Highlights
• E. coli O157:H7 suffered oxygen starvation under the stress of kojic acid
• E. coli O157:H7 suffered sulfur starvation under the stress of tea polyphenols
• Kojic acid and tea polyphenols hindered the uptake of iron of E. coli O157:H7
Open Access
Antibacterial mechanism of kojic acid and tea polyphenols against Escherichia coli O157:H7 through transcriptomic analysis
Yehui Zhangb 
(
), Yigang Yua,c()
(), Yigang Yua,c()Abstract
Escherichia coli O157:H7 is one of the major foodborne pathogenic bacterial that cause infectious diseases in humans. The previous found that a combination of kojic acid and tea polyphenols exhibited better activity against E. coli O157:H7 than using either alone. This study aimed to explore responses underlying the antibacterial mechanisms of kojic acid and tea polyphenols from the gene level. The functional enrichment analysis by comparing kojic acid and tea polyphenols individually or synergistically against E. coli O157:H7 found that acid resistance systems in kojic acid were activated, and the cell membrane and genomic DNA were destructed in the cells, resulting in “oxygen starvation”. The oxidative stress response triggered by tea polyphenols inhibited both sulfur uptake and the synthesis of ATP, which affected the bacteria's life metabolic process. Interestingly, we found that kojic acid combined with tea polyphenols hindered the uptake of iron that played an essential role in the synthesis of DNA, respiration, tricarboxylic acid cycle. The results suggested that the iron uptake pathways may represent a novel approach for kojic acid and tea polyphenols synergistically against E. coli O157:H7 and provided a theoretical basis for bacterial pathogen control in the food industry.
References
[1]
M.O. Masana, G.A. Leotta, L.D. Castillo, et al., Prevalence, characterization, and genotypic analysis of Escherichia coli O157:H7 from selected beef exporting abattoirs of argentina, J. Food Prot. 73 (2010) 649-656. https://doi.org/10.4315/0362-028X-73.4.649.
[2]
G.E. Mellor, T.E. Besser, M.A. Davis, et al., Multilocus genotype analysis of Escherichia coli O157 isolates from australia and the united states provides evidence of geographic divergence, Appl. Environ. Microbiol. 79 (2013) 5050-5058. https://doi.org/10.1128/AEM.01525-13.
[3]
M. Elhadidy, A. Álvarez-Ordóñez, Diversity of survival patterns among Escherichia coli O157:H7 genotypes subjected to food-related stress conditions, Front. Microbiol. 7 (2016) 322. https://doi.org/10.3389/fmicb.2016.00322.
[4]
K. Thea, J.V. Cassandra, R.A. Theo, et al., Transcriptomic response of Escherichia coli O157 isolates on meat: comparison between a typical australian isolate from cattle and a pathogenic clinical isolate, Food Microbiol. 82 (2019) 378-387. https://doi.org/10.1016/j.fm.2019.03.008.
[5]
M.S. Nair, P. Lau, K. Belskie, et al., Enhancing the thermal destruction of Escherichia coli O157:H7 in ground beef patties by natural antimicrobials, Meat Sci. 112 (2016) 163. https://doi.org/10.1016/j.meatsci.2015.08.138.
[6]
P.D. Hari, V.K. Juneja, X. Yan, Novel natural food antimicrobials, Annu. Rev. Food Sci. Technol. 3 (2012) 381-403. https://doi.org/10.1146/annurev-food-022811-101241.
[7]
R. Bentley, From miso, sake and shoyu to cosmetics: a century of science for kojic acid, Nat. Prod. Rep. 23 (2007) 1046-1062. https://doi.org/10.1002/chin.200718231.
[8]
X. Liu, W. Xia, Q. Jiang, et al., Effect of kojic acid-grafted-chitosan oligosaccharides as a novel antibacterial agent on cell membrane of gram-positive and gram-negative bacteria, J. Biosci. Bioeng. 120 (2015) 335-339. https://doi.org/10.1016/j.jbiosc.2015.01.010.
[9]
Y. Chusiri, R. Wongpoomchai, W. Min, et al., Modulation of cytochrome P450 expression by kojic acid in rats, Thai J. Toxicol. 26 (2011) 93-93.
[10]
T. Tamotsu, I. Toshio, O. Jun-Ichi, et al., Enhancement of hepatocarcinogen esis by kojic acid in rat two-stage models after initiation with N-bis(2-hydroxypropyl)nitrosamine or N-diethylnitrosamine, Toxicology 81 (2004) 43-49. https://doi.org/10.1093/toxsci/kfh195.
[11]
M.D. Aytemir, B. Ozcelik, A study of cytotoxicity of novel chlorokojic acid derivatives with their antimicrobial and antiviral activities, Eur. J. Med. Chem. 45 (2010) 4089-4095. https://doi.org/10.1016/j.ejmech.2010.05.069.
[12]
N.C. Gordon, D.W. Wareham, Antimicrobial activity of the green tea polyphenol (–)-epigallocatechin-3-gallate (EGCG) against clinical isolates of Stenotrophomonas maltophilia, Int. J. Antimicrob. Agents 36 (2010) 129-131. https://doi.org/10.1016/j.ijantimicag.2010.03.025.
[13]
S. Castillo, N. Heredia, S. García, 2(5H)-Furanone, epigallocatechin gallate, and a citric-based disinfectant disturb quorum-sensing activity and reduce motility and biofilm formation of Campylobacter jejuni, Folia Microbiol. 60 (2015) 89-95. https://doi.org/10.1007/s12223-014-0344-0.
[14]
W.H. Zhao, Z.Q. Hu, S. Okubo, et al., Mechanism of synergy between epigallocatechin gallate and β-lactams against methicillin-resistant Staphylococcus aureus, Antimicrob. Agents Chemother. 45 (2001) 1737-1742. https://doi.org/10.1128/AAC.45.6.1737-1742.2001.
[15]
X. Nie, L. Wang, W. Qi, et al., Effect of a sodium alginate coating infused with tea polyphenols on the quality of fresh Japanese sea bass (Lateolabrax japonicas) fillets, J. Food Sci. 83 (2018) 1695-1700. https://doi.org/10.1111/1750-3841.14184.
[16]
S. Zhao, N. Li, Z. Li, et al., Shelf life of fresh chilled pork as affected by antimicrobial intervention with nisin, tea polyphenols, chitosan, and their combination, Int. J. Food Prop. 22 (2019) 1047-1063. https://doi.org/10.1080/10942912.2019.1625918.
[17]
H. Li, L. Zou, Q. Yang, et al., Antimicrobial activities of nisin, tea polyphenols, and chitosan and their combinations in chilled mutton, J. Food Sci. 81 (2016) M1466. https://doi.org/10.1111/1750-3841.13312.
[18]
R. Wang, M. Fang, X. Hu, et al., Kojic acid and tea polyphenols inactivate Escherichia coli O157:H7 in vitro and on salmon fillets by inflicting damage on cell membrane and binding to genomic DNA, Int. J. Food Sci. Technol. 56 (2021) 6039-6051. https://doi.org/10.1111/ijfs.15268.
[19]
N. Noboru, H. Naomi, T. Claudia, et al., Epigallocatechin gallate inhibits the type Ⅲ secretion system of gram negative enteropathogenic bacteria under model condition, FEMS Microbiol. Lett. 364 (2017) 13. https://doi.org/10.1093/femsle/fnx111.
[20]
T.Nie, C.Zhang, A.Huang, et al., Epigallocatechin gallate-mediated cell death is triggered by accumulation of reactive oxygen species induced via the Cpx two-component system in Escherichia coli, Front. Microbiol. 9 (2018) 246. https://doi.org/10.3389/fmicb.2018.00246.
[21]
Y. Adewunmi, S. Namjilsuren, W.D. Walker, et al., Antimicrobial activity of, and cellular pathways targeted by, p-anisaldehyde and epigallocatechin gallate in the opportunistic human pathogen Pseudomonas aeruginosa, Appl. Environ. Microbiol. 86 (2020) e02482-02419. https://doi.org/10.1128/AEM.02482-19.
[22]
A. Kitichalermkiat, M. Katsuki, J. Sato, et al., Effect of epigallocatechin gallate on gene expression of Staphylococcus aureus, J. Glob. Antimicrob. Resist. 22 (2020) 854-859. https://doi.org/10.1016/j.jgar.2020.06.006.
[23]
B. Langmead, S. L. Salzberg, Fast gapped-read alignment with bowtie 2, Nat. Methods 9 (2012) 357-359. https://doi.org/10.1038/nmeth.1923.
[24]
D. Kim, G. Pertea, C. Trapnell, et al., TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions, Genome Biol. 14 (2013) 1-13. https://doi.org/10.1186/gb-2013-14-4-r36.
[25]
Z. Ailian, C. Yifang, Z. Donggen, et al., Global transcriptomic analysis of cronobacter sakazakii CICC 21544 by RNA-seq under inorganic acid and organic acid stresses, Food Res. Int. 130 (2020) 108963. https://doi.org/10.1016/j.foodres.2019.108963.
[26]
G.K. Smyth, edgeR: a bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics 26 (2010) 139-140. https://doi.org/10.1093/bioinformatics/btp616.
[27]
J. Trček, N.P. Mira, L.R. Jarboe, Adaptation and tolerance of bacteria against acetic acid, Appl. Microbiol. Biotechnol. 99 (2015) 6215-6229. https://doi.org/10.1007/s00253-015-6762-3.
[28]
L. Yu, S. Zhang, Y. Xu, et al., Acid resistance of E. coli O157:H7 and O26:H11 exposure to lactic acid revealed by transcriptomic analysis, LWT-Food Sci. Technol. 136 (2021) 110352. https://doi.org/10.1016/j.lwt.2020.110352.
[29]
J.W. Foster, Escherichia coli acid resistance: tales of an amateur acidophile, Nat. Rev. Microbiol. 2 (2004) 898-907. https://doi.org/10.1038/nrmicro1021.
[30]
M.P. Castanie-Cornet, T.A. Penfound, D. Smith, et al., Control of acid resistance in Escherichia coli. J. Bacteriol. 181 (1999) 3525-3535. https://doi.org/10.1128/JB.181.11.3525-3535.1999.
[31]
R. Iyer, C. Williams, C. Miller, Arginine-agmatine antiporter in extreme acid resistance in Escherichia coli, J. Bacteriol. 185 (2003) 6556-6561. https://doi.org/10.1128/JB.185.22.6556-6561.2003.
[32]
T. Oshima, H. Aiba, Y. Masuda, et al., Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12, Mol. Microbiol. 46 (2002) 281-291. https://doi.org/10.1046/j.1365-2958.2002.03170.x.
[33]
J. Cole, Nitrate reduction to ammonia by enteric bacteria: redundancy, or a strategy for survival during oxygen starvation, FEMS Microbiol. Lett. 136 (1996) 1-11. https://doi.org/10.1111/j.1574-6968.1996.tb08017.x.
[34]
M. Mokhtar, M.Z.M. Yusoff, M.S.M. Ali, et al., Pseudogene YdfW in Escherichia coli decreases hydrogen production through nitrate respiration pathways, Int. J. Hydrog. Energy 44 (2019) 16212-16223. https://doi.org/10.1016/j.ijhydene.2019.04.228.
[35]
C. Punginelli, B. Ize, N.R. Stanley, et al., mRNA secondary structure modulates translation of tat-dependent formate dehydrogenase N, J. Bacteriol. 186 (2004) 6311. https://doi.org/10.1128/JB.186.18.6311-6315.2004.
[36]
RS. Rabin, V. Stewart, Either of two functionally redundant sensor proteins, narX and narQ, is sufficient for nitrate regulation in Escherichia coli K-12, Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 8419-8423. https://doi.org/10.1073/pnas.89.18.8419.
[37]
C.P. Tseng, A.K. Hansen, P. Cotter, et al., Effect of cell growth rate on expression of the anaerobic respiratory pathway operons frdABCD, dmsABC, and narGHJI of Escherichia coli, J. Bacteriol. 176 (1994) 6599-6605. https://doi.org/0021-9193/94/04.00+0.
[38]
C. Bordi, L. Théraulaz, V. Méjean, et al., Anticipating an alkaline stress through the tor phosphorelay system in Escherichia coli, Mol. Microbiol. 48 (2003) 211-223. https://doi.org/10.1046/j.1365-2958.2003.03428.x.
[39]
Y. Wu, Y.G. Shi, L.Y. Zeng, et al., Evaluation of antibacterial and anti-biofilm properties of kojic acid against five food-related bacteria and related subcellular mechanisms of bacterial inactivation, Food Sci. Technol. Int. 25 (2019) 3-15. https://doi.org/10.1177/1082013218793075.
[40]
C. Engl, G. Jovanovic, L.J. Lloyd, et al., In vivo localizations of membrane stress controllers pspA and pspG in Escherichia coli, Mol. Microbiol. 73 (2010) 382-396. https://doi.org/10.1111/j.1365-2958.2009.06776.x.
[41]
S.E. Jones, L.J. Lloyd, K.K. Tan, et al., Secretion defects that activate the phage shock response of Escherichia coli, J. Bacteriol. 185 (2003) 6707-6711. https://doi.org/10.1128/JB.185.22.6707-6711.2003.
[42]
G. Jovanovic, L.J. Lloyd, M. Stumpf, et al., Induction and function of the phage shock protein extracytoplasmic stress response in Escherichia coli, J. Biol. Chem. 281 (2006) 21147-21161. https://doi.org/10.1074/jbc.M602323200.
[43]
A. Kumar, N. Beloglazova, C. Bundalovic-Torma, et al., Conditional epistatic interaction maps reveal global functional rewiring of genome integrity pathways in Escherichia coli, Cell Rep. 14 (2016) 648-661. https://doi.org/10.1016/j.celrep.2015.12.060.
[44]
X.X. Liu, B.M. Shen, P. Du, et al., Transcriptomic analysis of the response of Pseudomonas fluorescens to epigallocatechin gallate by RNA-seq, PLoS One 12 (2017) e0177938. https://doi.org/10.1371/journal.pone.0177938.
[45]
A. Lovato, A. Pignatti, N. Vitulo, et al., Inhibition of virulence-related traits in pseudomonas syringae pv. actinidiae by gunpowder green tea extracts, Front. Microbiol. 10 (2019) 2362. https://doi.org/10.3389/fmicb.2019.02362.
[46]
S.M. Chiang, H.E. Schellhorn, Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria, Arch. Biochem. Biophys. 525 (2021) 161-169. https://doi.org/10.1016/j.abb.2012.02.007.
[47]
P.J. Pomposiello, A. Koutsolioutsou, D. Carrasco, et al., SoxRS-regulated expression and genetic analysis of the yggX gene of Escherichia coli, J. Bacteriol. 185 (2003) 6624-6632. https://doi.org/10.1128/JB.185.22.6624-6632.2003.
[48]
J. Ploeg, E. Eichhorn, T. Leisinger, Sulfonate-sulfur metabolism and its regulation in Escherichia coli, Arch. Microbiol. 176 (2001) 1-8. https://doi.org/10.1007/s002030100298.
[49]
J.R. van der Ploeg, M.A. Weiss, E. Saller, et al., Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source, J. Bacteriol. 178 (1996) 5438-5446. https://doi.org/10.1590/S1516-35982005000700035.
[50]
M. Nishikawa, L.H.Shen, K. Ogawa, Taurine dioxygenase (tauD)-independent taurine assimilation in Escherichia coli, Microbiology 164 (2018) 1466-1456. https://doi.org/10.1099/mic.0.000723.
[51]
B.K. Cho, S. A. Federowicz, E Mallory, et al., The purR regulon in Escherichia coli K-12 MG1655, Nucleic Acids Res. 39 (2011) 6456-6464. https://doi.org/10.1093/nar/gkr307.
[52]
M.H. Jia, R.A. Larossa, J.M. Lee, et al., Global expression profiling of yeast treated with an inhibitor of amino acid biosynthesis, sulfometuron methyl, Physiol. Genomics 3 (2000) 83-92. https://doi.org/10.1152/physiolgenomics.2000.3.2.83.
[53]
K. Michalska, J. Gale, G. Joachimiak, et al., Conservation of the structure and function of bacterial tryptophan synthases, IUCrJ 6 (2019) 649-664. https://doi.org/10.1107/S2052252519005955.
[54]
X. Tang, S. Ezaki, S. Fujiwara, et al., The tryptophan biosynthesis gene cluster trpCDEGFBA from pyrococcus kodakaraensis KOD1 is regulated at the transcriptional level and expressed as a single mRNA, Mol. Genet. Genom. 262 (1999) 815-821. https://doi.org/10.1007/s004380051145.
[55]
D. Grandjean, F. Jorand, H. Guilloteau, et al., Iron uptake is essential for Escherichia coli survival in drinking water, Lett. Appl. Microbiol. 43 (2006) 111-117. https://doi.org/10.1111/j.1472-765X.2006.01895.x.
[56]
D.R. Peralta, C. Adle, N.S. Corbalán, et al., Enterobactin as part of the oxidative stress response repertoire, PLoS One 11 (2016) e0157799. https://doi.org/10.1371/journal.pone.0157799.
[57]
C.L. Washington Hughes, G.T Ford, A.D. Jones, et al., Nickel exposure reduces enterobactin production in Escherichia coli, Microbiologyopen 8 (2019) e00691. https://doi.org/10.1002/mbo3.691.
[58]
H.L. Pi, J.D. Helmann, Sequential induction of fur-regulated genes in response to iron limitation in bacillus subtilis, Proc. Natl. Acad. Sci. U.S.A. 114 (2019) 12785-12790. https://doi.org/10.1073/pnas.1713008114.
[59]
J. Li, C. Attila, T.K. Wood, et al., Quorum sensing in Escherichia coli is signaled by AI-2/LsrR: effects on small RNA and biofilm architecture, J. Bacteriol. 189 (2007) 6011-6020. https://doi.org/10.1128/JB.00014-07.
[60]
N.S. Jakubovics, J.C. Robinson, D.S. Samarian, et al., Critical roles of arginine in growth and biofilm development by streptococcus gordonii, Mol. Microbiol. 97 (2015) 281-300. https://doi.org/10.1111/mmi.13023.
[61]
S. Xu, J. Zhou, L. Liu, et al., Arginine: a novel compatible solute to protect candida glabrata against hyperosmotic stress, Process Biochem. 46 (2011) 1230-1235. https://doi.org/10.1016/j.procbio.2011.01.026.
[62]
J.P. Weerasinghe, T. Dong, M.R. Schertzberg, et al., Stationary phase expression of the arginine biosynthetic operon argCBH in Escherichia coli, BMC Microbiol. 6 (2006) 1-12. https://doi.org/10.1186/1471-2180-6-14.
Pages 736-747
Cite this article:
Lin Y, Wang R, Li X, et al. Antibacterial mechanism of kojic acid and tea polyphenols against Escherichia coli O157:H7 through transcriptomic analysis. Food Science and Human Wellness, 2024, 13(2): 736-747. https://doi.org/10.26599/FSHW.2022.9250063
Metrics & Citations
Article History
Copyright
Rights and Permissions
京公网安备11010802044758号