Sub-lethal Concentrations of Phytochemicals (Carvacrol and Oregano) Select for Reduced Susceptibility Mutants of Escherichia coli O23:H52

AFNAN A. AL-MNASER; MARTIN J. WOODWARD

doi:10.33073/pjm-2020-003

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Sub-lethal Concentrations of Phytochemicals (Carvacrol and Oregano) Select for Reduced Susceptibility Mutants of Escherichia coli O23:H52

Polish Journal of Microbiology

Volume 69 (2020): Issue 1 (March 2020)

By: AFNAN A. AL-MNASER and MARTIN J. WOODWARD

Open Access

|Feb 2020

Abstract

In vitro studies aimed at studying the mechanism of action of carvacrol and oregano as natural anti-bacterial agents to control multiple antibiotic-resistant avian pathogenic Escherichia coli (APEC) strain O23:H52 isolated from chicken were performed. Derivatives with increased minimum inhibitory concentrations (MIC) to the phytochemicals were selected after growing Escherichia coli (E. coli) strain O23:H52 at sub-lethal concentrations of carvacrol and oregano for a period of 60 days. Whole-genome sequencing (WGS) of two derivatives revealed a missense mutation in cadC and marR: the genes responsible for survival mechanisms and antibiotic resistance by efflux, respectively.

References

Alekshun MN, Levy SB. The Escherichia coli mar locus-antibiotic resistance and more. ASM News. 2004;70:451–456.
Search in Google Scholar Back to article
Alkhandari F. Characterization of Escherichia coli in poultry and their interaction with phytochemicals [dissertation]. University of Reading; 2017.
Search in Google Scholar Back to article
Al-Mnaser A. Phytochemicals (carvacrol and oregano extract) as possible alternatives to antibiotics in poultry feed [dissertation]. University of Reading; 2019.
Search in Google Scholar Back to article
Alvarez MV, Ortega-Ramirez LA, Silva-Espinoza BA, Gonzalez-Aguilar GA, Ayala-Zavala JF. Antimicrobial, antioxidant, and sensorial impacts of oregano and rosemary essential oils over broccoli florets. J Food Process Preserv. 2019 Mar;43(3):e13889. https://doi.org/10.1111/jfpp.13889
Search in Google Scholar Back to article
Ariza RR, Cohen SP, Bachhawat N, Levy SB, Demple B. Repressor mutations in the marRAB operon that activate oxidative stress genes and multiple antibiotic resistance in Escherichia coli. J Bacteriol. 1994 Jan;176(1):143–148. https://doi.org/10.1128/jb.176.1.143-148.1994
Search in Google Scholar Back to article
Baricevic D, Bartol T. The biological/pharmacological activity of the Origanum genus. Oregano, the genera Origanum and Lippia. New York (USA): Taylor & Francis Inc.; 2002. p. 177–201.
Search in Google Scholar Back to article
Bryant J, Chewapreecha C, Bentley SD. Developing insights into the mechanisms of evolution of bacterial pathogens from whole-genome sequences. Future Microbiol. 2012 Nov;7(11):1283–1296. https://doi.org/10.2217/fmb.12.108
Search in Google Scholar Back to article
Chueca B, Renzoni A, Berdejo D, Pagán R, Kelley WL, García-Gonzalo D. Whole-genome sequencing and genetic analysis reveals novel stress responses against individual constituents of essential oils in Escherichia coli. Appl Environ Microbiol. 2018 Mar 19;84(7):e02538-17. https://doi.org/10.1128/AEM.02538-17
Search in Google Scholar Back to article
Cohen SP, Hächler H, Levy SB. Genetic and functional analysis of the multiple antibiotic resistance (mar) locus in Escherichia coli. J Bacteriol. 1993 Mar;175(5):1484–1492. https://doi.org/10.1128/jb.175.5.1484-1492.1993
Search in Google Scholar Back to article
Cristani M, D’Arrigo M, Mandalari G, Castelli F, Sarpietro MG, Micieli D, Venuti V, Bisignano G, Saija A, Trombetta D. Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity. J Agric Food Chem. 2007 Jul;55(15):6300–6308. https://doi.org/10.1021/jf070094x
Search in Google Scholar Back to article
Di Pasqua R, Hoskins N, Betts G, Mauriello G. Changes in membrane fatty acids composition of microbial cells induced by addiction of thymol, carvacrol, limonene, cinnamaldehyde, and eugenol in the growing media. J Agric Food Chem. 2006 Apr;54(7): 2745–2749. https://doi.org/10.1021/jf052722l
Search in Google Scholar Back to article
Di Pasqua R, Mauriello G, Mamone G, Ercolini D. Expression of DnaK, HtpG, GroEL and Tf chaperones and the corresponding encoding genes during growth of Salmonella Thompson in presence of thymol alone or in combination with salt and cold stress. Food Res Int. 2013 Jun;52(1):153–159. https://doi.org/10.1016/j.foodres.2013.02.050
Search in Google Scholar Back to article
Friedman M, Henika PR, Mandrell R. Bactericidal activities of plant essential oils and some of their isolated constituents against Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, and Salmonella enterica. J Food Prot. 2002 Oct;65(10):1545–1560. https://doi.org/10.4315/0362-028X-65.10.1545
Search in Google Scholar Back to article
George AM, Levy SB. Amplifiable resistance to tetracycline, chloramphenicol, and other antibiotics in Escherichia coli: involvement of a non-plasmid-determined efflux of tetracycline. J Bacteriol. 1983 Aug;155(2):531–540.
Search in Google Scholar Back to article
Jayalakshmi B, Raveesha K, Amruthesh K. Phytochemical investigations and antibacterial activity of some medicinal plants against pathogenic bacteria. J Appl Pharm Sci. 2011;1:124.
Search in Google Scholar Back to article
Joensen KG, Tetzschner AM, Iguchi A, Aarestrup FM, Scheutz F. Rapid and easy in silico serotyping of Escherichia coli using whole genome sequencing (WGS) data. J Clin Microbiol. 2015 Aug;53(8): 2410-26. https://doi.org/10.1128/JCM.00008-15
Search in Google Scholar Back to article
Johnson TJ, Wannemuehler Y, Doetkott C, Johnson SJ, Rosenberger SC, Nolan LK. Identification of minimal predictors of avian pathogenic Escherichia coli virulence for use as a rapid diagnostic tool. J Clin Microbiol. 2008 Dec 01;46(12):3987–3996. https://doi.org/10.1128/JCM.00816-08
Search in Google Scholar Back to article
Küper C, Jung K. CadC-mediated activation of the cadBA promoter in Escherichia coli. J Mol Microbiol Biotechnol. 2005;10(1):26–39. https://doi.org/10.1159/000090346
Search in Google Scholar Back to article
Luz IS, de Melo ANF, Bezerra TKA, Madruga MS, Magnani M, de Souza EL. Sublethal amounts of Origanum vulgare L. essential oil and carvacrol cause injury and changes in membrane fatty acid of Salmonella Typhimurium cultivated in a meat broth. Foodborne Pathog Dis. 2014 May;11(5):357–361. https://doi.org/10.1089/fpd.2013.1695
Search in Google Scholar Back to article
Marcus A, Edori O, Maduagu M. Phytochemical and antimicrobial screening of Phyllantus fratenus and Taraxacuim officinale leaves. Biochem Anal Biochem. 2019;8(1):376. https://doi.org/10.35248/2161-1009.19.8.376
Search in Google Scholar Back to article
Mathlouthi N, Bouzaienne T, Oueslati I, Recoquillay F, Hamdi M, Urdaci M, Bergaoui R. Use of rosemary, oregano, and a commercial blend of essential oils in broiler chickens: in vitro antimicrobial activities and effects on growth performance1. J Anim Sci. 2012 Mar 01;90(3):813–823. https://doi.org/10.2527/jas.2010-3646
Search in Google Scholar Back to article
Miladi H, Zmantar T, Chaabouni Y, Fedhila K, Bakhrouf A, Mahdouani K, Chaieb K. Antibacterial and efflux pump inhibitors of thymol and carvacrol against food-borne pathogens. Microb Pathog. 2016 Oct;99:95–100. https://doi.org/10.1016/j.micpath.2016.08.008
Search in Google Scholar Back to article
Monte J, Abreu A, Borges A, Simões L, Simões M. Antimicrobial activity of selected phytochemicals against Escherichia coli and Staphylococcus aureus and their biofilms. Pathogens. 2014 Jun 18; 3(2):473–498. https://doi.org/10.3390/pathogens3020473
Search in Google Scholar Back to article
Rajamanickam K, Yang J, Sakharkar MK. Phytochemicals as alter natives to antibiotics against major pathogens involved in bovine respiratory disease (BRD) and bovine mastitis (BM). Bioinformation. 2019 Jan 31;15(1):32–35. https://doi.org/10.6026/97320630015032
Search in Google Scholar Back to article
Richter K, Haslbeck M, Buchner J. The heat shock response: life on the verge of death. Mol Cell. 2010 Oct;40(2):253–266. https://doi.org/10.1016/j.molcel.2010.10.006
Search in Google Scholar Back to article
Sepehri S, Kotlowski R, Bernstein CN, Krause DO. Phylogenetic analysis of inflammatory bowel disease associated Escherichia coli and the fimH virulence determinant. Inflamm Bowel Dis. 2009 Nov;15(11):1737–1745. https://doi.org/10.1002/ibd.20966
Search in Google Scholar Back to article
Sikkema J, de Bont JA, Poolman B. Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev. 1995 Jun;59(2):201–222.
Search in Google Scholar Back to article
Skalicka-Woźniak K, Walasek M, Aljarba TM, Stapleton P, Gibbons S, Xiao J, Łuszczki JJ. The anticonvulsant and anti-plasmid conjugation potential of Thymus vulgaris chemistry: an in vivo murine and in vitro study. Food Chem Toxicol. 2018 Oct;120: 472–478. https://doi.org/10.1016/j.fct.2018.07.045
Search in Google Scholar Back to article
Soksawatmaekhin W, Kuraishi A, Sakata K, Kashiwagi K, Igarashi K. Excretion and uptake of cadaverine by CadB and its physiological functions in Escherichia coli. Mol Microbiol. 2004 Mar; 51(5): 1401–1412. https://doi.org/10.1046/j.1365-2958.2003.03913.x
Search in Google Scholar Back to article
Sulavik MC, Gambino LF, Miller PF. The MarR repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli: prototypic member of a family of bacterial regulatory proteins involved in sensing phenolic compounds. Mol Med. 1995 May;1(4): 436–446. https://doi.org/10.1007/BF03401581
Search in Google Scholar Back to article
Tenaillon O, Taddei F, Radman M, Matic I. Second-order selection in bacterial evolution: selection acting on mutation and recombination rates in the course of adaptation. Res Microbiol. 2001 Jan; 152(1):11–16. https://doi.org/10.1016/S0923-2508(00)01163-3
Search in Google Scholar Back to article
Tetsch L, Koller C, Dönhöfer A, Jung K. Detection and function of an intramolecular disulfide bond in the pH-responsive CadC of Escherichia coli. BMC Microbiol. 2011;11(1):74. https://doi.org/10.1186/1471-2180-11-74
Search in Google Scholar Back to article
Tetsch L, Koller C, Haneburger I, Jung K. The membrane-integrated transcriptional activator CadC of Escherichia coli senses lysine indirectly via the interaction with the lysine permease LysP. Mol Microbiol. 2008 Feb;67(3):570–583. https://doi.org/10.1111/j.1365-2958.2007.06070.x
Search in Google Scholar Back to article
Ultee A, Bennik MHJ, Moezelaar R. The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl Environ Microbiol. 2002 Apr 01;68(4):1561–1568. https://doi.org/10.1128/AEM.68.4.1561-1568.2002
Search in Google Scholar Back to article
Watson N, Dunyak DS, Rosey EL, Slonczewski JL, Olson ER. Identification of elements involved in transcriptional regulation of the Escherichia coli cad operon by external pH. J Bacteriol. 1992 Jan;174(2):530–540. https://doi.org/10.1128/jb.174.2.530-540.1992
Search in Google Scholar Back to article
Wink M. Phytochemical diversity of secondary metabolites. In: Goodman RM, editor. Encyclopedia of plant and crop science. New ork (USA): Marcel Dekker, Inc.; 2004.
Search in Google Scholar Back to article
Wong JMW, de Souza R, Kendall CWC, Emam A, Jenkins DJA. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol. 2006 Mar;40(3):235–243. https://doi.org/10.1097/00004836-200603000-00015
Search in Google Scholar Back to article
Yuan W, Teo CHM, Yuk HG. Combined antibacterial activities of essential oil compounds against Escherichia coli O157:H7 and their application potential on fresh-cut lettuce. Food Control. 2019 Feb;96:112–118. https://doi.org/10.1016/j.foodcont.2018.09.005
Search in Google Scholar Back to article

Articles in this issue

DOI: https://doi.org/10.33073/pjm-2020-003 | Journal eISSN: 2544-4646 | Journal ISSN: 1733-1331

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Language: English

Page range: 121 - 125

Submitted on: Oct 14, 2019

Accepted on: Dec 21, 2019

Published on: Feb 18, 2020

Published by: Polish Society of Microbiologists

In partnership with: Paradigm Publishing Services

Publication frequency: 4 issues per year

Keywords:

E. coli ,

APEC,

phytochemicals,

antibiotic resistance,

WGS

Related subjects:

Life sciences,

Microbiology and virology

© 2020 AFNAN A. AL-MNASER, MARTIN J. WOODWARD, published by Polish Society of Microbiologists
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.

Volume 69 (2020): Issue 1 (March 2020)