J Appl Biomed 18:106-114, 2020 | DOI: 10.32725/jab.2020.014
Action of carvacrol in Salmonella Typhimurium biofilm: A proteomic study
- 1 State University of Maringá, Department of Clinical Analysis and Biomedicine, Maringá, Brazil
- 2 State University of Minas Gerais, Department of Biological Sciences, Ituiutaba, Brasil
- 3 State University of Maringá, Department of Technology, Umuarama, Brazil
- 4 State University of Maringá , Department of Biochemistry, Maringá, Brazil
- 5 State University of Maringá, Department of Basic Health Sciences, Maringá, Brazil
Carvacrol presents action in Salmonella Typhimurium biofilms, however the antibiofilm mechanism of this compound has not been fully established yet. In the present study, the aim was to evaluate protein profile changes in S. Typhimurium biofilm treated with carvacrol. Proteomic analysis of treated versus untreated biofilm showed several changes in proteins involved with S. Typhimurium biofilm and antioxidant activity. The proteins DsbA (thiol: disulfide interchange protein DsbA), LuxS (S-ribosylhomocysteine lyase), DksA (RNA polymerase binding transcription factor DksA), and SODs (superoxide dismutases) A, B and C had their synthesis decreased after treatment with carvacrol. These proteins play a key role in S. Typhimurium biofilm formation, demonstrating the dynamic antibiofilm action of carvacrol. The differentially expressed proteins identified provide possible action targets for future studies in order to gain more insight into the mechanism of action of carvacrol on S. Typhimurium biofilm.
Keywords: Carvacrol; Biofilms; Proteome; Salmonella Typhimurium
Grants and funding:
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001 and the Complexo de Centrais de Apoio à Pesquisa (COMCAP) of the State University of Maringá. We also thank the Laboratory of Mass Spectrometry at the Brazilian Biosciences National Laboratory (LNBio), CNPEM, CampiTrevisan et al. / J Appl Biomed 113 nas, Brazil for their support with the use of RP-nano UPLC (nanoAcquity, Waters) equipment coupled with a Q-Tof Premier mass spectrometer (Waters).
Conflicts of interest:
The authors declare that they have no conflict of interests.
Received: April 9, 2020; Revised: July 30, 2020; Accepted: September 8, 2020; Prepublished online: September 22, 2020; Published: December 14, 2020 Show citation
ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- Amaral VCS, Santos PR, Silva AF, Santos AR, Machinski M, Jr., Mikcha JMG (2015). Effect of carvacrol and thymol on Salmonella spp. biofilms on polypropylene. Int J Food Sci Technol 50: 2639-2643. DOI: 10.1111/ijfs.12934.
Go to original source...
- Anwar N, Rouf SF, Römling U, Rhen M (2014). Modulation of biofilm-formation in Salmonella enterica serovar Typhimurium by the periplasmic DsbA/DsbB oxidoreductase system requires the GGDEF-EAL domain protein STM3615. PLoS One 9(8): e106095. DOI: 10.1371/journal.pone.0106095.
Go to original source...
Go to PubMed...
- Aragão AZB, Belloni M, Simabuco FM, Zanetti MR, Yokoo S, Domingues RR, et al. (2012). Novel processed form of syndecan-1 shed from SCC-9 cells plays a role in cell migration. PLoS One 7(8): e43521. DOI: 10.1371/journal.pone.0043521.
Go to original source...
Go to PubMed...
- Azriel S, Goren A, Rahav G, Gal-Mor O (2016). The stringent response regulator DksA is required for Salmonella enterica Serovar Typhimurium growth in minimal medium, motility, biofilm formation, and intestinal colonization. Infect Immun 84(1): 375-384. DOI: 10.1128/IAI.01135-15.
Go to original source...
Go to PubMed...
- Borges A, Abreu AC, Dias C, Saavedra MJ, Borges F, Simões M (2016). New perspectives on the use of phytochemicals as an emergent strategy to control bacterial infections including biofilms. Molecules 21(7): 877. DOI: 10.3390/molecules21070877.
Go to original source...
Go to PubMed...
- Bradford M (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
Go to original source...
Go to PubMed...
- Bridier A, Sanchez-Vizuete P, Guilbaud M, Piard JC, Naitali M, Briandet R (2015). Biofilm-associated persistence of food-borne pathogens. Food Microbiol 45: 167-178. DOI: 10.1016/j.fm.2014.04.015.
Go to original source...
Go to PubMed...
- Burt S (2004). Essential oils: their antibacterial properties and potential applications in foods - a review. Int J Food Microbiol 94(3): 223-253. DOI: 10.1016/j.ijfoodmicro.2004.03.022.
Go to original source...
Go to PubMed...
- Burt SA, Ojo-Fakunle VTA, Woertman J, Veldhuizen EJA (2014) The natural antimicrobial carvacrol inhibits quorum sensing in Chromobacterium violaceum and reduces bacterial biofilm formation at sub-lethal concentrations. PLoS One 9(4): e93414. DOI: 10.1371/journal.pone.0093414.
Go to original source...
Go to PubMed...
- Cappitelli F, Polo A, Villa F (2014). Biofilm formation in food processing environments is still poorly understood and controlled. Food Eng Rev 6(1-2): 29-42. DOI: 10.1007/s12393-014-9077-8.
Go to original source...
- Center for Disease Control and Prevention - CDC (2018). National Salmonella Surveillance. [online] [cit. 2019-03-05]. Available at: https://www.cdc.gov/nationalsurveillance/salmonella-surveillance.html
- Center for Disease Control and Prevention - CDC (2019). [online] [cit. 2019-04-15]. Available at: https://www.cdc.gov/salmonella/index.html
- Choi J, Shin D, Ryu S (2007). Implication of quorum sensing in Salmonella enterica serovar Typhimurium virulence: The luxS gene is necessary for expression of genes in pathogenicity island 1. Infect Immun 75(10): 4885-4890. DOI: 10.1128/IAI.01942-06.
Go to original source...
Go to PubMed...
- Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Wokman C, et al. (2007). Integration of biological networks and gene expression data using cytoscape. Nat Protoc 2(10): 2366-2382. DOI: 10.1038/nprot.2007.324.
Go to original source...
Go to PubMed...
- Condell O, Sheridan Á, Power KA, Bonilla-Santiago R, Sergeant K, Renaut J, et al. (2012). Comparative proteomic analysis of Salmonella tolerance to the biocide active agent triclosan. J Proteomics 75(14): 4505-45019. DOI: 10.1016/j.jprot.2012.04.044.
Go to original source...
Go to PubMed...
- Erel O (2004). A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 37(4): 277-285. DOI: 10.1016/j.clinbiochem.2003.11.015.
Go to original source...
Go to PubMed...
- FDA/Food and Drug Administration (2019). Food additives permitted for direct addition to food for human consumption. U.S. [online] [cit. 2020-07-28]. Available at: https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFR Search.cfm?FR=172.515
- Giaouris E, Samoilis G, Chorianopoulos N, Ercolini D, Nychas GJ (2013). Differential protein expression patterns between planktonic and biofilm cells of Salmonella enterica serovar Enteritidis PT4 on stainless steel surface. Int J Food Microbiol 162(1): 105-113. DOI: 10.1016/j.ijfoodmicro.2012.12.023.
Go to original source...
Go to PubMed...
- Heras B, Shouldice SR, Totsika M, Scanlon MJ, Schembri MA, Martin JL (2009). DSB proteins and bacterial pathogenicity. Nat Rev Microbiol 7(3): 215-225. DOI: 10.1038/nrmicro2087.
Go to original source...
Go to PubMed...
- Heras B, Totsika M, Jarrott R, Shouldice SR, Guntar G, Achard MES, et al. (2010). Structural and functional characterization of three DsbA paralogues from Salmonella enterica serovar Typhimurium. J Biol Chem 285(24): 18423-18432. DOI: 10.1074/jbc.M110.101360.
Go to original source...
Go to PubMed...
- Jarrott R, Shouldice SR, Gunèar G, Totsika M, Schembri MA, Heras B (2010). Expression and crystallization of SeDsbA, SeDsbL and SeSrgA from Salmonella enterica serovar Typhimurium. Acta Cryst 66(5): 601-604. DOI: 10.1107/S1744309110011942.
Go to original source...
Go to PubMed...
- Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, et al. (2009). STRING 8 - A global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 37 (Suppl. 1): 1-73. DOI: 10.1093/nar/gkn760.
Go to original source...
Go to PubMed...
- Jesudhasan, PR, Cepeda, ML, Widmer, K, Dowd, SE, Soni KA, Hume ME, et al. (2010). Transcriptome analysis of genes controlled by luxS/autoinducer-2 in Salmonella enterica serovar Typhimurium. Foodborne Pathog Dis 7(4): 399-410. DOI: 10.1089=fpd.2009.0372.
Go to original source...
Go to PubMed...
- Jiang T, Li M (2013). Quorum sensing inhibitors: a patent overview. Expert Opin Ther Patents 23(7): 867-894. DOI: 10.1517/13543776.2013.779674.
Go to original source...
Go to PubMed...
- Kim YH, Lee Y, Kim S, Yeom J, Yeom S, Kim BS, et al. (2006). The role of periplasmic antioxidant enzymes (superoxide dismutase and thiol peroxidase) of the Shiga toxin-producing Escherichia coli O157:H7 in the formation of biofilms. Proteomics 6(23): 6181-6193. DOI: 10.1002/pmic.200600320.
Go to original source...
Go to PubMed...
- Knowles JR, Roller S, Murray DB, Naidu AS (2005.) Antimicrobial action of carvacrol at different stages of dual-species biofilm development by Staphylococcus aureus and Salmonella enterica serovar Typhimurium. Appl Environ Microbiol 71(2): 797-803. DOI: 10.1128/AEM.71.2.797-803.2005.
Go to original source...
Go to PubMed...
- Krishnakumar R, Craig M, Imlay JA, Slauch JM (2004). Differences in enzymatic properties allow SodCI but not SodCII to contribute to virulence in Salmonella enterica serovar Typhimurium strain 14028. J Bacteriol 186(16): 5230-5238. DOI: 10.1128/JB.00010-07.
Go to original source...
Go to PubMed...
- Lee Y, Kim Y, Yeom S, Kim S, Park S, Jeon CO, et al. (2008). The role of disulfide bond isomerase A (DsbA) of Escherichia coli O157:H7 in biofilm formation and virulence. FEMS Microbiol Lett 278(2): 213-222. DOI: 10.1111/j.1574-6968.2007.00993.x.
Go to original source...
Go to PubMed...
- Lee Y, Seo H, Yeom J, Park W (2011). Molecular characterization of the extracellular matrix in a Pseudomonas putida dsbA mutant: Implications for acidic stress defense and plant growth. Res Microbiol 162(3): 302-310. DOI: 10.1016/j.resmic.2010.11.002.
Go to original source...
Go to PubMed...
- Li YH, Tian X (2012). Quorum sensing and bacterial social interactions in biofilms. Sensors 12(3): 2519-2538. DOI: 10.3390/s120302519.
Go to original source...
Go to PubMed...
- Magalhães S, Aroso M, Roxo I, Ferreira S, Cerveira F, Ramalheira E, et al. (2017). Proteomic profile of susceptible and multidrug-resistant clinical isolates of Escherichia coli and Klebsiella pneumoniae using label-free and immunoproteomic strategies. Res Microbiol 168(3): 222-233. DOI: 10.1016/j.resmic.2016.12.002.
Go to original source...
Go to PubMed...
- Mangalappalli-Illathu AK, Korber DR (2006). Adaptive resistance and differential protein expression of Salmonella enterica serovar Enteritidis biofilms exposed to benzalkonium chloride. Antimicrob Agents Chemother 50(11): 3588-3596. DOI: 10.1128/AAC.00573-06.
Go to original source...
Go to PubMed...
- Mangalappalli-Illathu AK, Lawrence JR, Swerhone GDW, Korber DR (2008). Architectural adaptation and protein expression patterns of Salmonella enterica serovar Enteritidis biofilms under laminar flow conditions. Int J Food Microbiol 123(1-2): 109-120. DOI: 10.1016/j.ijfoodmicro.2007.12.021.
Go to original source...
Go to PubMed...
- McCord JM, Fridovich I (1969). Superoxide Dismutase An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244(25): 6049-1969.
Go to original source...
- Neuhoff V, Arold N, Taube D, Ehrhardt W (1988). Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9(6): 255-262. DOI: 10.1002/elps.1150090603.
Go to original source...
Go to PubMed...
- Nostro A, Marino A, Blanco AR, Cellini L, Giulio MD, Pizzimenti F, et al. (2009). In vitro activity of carvacrol against staphylococcal preformed biofilm by liquid and vapour contact. J Med Microbiol 58(6): 791-797. DOI: 10.1099/jmm.0.009274-0.
Go to original source...
Go to PubMed...
- Parsonage D, Karplus PA, Poole LB (2008). Substrate specificity and redox potential of AhpC, a bacterial peroxiredoxin. Proc Natl Acad Sci 105(24): 8209-8214. DOI: 10.1073_pnas.0708308105.
Go to original source...
Go to PubMed...
- Sharma P, Kumar B, Gupta Y, Singhal N, Katoch VW, Venkatesan K, et al. (2010). Proteomic analysis of streptomycin resistant and sensitive clinical isolates of Mycobacterium tuberculosis. Proteome Sci 8(1): 59. DOI: 10.1186/1477-5956-8-59.
Go to original source...
Go to PubMed...
- Shevchenko A, Wilm M, Vorm O, Mann M (1996). Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem 68(5): 850-858. DOI: 10.1021/ac950914h.
Go to original source...
Go to PubMed...
- Shouldice SR, Heras B, Walden PM, Totsika M, Schembri MA, Martin JL (2011). Structure and function of DsbA, a key bacterial oxidative folding catalyst. Antioxid Redox Signal 14(9): 1729-1760. DOI: 10.1089=ars.2010.3344.
Go to original source...
Go to PubMed...
- Silva AF, Santos AR, Trevisan DAC, Ribeiro AB, Campanerut-Sá PAZ, Kukolj C, et al. (2018). Cinnamaldehyde induces changes in the protein profile of Salmonella Typhimurium biofilm. Res Microbiol 169(1): 33-43. DOI: 10.1016/j.resmic.2017.09.007.
Go to original source...
Go to PubMed...
- Soares AA, Souza CGM, Daniel FM, Ferrari GP, Costa SMG, Peralta RM (2009). Antioxidant activity and total phenolic content of Agaricus brasiliensis (Agaricus blazei Murril) in two stages of maturity. Food Chem 112(4): 775-781. DOI: 10.1016/j.foodchem.2008.05.117.
Go to original source...
- Soni KA, Oladunjoye A, Nannapaneni R, Schilling MW, Silva JL, Mikel B, et al. (2013). Inhibition and inactivation of Salmonella Typhimurium biofilms from polystyrene and stainless steel surfaces by essential oils and phenolic constituent carvacrol. J Food Prot 76(2): 205-212. DOI: 10.4315/0362-028X.JFP- 12-196.
Go to original source...
Go to PubMed...
- Steenackers H, Hermans K, Vanderleyden J, De Keersmaecker SCJ (2012). Salmonella biofilms: An overview on occurrence, structure,regulation and eradication. Food Res Int 45(2): 502-531. DOI: 10.1016/j.foodres.2011.01.038.
Go to original source...
- Suo Y, Huang Y, Liu Y, Shi C, Shi X (2012). The expression of superoxide dismutase (SOD) and a putative ABC transporter permease is inversely correlated during biofilm formation in Listeria monocytogenes 4b G. PLoS One 7(10): e48467. DOI: 10.1371/journal.pone.0048467.
Go to original source...
Go to PubMed...
- Surette MG, Miller MB, Bassler BL (1999). Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc Natl Acad Sci U S A 96(4): 1639-1644. DOI: 10.1073/pnas.96.4.1639.
Go to original source...
Go to PubMed...
- Tapia-Rodriguez MR, Hernandez-Mendoza A, Gonzalez-Aguilar GA, Martinez-Tellez MA, Martins CM, Ayala-Zavala F (2017). Carvacrol as potential quorum sensing inhibitor of Pseudomonas aeruginosa and biofilm production on stainless steel surfaces. Food Control 75: 255-261. DOI: 10.1016/j.foodcont.2016.12.014.
Go to original source...
- Tomlinson IM, Holt LJ (2001). Protein profiling comes of age. Genome Biol 2(2). DOI: 10.1186/gb-2001-2-2-reviews1004.
Go to original source...
Go to PubMed...
- Trémoulet F, Duché O, Namane A, Martinie B (2002). Comparison of protein patterns of Listeria monocytogenes grown in biofilm or in planktonic mode by proteomic analysis. FEMS Microbiol Lett 210(1): 25-31. DOI: 10.1111/j.1574-6968.2002.tb11155.x.
Go to original source...
Go to PubMed...
- Trevisan DAC, Silva AF, Negri M, Abreu Filho BA, Machinski Junior M, Patussi EV, et al. (2018). Antibacterial and antibiofilm activity of carvacrol against Salmonella enterica serotype Typhimurium. Brazilian J Pharm Sci. 54(1): e17229. DOI: 10.1590/s2175-97902018000117229.
Go to original source...
- Uchida NS, Grespan R, Piovezan M, Ferreira EC, Machinski Junior M, Cuman RKN, et al. (2014). Effect of carvacrol on Salmonella Saintpaul biofilms on stainless steel surface. Trop J Pharm Res 14: 1075-1079. DOI: 10.4314/tjpr.v14i6.20.
Go to original source...
- Wagon S (1999). Mathematica in action - Problem Solving Through Visualization and Computation. Springer. Nova York (NY).
- Walsh DJ, Livinghouse T, Goeres DM, Mettler M, Stewart PS (2019). Antimicrobial Activity of Naturally Occurring Phenols and Derivatives against Biofilm and Planktonic Bacteria. Front Chem 7: 1-13. DOI: 10.3389/fchem.2019.00653.
Go to original source...
Go to PubMed...
- Wang H, Wang H, Xing T, Wu N, Xu X, Zhoug G (2016). Removal of Salmonella biofilm formed under meat processing environment by surfactant in combination with bio-enzyme. LWT - Food Sci Technol 66: 298-304. DOI: 10.1016/j.lwt.2015.10.049.
Go to original source...
- World Health Organization - WHO (2018). Salmonella. [online] [cit. 2018-04-14]. Available at: https://www.who.int/foodsafety/areas_work/foodborne-diseases/salmonella/en/
This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.