Inhibitory Effects of <i>Enterococcus faecalis</i> Z096 on Biofilm and Quorum Sensing of <i>Vibrio parahaemolyticus</i>

HAN Xiangpeng; CHEN Qingying; ZHANG Xingguo; HE Shuang; ZHONG Qingping

doi:10.13386/j.issn1002-0306.2021120291

Volume 43 Issue 19

Sep. 2022

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Science and Technology of Food Industry > 2022 > 43(19): 167-176. > DOI: 10.13386/j.issn1002-0306.2021120291

HAN Xiangpeng, CHEN Qingying, ZHANG Xingguo, et al. Inhibitory Effects of Enterococcus faecalis Z096 on Biofilm and Quorum Sensing of Vibrio parahaemolyticus[J]. Science and Technology of Food Industry, 2022, 43(19): 167−176. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2021120291.

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Inhibitory Effects of Enterococcus faecalis Z096 on Biofilm and Quorum Sensing of Vibrio parahaemolyticus

Guangdong Provincial Key Laboratory of Food Quality and Safety, College of Food Science, South China Agricultural University, Guangzhou 510642, China

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Received Date: December 26, 2021
Available Online: August 01, 2022

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Abstract

Abstract

To study the inhibitory effects of Enterococcus faecalis Z096 on the biofilm and quorum sensing (QS) system of Vibrio parahaemolyticus, the competition, elimination and exclusion were performed to simulate the interaction between Z096 and V. parahaemolyticus in microbial communities. In addition, the effects of Z096 extract (Z096-E) on V. parahaemolyticus biofilm formation, mature biofilm elimination, cell surface hydrophobicity, auto-aggregation, QS signal molecule AI-2 activity, motility ability (swarming and swimming), extracellular polysaccharide and protein synthesis were further explored. The results showed that Z096 could significantly reduce the number of V. parahaemolyticus cells in plankton and biofilm by competition, elimination and exclusion, and interfere with the adhesion of V. parahaemolyticus on the carrier surface. Moreover, Z096-E could significantly inhibit biofilm formation and effectively eliminate the mature biofilm of V. parahaemolyticus. When treated with 1.6 mg/mL of Z096-E for 12 h, the biofilm inhibition rate was 70.43%, and the metabolic activity decreased by 84.15%; When the mature biofilm of V. parahaemolyticus was treated with 12.8 mg/mL of Z096-E for 4 h, the biofilm removing rate was 58.21%, and the metabolic activity decreased by 69.84%. The swarming and swimming ability, cell surface hydrophobicity and auto-aggregation, extracellular polysaccharide and protein synthesis of V. parahaemolyticus were inhibited by 1.6 mg/mL of Z096-E by 47.26%, 53.56%, 63.37%, 89.38%, 77.65% and 51.91%, respectively, and the inhibitory effect was dose-dependent. In addition, Z096-E weakened the activity of QS signal molecule AI-2 of V. parahaemolyticus, indicating that Z096-E was an AI-2 quorum sensing inhibitor, which could affect the physiological characteristics of V. parahaemolyticus by interfering with the QS system. Therefore, we found one strain of lactic acid bacteria (LAB) that could inhibit V. parahaemolyticus biofilm, and the Z096-E could be used as a novel LAB-based biological agent to prevent and control V. parahaemolyticus biofilm. This study would be of positive significance to eliminate V. parahaemolyticus biofilm pollution and develop novel antibacterial agents.
- Enterococcus faecalis,
- Vibrio parahaemolyticus,
- inhibitory effects,
- biofilm,
- quorum sensing

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[1]	雷欢, 谢婷, 魏宇清, 等. 4种防腐剂对副溶血弧菌生物被膜形成的抑制作用[J]. 食品科学,2017,38(7):6−10. [LEI H, XIE T, WEI Y Q, et al. Inhibitory effects of four kinds of food preservatives on bioﬁlm formation by Vibrio parahaemolyticus[J]. Food Science,2017,38(7):6−10. doi: 10.7506/spkx1002-6630-201707002 LEI H, XIE T, WEI Y Q, et al. Inhibitory effects of four kinds of food preservatives on bioﬁlm formation by Vibrio parahaemolyticus[J]. Food Science, 2017, 38(7): 6-10. doi: 10.7506/spkx1002-6630-201707002
[2]	LETCHUMANAN V, CHAN K G, LEE L H. Vibrio parahaemolyticus: A review on the pathogenesis, prevalence, and advance molecular identification techniques[J]. Frontiers in Microbio-logy,2014,5:705.
[3]	张婷, 杨梦华. 副溶血弧菌的毒力基因表达调控的分子机制[J]. 微生物学报,2020,60(7):1345−1357. [ZHANG T, YANG M H. Molecular mechanisms of virulence genes expression in Vibrio parahaemolyticus[J]. Acta Microbiologica Sinica,2020,60(7):1345−1357. ZHANG T, YANG M H. Molecular mechanisms of virulence genes expression in Vibrio parahaemolyticus[J]. Acta Microbiologica Sinica, 2020, 60(7): 1345-1357.
[4]	ASHRAFUDOULIA M, MIZA M F R, PARK H, et al. Genetic relationship, virulence factors, drug resistance profile and biofilm formation ability of Vibrio parahaemolyticus isolated from mussel[J]. Frontiers in Microbiology,2019,10(513):1−14.
[5]	MIZAN M F, JAHID I K, HA S D. Microbial biofilms in seafood: A food-hygiene challenge[J]. Food Microbiol,2015,49:41−55. doi: 10.1016/j.fm.2015.01.009
[6]	XIE T, LIAO Z L, LEI H, et al. Antibacterial activity of food-grade chitosan against Vibrio parahaemolyticus biofilms[J]. Microbial Pathogenesis,2017,110:291−297. doi: 10.1016/j.micpath.2017.07.011
[7]	PANG X, WONG C, CHUNG H J, et al. Biofilm formation of Listeria monocytogenes and its resistance to quaternary ammonium compounds in a simulated salmon processing environment[J]. Food Control,2018,98:200−208.
[8]	PAPENFORT K, BASSLER B L. Quorum sensing signal-response systems in gram-negative bacteria[J]. Nature Reviews Microbiology,2016,14(9):576−588. doi: 10.1038/nrmicro.2016.89
[9]	WATERS C M, BASSLER B L. Quorum sensing: Cell-to-cell communication in bacteria[J]. Annual Review of Cell and Developmental Biology,2005,21(1):319−346. doi: 10.1146/annurev.cellbio.21.012704.131001
[10]	肖梦圆, 武瑞赟, 谭春明, 等. 群体感应系统及其抑制剂对细菌生物被膜调控的研究进展[J]. 食品科学,2020,41(13):227−234. [XIAO M Y, WU R Y, TAN C M, et al. Recent advances in understanding the role of quorum sensing system and quorum sensing inhibitors in regulating bacterial biofilm formation[J]. Food Science,2020,41(13):227−234. doi: 10.7506/spkx1002-6630-20200109-115 XIAO M Y, WU R Y, TAN C M, et al. Recent advances in understanding the role of quorum sensing system and quorum sensing inhibitors in regulating bacterial biofilm formation[J]. Food Science, 2020, 41(13): 227-234. doi: 10.7506/spkx1002-6630-20200109-115
[11]	ZHANG J, FENG T, WANG J, et al. The mechanisms and applications of quorum sensing (QS) and quorum quenching (QQ)[J]. Journal of Ocean University of China,2019,18(6):1427−1442. doi: 10.1007/s11802-019-4073-5
[12]	SIENKIEWICZ M, GLOWACKA A, KOWALCZYK E, et al. The biological activities of cinnamon, geranium and lavender essential oils[J]. Molecules, 19(12): 20929−20940.
[13]	杨晓萍, 陈梓琦, 钟先锋. 乳酸菌的分离鉴定方法及益生功能应用研究[J]. 农产品加工,2020(7):50−54. [YANG X P, CHEN Z Q, ZHONG X F. Advances in the isolation and identification of lactic acid bacteria and the application of probiotics[J]. Farm Products Processing,2020(7):50−54. YANG X P, CHEN Z Q, ZHONG X F. Advances in the isolation and identification of lactic acid bacteria and the application of probiotics[J]. Farm Products Processing, 2020(7): 50-54.
[14]	上官文丹, 陈可, 陈清莹, 等. 戊糖乳杆菌DF9对副溶血弧菌群体感应的淬灭作用[J]. 食品工业科技,2022,43(6):126−132. [SHANGGUAN W D, CHEN K, CHEN Q Y, et al. Quenching effects of Lactobacillus pentosus DF9 on quorum sensing of Vibrio parahaemolyticus[J]. Science and Technology of Food Industry,2022,43(6):126−132. doi: 10.13386/j.issn1002-0306.2021070267 SHANGGUAN W D, CHEN K, CHEN Q Y, et al. Quenching effects of Lactobacillus pentosus DF9 on quorum sensing of Vibrio parahaemolyticus[J]. Science and Technology of Food Industry, 2022, 43(6): 126-132. doi: 10.13386/j.issn1002-0306.2021070267
[15]	YAN X, GU S S, CUI X Y, et al. Antimicrobial, anti-adhesive and anti-biofilm potential of biosurfactants isolated from Pediococcus acidilactici and Lactobacillus plantarum against Staphylococcus aureus CMCC26003[J]. Microbial Pathogenesis,2019,127:12−20. doi: 10.1016/j.micpath.2018.11.039
[16]	黄湘湄, 吴雅茜, 刘颖, 等. 海洋源乳酸菌AI-2类群体感应抑制剂对单增李斯特菌抑制效果研究[J]. 生物技术通报,2019,35(4):36−42. [HUANG X M, WU Y Q, LIU Y, et al. Inhibitory effects of AI-2 quorum sensing inhibitors from marine lactic acid bacteria on Listeria monocytogenes[J]. Biotechnology Bulletin,2019,35(4):36−42. HUANG X M, WU Y Q, LIU Y, et al. Inhibitory effects of AI-2 quorum sensing inhibitors from marine lactic acid bacteria on Listeria monocytogenes[J]. Biotechnology Bulletin, 2019, 35(4): 36-42.
[17]	MARIANA P I, PATRICIA C, ALEXANDRE L, et al. Control of Listeria monocytogenes biofilms on industrial surfaces by the bacteriocin-producing Lactobacillus sakei CRL1862[J]. FEMS Microbiology Letters,2016,363(12):118−124. doi: 10.1093/femsle/fnw118
[18]	WOO J, AHN J. Probiotic-mediated competition, exclusion and displacement in biofilm formation by food-borne pathogens[J]. Letters in Applied Microbiology,2013,56(4):307−320. doi: 10.1111/lam.12051
[19]	SALAHEEN S, NGUYEN C, HEWES D, et al. Cheap extraction of antibacterial compounds of berry pomace and their mode of action against the pathogen Campylobacter jejuni[J]. Food Control,2014,46:174−181. doi: 10.1016/j.foodcont.2014.05.026
[20]	燕彩玲, 李博, 顾悦, 等. 信号分子AI-2的检测方法研究进展[J]. 微生物学通报,2016,43(6):1333−1338. [YAN C L, LI B, GU Y, et al. Methods for the determination of autoinducer-2-a review[J]. Microbiology China,2016,43(6):1333−1338. YAN C L, LI B, GU Y, et al. Methods for the determination of autoinducer-2-a review[J]. Microbiology China, 2016, 43(6): 1333-1338
[21]	ZHANG C H, LI C Z, ABDEL-SAMIE M A, et al. Unraveling the inhibitory mechanism of clove essential oil against Listeria monocytogenes biofilm and applying it to vegetable surfaces[J]. LWT-Food Science and Technology,2020,134:110210−110219. doi: 10.1016/j.lwt.2020.110210
[22]	SHANGGUAN W D, XIE T, ZHANG R, et al. Anti-biofilm potential of kefir-derived Lactobacillus paracasei L10 against Vibrio parahaemolyticus[J]. Letters in Applied Microbiology,2021,73:750−758. doi: 10.1111/lam.13568
[23]	WASFI R, EL-RAHMAN O A A, ZAFER M M, et al. Probiotic Lactobacillus sp. inhibit growth, biofilm formation and gene expression of caries-inducing Streptococcus mutans[J]. Journal of Cellular and Molecular Medicine,2018,22:1972−1983. doi: 10.1111/jcmm.13496
[24]	ZHANG Y, LIU H, GU D, et al. Transcriptomic analysis of PhoR reveals its role in regulation of swarming motility and T3SS expression in Vibrio parahaemolyticus[J]. Microbiological Research,2020,235:126448. doi: 10.1016/j.micres.2020.126448
[25]	宋杏, 尤宏, 李福赞, 等. 植物乳杆菌Y42无细胞培养上清抑制单增李斯特菌生物膜形成研究[J]. 食品科学技术学报,2018,36(2):35−41. [SONG X, YOU H, LI F Z, et al. Effects of Lactobacillus plantarum Y42 cell-free culture supernatant on Listeria monocytogenes biofilm formation[J]. Journal of Food Science and Technology,2018,36(2):35−41. doi: 10.3969/j.issn.2095-6002.2018.02.005 SONG X, YOU H, LI F Z, et al. Effects of Lactobacillus plantarum Y42 cell-free culture supernatant on Listeria monocytogenes biofilm formation[J]. Journal of Food Science and Technology, 2018, 36(2): 35-41. doi: 10.3969/j.issn.2095-6002.2018.02.005
[26]	SALAHEEN S, JAISWAL E, JOO J, et al. Bioactive extracts from berry byproducts on the pathogenicity of Salmonella typhimurium[J]. International Journal of Food Microbiology,2016,237:128−135. doi: 10.1016/j.ijfoodmicro.2016.08.027
[27]	宋莹龙, 梁雪, 宋杏, 等. Lactobacillus plantarum-12胞外多糖抑制志贺氏菌生物膜形成的研究[J]. 食品研究与开发,2018,39(8):144−151. [SONG Y L, LIANG X, SONG X, et al. The study on the inhibition of Shigella biofilm formation by the exopolysaccharides of Lactobacillus plantarum-12[J]. Food Research and Development,2018,39(8):144−151. doi: 10.3969/j.issn.1005-6521.2018.08.025 SONG Y L, LIANG X, SONG X, et al. The study on the inhibition of Shigella biofilm formation by the exopolysaccharides of Lactobacillus plantarum-12[J]. Food Research and Development, 2018, 39(8): 144-151]. doi: 10.3969/j.issn.1005-6521.2018.08.025
[28]	蒋富凤, 雷涛, 吴清平, 等. 副溶血性弧菌生物被膜形成及其调控机制研究进展[J]. 微生物学报,2020,60(11):2381−2390. [JIANG F F, LEI T, WU Q P, et al. Biofilm formation and regulation mechanism of Vibrio parahaemolyticus: Progress and trends[J]. Acta Microbiologica Sinica,2020,60(11):2381−2390. JIANG F F, LEI T, WU Q P, et al. Biofilm formation and regulation mechanism of Vibrio parahaemolyticus: Progress and trends[J]. Acta Microbiologica Sinica, 2020, 60(11): 2381-2390].
[29]	PELYUNTHA W, CHAIYASUT C, KANTACHOTE D, et al. Cell-free supernatants from cultures of lactic acid bacteria isolated from fermented grape as biocontrol against Salmonella typhi and Salmonella typhimurium virulence via autoinducer-2 and biofilm interference[J]. Peer J,2019,7:7555−75565. doi: 10.7717/peerj.7555
[30]	BRINDHADEVI K, LEWISOSCAR F, MYLONAKIS E, et al. Biofilm and quorum sensing mediated pathogenicity in Pseudomonas aeruginosa[J]. Process Biochemistry,2020,96:49−57. doi: 10.1016/j.procbio.2020.06.001
[31]	YILDIZ F H, FONG J N C. Biofilm matrix proteins[J]. Microbiol Spectr,2015,3(2):10−26.
[32]	ONBAS T, OSMANAGAOGLU O, KIRAN F. Potential properties of Lactobacillus plantarum F-10 as a bio-control strategy for wound infections[J]. Probiotics and Antimicrobial Proteins,2019,11:1110−1123. doi: 10.1007/s12602-018-9486-8
[33]	RATTI R P, GOMES B C, MARTINEZ R C R, et al. Elongated cells of Listeria monocytogenes in biofilms in the presence of sucrose and bacteriocin-producing Leuconostoc mesenteroides A11[J]. Food Science and Technology (Campinas),2010,30:1011−1017. doi: 10.1590/S0101-20612010000400027
[34]	WINKELSTROTER L K, GOMES B C, THOMAZ M R S, et al. Lactobacillus sakei 1 and its bacteriocin influence adhesion of Listeria monocytogenes on stainless steel surface[J]. Food Control,2011,22:1404−1411. doi: 10.1016/j.foodcont.2011.02.021
[35]	LERICHE V, CARPENTIER B. Limitation of adhesion and growth of Listeria monocytogenes on stainless steel surfaces by Staphylococcus sciuri biofilms[J]. Journal of Applied Microbiology,2000,88:594−605. doi: 10.1046/j.1365-2672.2000.01000.x
[36]	TAHMOURESPOUR A, KERMANSHAHI R K. The effect of a probiotic strain (Lactobacillus acidophilus) on the plaque formation of oral streptococci[J]. Bosnian Journal of Basic Medical Sciences,2011,11:37−40. doi: 10.17305/bjbms.2011.2621
[37]	姚沛琳, 王剑, 张新剑, 等. 对大肠杆菌生物被膜具有高抑制能力的乳酸菌的筛选[J]. 食品与发酵工业,2019,45(6):59−64. [YAO P L, WANG J, ZHANG X J, et al. Screening of lactic acid bacteria with strong inhibitory effects on Escherichia coli biofilm formation[J]. Food and Fermentation Industries,2019,45(6):59−64. YAO P L, WANG J, ZHANG X J, et al. Screening of lactic acid bacteria with strong inhibitory effects on Escherichia coli biofilm formation[J]. Food and Fermentation Industries, 2019, 45(6): 59-64.
[38]	GIORDANI B, COSTANTINI P E, FEDI S, et al. Liposomes containing biosurfactants isolated from Lactobacillus gasseri exert antibiofilm activity against methicillin resistant Staphylococcus aureus strains[J]. European Journal of Pharmaceutics and Biopharmaceutics,2019,139:246−252. doi: 10.1016/j.ejpb.2019.04.011
[39]	PRADEEP A, SHETTY A D, MATTHEWS K, et al. Multidrug resistant pathogenic bacterial biofilm inhibition by Lactobacillus plantarum exopolysaccharide[J]. Bioactive Carbohydrates and Dietary Fibre,2016,8(1):7−14. doi: 10.1016/j.bcdf.2016.06.002
[40]	WANG N, YUAN L, SADIQ F A, et al. Inhibitory effect of Lactobacillus plantarum metabolites against biofilm formation by Bacillus licheniformis isolated from milk powder products[J]. Food Control,2019,106:106721−106732. doi: 10.1016/j.foodcont.2019.106721
[41]	CUI T Q, BAI F L, SUN M T, et al. Lactobacillus crustorum ZHG 2-1 as novel quorum-quenching bacteria reducing virulence factors and biofilms formation of Pseudomonas aeruginosa[J]. LWT-Food Science and Technology,2020,117:108696−108704. doi: 10.1016/j.lwt.2019.108696
[42]	MELIAN C, SEGLI F, GONZALEZ R, et al. Lactocin AL705 as quorum sensing inhibitor to control Listeria monocytogenes biofilm formation[J]. Journal of applied microbiology,2019,127(3):1−10.

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