resistance. These results suggest that a GDAR system can be a promising target for developing control measures to prevent E. coli resistance to acid and copper treatments.
참고문헌 (50)
- Hernandez-Reyes C, "Salmonella, a cross-kingdom pathogen infecting humans and plants", FEMS Microbiol. Lett, 343, pp.1~7 (2013)
- Willis C, "Occurrence of listeria and Escherichia coli in frozen fruit and vegetables collected from retail and catering premises in England 2018-2019", Int. J. Food Microbiol, 334, pp.108849~ (2020)
- Mokoena MP, "Applications of lactic acid bacteria and their bacteriocins against food spoilage microorganisms and foodborne pathogens", Molecules, 26, pp.7055~ (2021)
- 조준일, "Characterization of Pathogenic Escherichia coli Strains Linked to an Outbreak Associated with Kimchi Consumption in South Korea, 2012", Food Science and Biotechnology, 23(1), pp.209~214 (2014), 한국식품과학회[DOI]
- Shin J, "Consecutive outbreaks of enterotoxigenic Escherichia coli O6 in schools in South Korea caused by contamination of fermented vegetable kimchi", Foodborne Pathog. Dis, 13, pp.535~543 (2016)
- Croxen MA, "Recent advances in understanding enteric pathogenic Escherichia coli", Clin. Microbiol. Rev, 26, pp.822~880 (2013)
- Nataro JP, "Diarrheagenic Escherichia coli", Clin. Microbiol. Rev, 11, pp.142~201 (1998)
- Lund P, "Coping with low pH : molecular strategies in neutralophilic bacteria", FEMS Microbiol. Rev, 38, pp.1091~1125 (2014)
- Sun Y, "Respiration and the F(1)Fo-ATPase enhance survival under acidic conditions in Escherichia coli", PLoS One, 7, pp.e52577~ (2012)
- Lu P, "L-glutamine provides acid resistance for Escherichia coli through enzymatic release of ammonia", Cell Res, 23, pp.635~644 (2013)
- Ying-Ying Chang, "Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli", Molecular Microbiology, 33(2), pp.249~259 (1999), Wiley[DOI]
- Dahl JU, "HdeB functions as an acid-protective chaperone in bacteria", J. Biol. Chem, 290, pp.9950~ (2015)
- Eguchi Y, "Regulation of acid resistance by connectors of two-component signal transduction systems in Escherichia coli", J. Bacteriol, 193, pp.1222~1228 (2011)
- Hengge R, "Proteolysis of sigmaS(RpoS)and the general stress response in Escherichia coli", Res. Microbiol, 160, pp.667~676 (2009)
- Aquino P, "Coordinated regulation of acid resistance in Escherichia coli", BMC Syst. Biol, 11, pp.1~ (2017)
- Diez-Gonzalez F, "Comparison of the glutamate-, arginine-and lysine-dependent acid resistance systems in Escherichia coli O157 : H7", J Appl. Microbiol, 96, pp.1237~1244 (2004)
- Sayed AK, "A 750 bp sensory integration region directs global control of the Escherichia coli GadE acid resistance regulator", Mol. Microbiol, 71, pp.1435~1450 (2009)
- Zhao B, "Acid stress response in enteropathogenic gammaproteobacteria : an aptitude for survival", Biochem. Cell Biol, 88, pp.301~314 (2010)
- Rensing C, "Escherichia coli mechanisms of copper homeostasis in a changing environment", FEMS Microbiol. Rev, 27, pp.197~213 (2003)
- Djoko KY, "Interplay between tolerance mechanisms to copper and acid stress in Escherichia coli", Proc. Natl. Acad. Sci, 114, pp.6818~6823 (2017)
- Blattner FR, "The complete genome sequence of Escherichia coli K-12", Science, 277, pp.1453~1462 (1997)
- Datsenko KA, "One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products", Proc. Natl. Acad. Sci, 97, pp.6640~6645 (2000)
- Murphy KC, "Lambda Red-mediated recombinogenic engineering of enterohemorrhagic and enteropathogenic E. coli.", BMC Mol. Biol, 4, pp.1~12 (2003)
- Cherepanov PP, "Gene disruption in Escherichia coli : TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant", Gene, 158, pp.9~14 (1995)
- Lynn C. Thomason, "E. coli genome manipulation by P1 transduction", Current Protocols in Molecular Biology, 79(1) (2007), Wiley[DOI]
- Guzman L-M, "Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter", J. Bacteriol, 177, pp.4121~4130 (1995)
- Risso D, "Normalization of RNA-seq data using factor analysis of control genes or samples", Nat. Biotechnol, 32, pp.896~902 (2014)
- Robinson MD, "A scaling normalization method for differential expression analysis of RNA-seq data", Genome Biol, 11, pp.R25~ (2010)
- Dillies M-A, "A comprehensive evaluation of normalization methods for Illumina high-throughput RNA sequencing data analysis", Brief. Bioinform, 14, pp.671~683 (2013)
- Perez-Llamas C, "Gitools : analysis and visualisation of genomic data using interactive heat-maps", PLoS One, 6, pp.e19541~ (2011)
- Arenas FA, "The Escherichia coli btuE gene, encodes a glutathione peroxidase that is induced under oxidative stress conditions", Biochem. Biophys. Res. Commun, 398, pp.690~694 (2010)
- De Biase D, "The response to stationary-phase stress conditions in Escherichia coli : role and regulation of the glutamic acid decarboxylase system", Mol. Microbiol, 32, pp.1198~1211 (1999)
- Outten FW, "The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli", J. Biol. Chem, 276, pp.30670~30677 (2001)
- Lyu C, "Exploring the contributions of two glutamate decarboxylase isozymes in Lactobacillus brevis to acid resistance and gamma-aminobutyric acid production", Microb. Cell Fact, 17, pp.180~ (2018)
- Kimura R, "Glutamate acid decarboxylase 1 promotes metastasis of human oral cancer by β-catenin translocation and MMP7 activation", BMC Cancer, 13, pp.1~11 (2013)
- Lamar Jr C, "Mercaptopropionic acid : a convulsant that inhibits glutamate decarboxylase 1", J. Neurochem, 17, pp.165~170 (1970)
- Grossfeld RM, "Inhibitors of crayfish glutamic acid decarboxylase", Neurochem. Res, 9, pp.947~963 (1984)
- Yin Y, "Effects of the inhibitor of glutamate decarboxylase on the development and GABA accumulation in germinating fava beans under hypoxia-NaCl stress", RSC Adv, 8, pp.20456~20461 (2018)
- Snider Jr DE, "Pyridoxine supplementation during isoniazid therapy", Tubercle, 61, pp.191~196 (1980)
- Wood J, "A correlation between changes in GABA metabolism and isonicotinic acid hydrazide-induced seizures", Brain Res, 45, pp.489~498 (1972)
- Salazar P, "Epilepsy and hippocampal neurodegeneration induced by glutamate decarboxylase inhibitors in awake rats", Epilepsy Res, 116, pp.27~33 (2015)
- Horton R, "Seizures induced by allylglycine, 3-mercaptopropionic acid and 4-deoxypyridoxine in mice and photosensitive baboons, and different modes of inhibition of cerebral glutamic acid decarboxylase", Br. J. Pharmacol, 49, pp.52~63 (1973)
- Lund P, "Coping with low pH : molecular strategies in neutralophilic bacteria", FEMS Microbiol. Rev, 38, pp.1091~1125 (2014)
- Seo SW, "Decoding genome-wide GadEWX-transcriptional regulatory networks reveals multifaceted cellular responses to acid stress in Escherichia coli", Nat. Commun, 6, pp.17970~ (2015)
- Hommais F, "GadE(YhiE) : a novel activator involved in the response to acid environment in Escherichia coli", Microbiology(Reading), 150, pp.61~72 (2004)
- Tucker DL, "Genes of the GadX-GadW regulon in Escherichia coli", J. Bacteriol, 185, pp.3190~3201 (2003)
- Ma Z, "Characterization of EvgAS-YdeO-GadE branched regulatory circuit governing glutamatedependent acid resistance in Escherichia coli", J. Bacteriol, 186, pp.7378~7389 (2004)
- Grass G, "Metallic copper as an antimicrobial surface", Appl. Environ. Microbiol, 77, pp.1541~1547 (2011)
- Montero DA, "Antimicrobial properties of a novel copper-based composite coating with potential for use in healthcare facilities", Antimicrob Resist Infect. Control, 8, pp.3~ (2019)
- Munson GP, "Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12", J. Bacteriol, 182, pp.5864~5871 (2000)