Inhibitory effects of Flavourzyme on biofilm formation, quorum sensing, and virulence genes of foodborne pathogens Salmonella Typhimurium and Escherichia coli

Food Research International - Tập 147 - Trang 110461 - 2021
Shamsun Nahar1, Ha Lim Jeong1, Younsoo Kim1, Angela Jie-won Ha1, Pantu Kumar Roy1, Si Hong Park2, Md. Ashrafudoulla1, Md. Furkanur Rahaman Mizan1, Sang-Do Ha1
1Department of Food Science and Technology, Chung-Ang University, Anseong, Gyeonggi-do 17546, Republic of Korea
2Department of Food Science & Technology, Oregon State University, Corvallis, OR, USA

Tài liệu tham khảo

Absalon, 2011, A communal bacterial adhesin anchors biofilm and bystander cells to surfaces, PLoS Pathogens, 7, 10.1371/journal.ppat.1002210 Adcox, 2016, Salmonella extracellular matrix components influence biofilm formation and gallbladder colonization, Infection and Immunity, 84, 3243, 10.1128/IAI.00532-16 Ali Mohammed, 2013, Characterization of extracellular polymeric matrix, and treatment of Fusobacterium nucleatum and Porphyromonas gingivalis biofilms with DNase I and proteinase K, Journal of Oral Microbiology, 5, 20015, 10.3402/jom.v5i0.20015 Bahulikar, 2007, Localization of EPS components secreted by freshwater diatoms using differential staining with fluorophore-conjugated lectins and other fluorochromes, European Journal of Phycology, 42, 199, 10.1080/09670260701289779 Baidamshina, 2017, Targeting microbial biofilms using Ficin, a nonspecific plant protease, Scientific Reports, 7, 46068, 10.1038/srep46068 Bansal, 2019, Rugose morphotype in Salmonella Typhimurium and Salmonella Heidelberg induced by sequential exposure to subinhibitory sodium hypochlorite aids in biofilm tolerance to lethal sodium hypochlorite on polystyrene and stainless steel surfaces, Frontiers in Microbiology, 10, 2704, 10.3389/fmicb.2019.02704 Bassler, 1993, Intercellular signalling in Vibrio harveyi: Sequence and function of genes regulating expression of luminescence, Molecular Microbiology, 9, 773, 10.1111/j.1365-2958.1993.tb01737.x Center for Disease Control and Prevention. (2020, March 18). Food safety. https://www.cdc.gov/foodsafety/foodborne-germs.html#:~:text=Some%20Common%20Foodborne%20Germs&text=Salmonella,Staphylococcus%20aureus%20(Staph). Chen, 2013, Quorum quenching enzymes and their application in degrading signal molecules to block quorum sensing-dependent infection, International Journal of Molecular Sciences, 14, 17477, 10.3390/ijms140917477 Choi, 2007, Implication of quorum sensing in Salmonella enterica serovar Typhimurium virulence: The luxS gene is necessary for expression of genes in pathogenicity island 1, Infection and Immunity, 75, 4885, 10.1128/IAI.01942-06 Clinical and Laboratory Standards Institute. (2016). Performance standards for antimicrobial susceptibility testing—26th edition (CLSI document M100-S26). CLSI. De Keersmaecker, 2006, Let LuxS speak up in AI-2 signaling, Trends in Microbiology, 14, 114, 10.1016/j.tim.2006.01.003 Dong, 2009, Global effect of RpoS on gene expression in pathogenic Escherichia coli O157:H7 strain EDL933, BMC Genomics, 10, 349, 10.1186/1471-2164-10-349 Dong, 2005, Quorum sensing and quorum-quenching enzymes, Journal of Microbiology, 43, 101 Elchinger, 2014, Effect of proteases against biofilms of Staphylococcus aureus and Staphylococcus epidermidis, Letters in Applied Microbiology, 59, 507, 10.1111/lam.12305 Galié, 2018, Biofilms in the food industry: Health aspects and control methods, Frontiers in Microbiology, 9, 898, 10.3389/fmicb.2018.00898 Gu, 2019, Alternative sigma factor RpoX is a part of the RpoE regulon and plays distinct roles in stress responses, motility, biofilm formation, and hemolytic activities in the marine pathogen Vibrio alginolyticus, Applied and Environmental Microbiology, 85, e00234, 10.1128/AEM.00234-19 Han, 2015, Deletion of luxS further attenuates the virulence of the avian pathogenic Escherichia coli aroA mutant, Microbial Pathogenesis, 88, 39, 10.1016/j.micpath.2015.08.003 Harrison, 2010, Microtiter susceptibility testing of microbes growing on peg lids: A miniaturized biofilm model for high-throughput screening, Nature Protocols, 5, 1236, 10.1038/nprot.2010.71 Koo, 2017, Targeting microbial biofilms: Current and prospective therapeutic strategies, Nature Reviews Microbiology, 15, 740, 10.1038/nrmicro.2017.99 Kragh, 2019, Into the well—A close look at the complex structures of a microtiter biofilm and the crystal violet assay, Biofilm, 1, 10.1016/j.bioflm.2019.100006 Laganenka, 2018, Autoinducer 2-dependent Escherichia coli biofilm formation is enhanced in a dual-species coculture, Applied and Environmental Microbiology, 84, e02638, 10.1128/AEM.02638-17 Lei, 2019, Biofilm bridges forming structural networks on patterned lubricant-infused surfaces, Advanced Science, 6, 1900519, 10.1002/advs.201900519 Lequette, 2010, Using enzymes to remove biofilms of bacterial isolates sampled in the food-industry, Biofouling, 26, 421, 10.1080/08927011003699535 Lévi-Meyrueis, 2014, Expanding the RpoS/σS-network by RNA sequencing and identification of σS-controlled small RNAs in Salmonella, PLoS ONE, 9, 10.1371/journal.pone.0096918 Lim, 2019, Bio-enzymes for inhibition and elimination of Escherichia coli O157:H7 biofilm and their synergistic effect with sodium hypochlorite, Scientific Reports, 9, 9920, 10.1038/s41598-019-46363-w Liu, 2019, Inhibitory effects of two types of food additives on biofilm formation by foodborne pathogens, MicrobiologyOpen, 8, 10.1002/mbo3.853 López-Pedrouso, 2020, Antioxidant activity and peptidomic analysis of porcine liver hydrolysates using alcalase, bromelain, flavourzyme and papain enzymes, Food Research International, 137, 10.1016/j.foodres.2020.109389 Maciel, 2018, Application of multiplex real-time polymerase chain reaction assay for simultaneous quantification of Escherichia coli virulence genes in oysters, Journal of Food Science and Technology-Mysore, 55, 2765, 10.1007/s13197-018-3200-4 Merz, 2016, Batch-to-batch variation and storage stability of the commercial peptidase preparation Flavourzyme in respect of key enzyme activities and its influence on process reproducibility, European Food Research and Technology, 242, 1005, 10.1007/s00217-015-2606-8 Merz, 2015, Flavourzyme, an enzyme preparation with industrial relevance: Automated nine-step purification and partial characterization of eight enzymes, Journal of Agricultural and Food Chemistry, 63, 5682, 10.1021/acs.jafc.5b01665 Merz, 2015, Wheat gluten hydrolysis using isolated Flavourzyme peptidases: Product inhibition and determination of synergistic effects using response surface methodology, Journal of Molecular Catalysis B-Enzymatic, 122, 218, 10.1016/j.molcatb.2015.09.010 Mizan, 2017, Molecular characteristics, biofilm-forming abilities, and quorum sensing molecules in Vibrio parahaemolyticus strains isolated from marine and clinical environments in Korea, Biofouling, 33, 369, 10.1080/08927014.2017.1316840 Nagar, 2015, Diverse profiles of N-acyl homoserine L-lactones, biofilm, virulence genes and integrons in food-borne Aeromonas isolates, Journal of Food Science, 80, M1861, 10.1111/1750-3841.12949 Nahar, 2021, Efficacy of flavourzyme against Salmonella Typhimurium, Escherichia coli, and Pseudomonas aeruginosa biofilms on food-contact surfaces, International Journal of Food Microbiology, 336, 10.1016/j.ijfoodmicro.2020.108897 Nahar, 2018, Advances and future prospects of enzyme-based biofilm prevention approaches in the food industry, Comprehensive Reviews in Food Science and Food Safety, 17, 1484, 10.1111/1541-4337.12382 Nguyen, 2014, DNase I and proteinase K impair Listeria monocytogenes biofilm formation and induce dispersal of pre-existing biofilms, International Journal of Food Microbiology, 187, 26, 10.1016/j.ijfoodmicro.2014.06.025 Niu, 2013, LuxS influences Escherichia coli biofilm formation through autoinducer-2-dependent and autoinducer-2-independent modalities, FEMS Microbiology Ecology, 83, 778, 10.1111/1574-6941.12034 Paluch, 2020, Prevention of biofilm formation by quorum quenching, Applied Microbiology and Biotechnology, 104, 1871, 10.1007/s00253-020-10349-w Park, 2016, Antimicrobial effects of vinegar against norovirus and Escherichia coli in the traditional Korean vinegared green laver (Enteromorpha intestinalis) salad during refrigerated storage, International Journal of Food Microbiology, 238, 208, 10.1016/j.ijfoodmicro.2016.09.002 Peng, 2018, Rutin inhibits quorum sensing, biofilm formation and virulence genes in avian pathogenic Escherichia coli, Microbial Pathogenesis, 119, 54, 10.1016/j.micpath.2018.04.007 Sadekuzzaman, 2018, Activity of thyme and tea tree essential oils against selected foodborne pathogens in biofilms on abiotic surfaces, LWT, 89, 134, 10.1016/j.lwt.2017.10.042 Sadekuzzaman, 2017, Effectiveness of a phage cocktail as a biocontrol agent against L. monocytogenes biofilms, Food Control, 78, 256, 10.1016/j.foodcont.2016.10.056 Sharahi, 2019, Advanced strategies for combating bacterial biofilms, Journal of Cellular Physiology, 234, 14689, 10.1002/jcp.28225 Shi, 2018, Combination of berberine and ciprofloxacin reduces multi-resistant Salmonella strain biofilm formation by depressing mRNA expressions of luxS, rpoE, and ompR, Journal of Veterinary Science, 19, 808, 10.4142/jvs.2018.19.6.808 Shukla, 2017, Staphylococcus aureus biofilm removal by targeting biofilm-associated extracellular proteins, Indian Journal of Medical Research, 146, S1 Shukla, 2017, An improved crystal violet assay for biofilm quantification in 96-well microtitre plate, Biorxiv, 100214 Song, 2014, Determination of autoinducer-2 in biological samples by high-performance liquid chromatography with fluorescence detection using pre-column derivatization, Journal of Chromatography A, 1361, 162, 10.1016/j.chroma.2014.07.103 Soni, 2008, Autoinducer AI-2 is involved in regulating a variety of cellular processes in Salmonella Typhimurium, Foodborne Pathogens and Disease, 5, 147, 10.1089/fpd.2007.0050 Soni, 2013, Inhibition and inactivation of Salmonella Typhimurium biofilms from polystyrene and stainless steel surfaces by essential oils and phenolic constituent carvacrol, Journal of Food Protection, 76, 205, 10.4315/0362-028X.JFP-12-196 Stiefel, 2016, Is biofilm removal properly assessed? Comparison of different quantification methods in a 96-well plate system, Applied Microbiology and Biotechnology, 100, 4135, 10.1007/s00253-016-7396-9 Wasfi, 2016, Effects of selected Egyptian honeys on the cellular ultrastructure and the gene expression profile of Escherichia coli, PloS ONE, 11, 10.1371/journal.pone.0150984 WHO. (2018a, February 7). Newsroom. Fact sheets. Detail. E. coli. https://www.who.int/news-room/fact-sheets/detail. WHO. (2018b, June 2). Newsroom. Fact sheets. Detail. Salmonella (non-typhoidal). https://www.who.int/news-room/fact-sheets/detail. Yang, 2014, Growth temperature alters Salmonella Enteritidis heat/acid resistance, membrane lipid composition and stress/virulence related gene expression, International Journal of Food Microbiology, 172, 102, 10.1016/j.ijfoodmicro.2013.12.006 Yin, 2011, Differential gene expression and adherence of Escherichia coli O157:H7 in vitro and in ligated pig intestines, PLoS ONE, 6, 10.1371/journal.pone.0017424 Zhang, 2019, The AI-2/luxS quorum sensing system affects the growth characteristics, biofilm formation, and virulence of Haemophilus parasuis, Frontiers in Cellular and Infection Microbiology, 9, 62, 10.3389/fcimb.2019.00062 Zhang, 2017, Effect of Flavourzyme on proteolysis, antioxidant activity and sensory qualities of Cantonese bacon, Food Chemistry, 237, 779, 10.1016/j.foodchem.2017.06.026 Zhao, 2017, Biofilm formation and control strategies of foodborne pathogens: Food safety perspectives, RSC Advances, 7, 36670, 10.1039/C7RA02497E