Research progress of quorum sensing in fermented foods

  • WANG Wenyue ,
  • YU Fan ,
  • YI Chi ,
  • ZHANG Lin ,
  • XIAO Ke ,
  • FAN Xin ,
  • XIAO Junfeng ,
  • ZHU Xiaoqing ,
  • MU Yang ,
  • WANG Chao ,
  • ZHOU Mengzhou
Expand
  • (Key Laboratory of Fermentation Engineering (Ministry of Education), Hubei Collaboration Innovation Center of Industrial Fermentation, National “111” Center for Cellular Regulation and Molecular Pharmaceutics, Hubei University of Technology, Wuhan 430068, China)

Received date: 2023-04-20

  Revised date: 2023-05-23

  Online published: 2024-04-17

Abstract

Microorganisms play an important role in fermented foods.As a mechanism to regulate the physiological behavior of microorganisms depending on cell density, quorum sensing (QS) should also be of interest in fermented foods.In recent years, studies have shown that the regulation of quorum sensing in fermented foods is closely related to food quality and flavor.Therefore, this study try to elucidate the definition and classification of quorum sensing molecules (QSMs) and the regulatory effect of quorum sensing on microorganisms and various fermented foods in fermentation systems.Finally, the research and application prospect of quorum sensing in fermented food industry are summarized and prospected, aiming to provide new insights for fermented food industry.

Cite this article

WANG Wenyue , YU Fan , YI Chi , ZHANG Lin , XIAO Ke , FAN Xin , XIAO Junfeng , ZHU Xiaoqing , MU Yang , WANG Chao , ZHOU Mengzhou . Research progress of quorum sensing in fermented foods[J]. Food and Fermentation Industries, 2024 , 50(6) : 290 -299 . DOI: 10.13995/j.cnki.11-1802/ts.035890

References

[1] KEMPNER E S, HANSON F E. Aspects of light production by Photobacterium fischeri[J]. Journal of Bacteriology, 1968, 95(3):975-979.
[2] FUQUA W C, WINANS S C, GREENBERG E P. Quorum sensing in bacteria: The LuxR-LuxI family of cell density-responsive transcriptional regulators[J]. Journal of Bacteriology, 1994, 176(2):269-275.
[3] MUKHERJEE S, BASSLER B L. Bacterial quorum sensing in complex and dynamically changing environments[J]. Nature Reviews. Microbiology, 2019, 17(6):371-382.
[4] 李彩艳, 梁志宏. 细菌和真菌群体感应研究进展[J]. 延安大学学报(自然科学版), 2016, 35(2):39-44.
LI C Y, LIANG Z H. Research progress on quorum sensing in bacteria and fungi[J]. Journal of Yanan University (Natural Science Edition), 2016, 35(2):39-44.
[5] BAI A J, RAI V R. Bacterial quorum sensing and food industry[J]. Comprehensive Reviews in Food Science and Food Safety, 2011, 10(3):183-193.
[6] ALBUQUERQUE P, CASADEVALL A. Quorum sensing in fungi-a review[J]. Medical Mycology, 2012, 50(4):337-345.
[7] MONDS R D, O’TOOLE G A. Metabolites as Intercellular Signals for Regulation of Community-Level Traits[M]. Washington, DC, USA: ASM Press, 2014:105-129.
[8] WINZER K, HARDIE K R, BURGESS N, et al. LuxS: Its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone[J]. Microbiology, 2002, 148(Pt 4):909-922.
[9] WINTERS M, ARNEBORG N, APPELS R, et al. Can community-based signalling behaviour in Saccharomyces cerevisiae be called quorum sensing? A critical review of the literature[J]. FEMS Yeast Research, 2019, 19(5): foz046.
[10] NEALSON K H, PLATT T, HASTINGS J W. Cellular control of the synthesis and activity of the bacterial luminescent system[J]. Journal of Bacteriology, 1970, 104(1):313-322.
[11] KUMAR L, PATEL S K S, KHARGA K, et al. Molecular mechanisms and applications of N-acyl homoserine lactone-mediated quorum sensing in bacteria[J]. Molecules, 2022, 27(21):7584.
[12] MCBRAYER D N, CAMERON C D, TAL-GAN Y. Development and utilization of peptide-based quorum sensing modulators in Gram-positive bacteria[J]. Organic & Biomolecular Chemistry, 2020, 18(37):7273-7290.
[13] PENG P, BALDRY M, GLESS B H, et al. Effect of co-inhabiting coagulase negative staphylococci on S. aureus agr quorum sensing, host factor binding, and biofilm formation[J]. Frontiers in Microbiology, 2019, 10:2212.
[14] 韩翔鹏, 上官文丹, 李尧, 等. 细菌群体感应系统调控及淬灭机制研究进展[J]. 中国食品学报, 2022, 22(2):390-401.
HAN X P, SHANGGUAN W D, LI Y, et al. Research progress on the regulation and quenching mechanisms of bacterial quorum sensing system[J]. Journal of Chinese Institute of Food Science and Technology, 2022, 22(2):390-401.
[15] JOHANSEN P, JESPERSEN L. Impact of quorum sensing on the quality of fermented foods[J]. Current Opinion in Food Science, 2017, 13:16-25.
[16] HE Y W, DENG Y Y, MIAO Y S, et al. DSF-family quorum sensing signal-mediated intraspecies, interspecies, and inter-Kingdom communication[J]. Trends in Microbiology, 2023, 31(1):36-50.
[17] 励建荣, 李婷婷, 王当丰. 微生物群体感应系统及其在现代食品工业中应用的研究进展[J]. 食品科学技术学报, 2020, 38(1):1-11.
LI J R, LI T T, WANG D F. Research progress on microbial quorum sensing system and its application in modern food industry[J]. Journal of Food Science and Technology, 2020, 38(1):1-11.
[18] 高婧, 彭梦雪, 梁志宏. 真菌群体感应信号分子及群体感应猝灭的研究进展[J]. 生物加工过程, 2020, 18(2):214-223.
GAO J, PENG M X, LIANG Z H. Research progress of quorum sensing signal molecules and quorum sensing quenching in fungi[J]. Chinese Journal of Bioprocess Engineering, 2020, 18(2):214-223.
[19] 柯慧慧, 牛永武, 顾頔, 等. 真菌群体感应分子法尼醇及其作用机制[J]. 食品安全质量检测学报, 2017, 8(3):862-868.
KE H H, NIU Y W, GU D, et al. Quorum sensing molecule, farnesol and its action mechanism in fungi[J]. Journal of Food Safety & Quality, 2017, 8(3):862-868.
[20] AHMAD PADDER S, PRASAD R, SHAH A H. Quorum sensing: A less known mode of communication among fungi[J]. Microbiological Research, 2018, 210:51-58.
[21] LOREK J, PÖGGELER S, WEIDE M R, et al. Influence of farnesol on the morphogenesis of Aspergillus niger[J]. Journal of Basic Microbiology, 2008, 48(2):99-103.
[22] DE A CORDEIRO R, TEIXEIRA C E C, BRILHANTE R S N, et al. Exogenous tyrosol inhibits planktonic cells and biofilms of Candida species and enhances their susceptibility to antifungals[J]. FEMS Yeast Research, 2015, 15(4): fov012.
[23] GORI K, KNUDSEN P B, NIELSEN K F, et al. Alcohol-based quorum sensing plays a role in adhesion and sliding motility of the yeast Debaryomyces hansenii[J]. FEMS Yeast Research, 2011, 11(8):643-652.
[24] CHEN H, FUJITA M, FENG Q H, et al. Tyrosol is a quorum-sensing molecule in Candida albicans[J]. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(14):5048-5052.
[25] ZHANG D L, WANG F J, YU Y, et al. Effect of quorum-sensing molecule 2-phenylethanol and ARO genes on Saccharomyces cerevisiae biofilm[J]. Applied Microbiology and Biotechnology, 2021, 105(9):3635-3648.
[26] MARTINS M, HENRIQUES M, AZEREDO J, et al. Morphogenesis control in Candida albicans and Candida dubliniensis through signaling molecules produced by planktonic and biofilm cells[J]. Eukaryotic Cell, 2007, 6(12):2429-2436.
[27] CHEN W Y, LI C, ZHANG B Y, et al. Advances in biodetoxification of ochratoxin A-a review of the past five decades[J]. Frontiers in Microbiology, 2018, 9:1386.
[28] LIU P, FANG J F, CHEN K, et al. Phenylethanol promotes adhesion and biofilm formation of the antagonistic yeast Kloeckera apiculata for the control of blue mold on citrus[J]. FEMS Yeast Research, 2014, 14(4):536-546.
[29] TSITSIGIANNIS D I, ZARNOWSKI R, KELLER N P. The lipid body protein, PpoA, coordinates sexual and asexual sporulation in Aspergillus nidulans[J]. Journal of Biological Chemistry, 2004, 279(12):11344-11353.
[30] SORRENTINO F, ROY I, KESHAVARZ T. Impact of linoleic acid supplementation on lovastatin production in Aspergillus terreus cultures[J]. Applied Microbiology and Biotechnology, 2010, 88(1):65-73.
[31] SEBOLAI O M, POHL C H, BOTES P J, et al. 3-hydroxy fatty acids found in capsules of Cryptococcus neoformans[J]. Canadian Journal of Microbiology, 2007, 53(6):809-812.
[32] HOROWITZ BROWN S, ZARNOWSKI R, SHARPEE W C, et al. Morphological transitions governed by density dependence and lipoxygenase activity in Aspergillus flavus[J]. Applied and Environmental Microbiology, 2008, 74(18):5674-5685.
[33] KÜGLER S, SCHURTZ SEBGHATI T, GROPPE EISSENBERG L, et al. Phenotypic variation and intracellular parasitism by histoplasma Capsulatum[J]. Proceedings of the National Academy of Sciences of the United States of America, 2000, 97(16):8794-8798.
[34] SPRAGUE G F Jr, WINANS S C. Eukaryotes learn how to count: Quorum sensing by yeast[J]. Genes & Development, 2006, 20(9):1045-1049.
[35] RAPPLEYE C A, EISSENBERG L G, GOLDMAN W E. Histoplasma capsulatum alpha-(1, 3)-glucan blocks innate immune recognition by the beta-glucan receptor[J]. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(4):1366-1370.
[36] SMUKALLA S, CALDARA M, POCHET N, et al. FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast[J]. Cell, 2008, 135(4):726-737.
[38] RAINA S, ODELL M, KESHAVARZ T. Quorum sensing as a method for improving sclerotiorin production in Penicillium sclerotiorum[J]. Journal of Biotechnology, 2010, 148(2-3):91-98.
[39] COONEY J M, LAUREN D R. Trichoderma/pathogen interactions: Measurement of antagonistic chemicals produced at the antagonist/pathogen interface using a tubular bioassay[J]. Letters in Applied Microbiology, 1998, 27(5):283-286.
[40] VAKIL J R, RAGHAVENDRA RAO M R, BHATTACHARYYA P K. Effect of CO2 on the germination of conidiospores of Aspergillus niger[J]. Archiv Für Mikrobiologie, 1961, 39(1):53-57.
[41] AHMAD KHAN M S, AHMAD I, AQIL F, et al. Virulence and Pathogenicity of Fungal Pathogens with Special Reference to Candida albicans[M]. Berlin, Heidelberg: Springer Berlin Heidelberg, 2010:21-45.
[42] BAHN Y S, COX G M, PERFECT J R, et al. Carbonic anhydrase and CO2 sensing during Cryptococcus neoformans growth, differentiation, and virulence[J]. Current Biology, 2005, 15(22):2013-2020.
[43] NEMČOVIČM, JAKUBÍKOVÁ L, VÍDEN I, et al. Induction of conidiation by endogenous volatile compounds in Trichoderma spp[J]. FEMS Microbiology Letters, 2008, 284(2):231-236.
[44] ZHANG Y, GU Y, WU R, et al. Exploring the relationship between the signal molecule AI-2 and the biofilm formation of Lactobacillus sanfranciscensis[J]. LWT, 2022, 154:112704.
[45] YANG Q, DEFOIRDT T. Quorum sensing positively regulates flagellar motility in pathogenic Vibrio harveyi[J]. Environmental Microbiology, 2015, 17(4):960-968.
[46] YU T, MA M Y, SUN Y X, et al. The effect of sublethal concentrations of benzalkonium chloride on the LuxS/AI-2 quorum sensing system, biofilm formation and motility of Escherichia coli[J]. International Journal of Food Microbiology, 2021, 353:109313.
[47] ROBITAILLE S, GROLEAU M C, DÉZIEL E. Swarming motility growth favours the emergence of a subpopulation of Pseudomonas aeruginosa quorum-sensing mutants[J]. Environmental Microbiology, 2020, 22(7):2892-2906.
[48] WANG X, LI X L, LING J Q. Streptococcus gordonii LuxS/autoinducer-2 quorum-sensing system modulates the dual-species biofilm formation with Streptococcus mutans[J]. Journal of Basic Microbiology, 2017, 57(7):605-616.
[49] 朱寒剑, 李雷兵, 郑心, 等. 乳酸菌生物膜形成调控及在食品中的应用研究进展[J]. 食品科学, 2021, 42(5):296-304.
ZHU H J, LI L B, ZHENG X, et al. Recent progress in understanding the formation and regulation of lactic acid bacteria biofilm and its application in foods[J]. Food Science, 2021, 42(5):296-304.
[50] DENG Z X, HOU K W, VALENCAK T G, et al. AI-2/LuxS quorum sensing system promotes biofilm formation of Lactobacillus rhamnosus GG and enhances the resistance to enterotoxigenic Escherichia coli in germ-free zebrafish[J]. Microbiology Spectrum, 2022, 10(4): e0061022.
[51] JIA F F, ZHENG H Q, SUN S R, et al. Role of luxS in stress tolerance and adhesion ability in Lactobacillus plantarum KLDS1.0391[J]. BioMed Research International, 2018, 2018:4506829.
[52] LIU X X, JI L, WANG X, et al. Role of RpoS in stress resistance, quorum sensing and spoilage potential of Pseudomonas fluorescens[J]. International Journal of Food Microbiology, 2018, 270:31-38.
[53] QIU X M, ZHANG Y, HONG H S. Classification of acetic acid bacteria and their acid resistant mechanism[J]. AMB Express, 2021, 11(1):29.
[54] NATH B J, DAS K K, TALUKDAR R, et al. Tyrosols retrieved from traditionally brewed yeasts assist in tolerance against heavy metals and promote the growth of cells[J]. FEMS Microbiology Letters, 2022, 368(21-24): 152.
[55] PEREZ R H, ZENDO T, SONOMOTO K. Multiple bacteriocin production in lactic acid bacteria[J]. Journal of Bioscience and Bioengineering, 2022, 134(4):277-287.
[56] CHIKINDAS M L, WEEKS R, DRIDER D, et al. Functions and emerging applications of bacteriocins[J]. Current Opinion in Biotechnology, 2018, 49:23-28.
[57] WANG P P, YI Y L, LÜ X. CRISPR/Cas9-based genome editing platform for Companilactobacillus crustorum to reveal the molecular mechanism of its probiotic properties[J]. Journal of Agricultural and Food Chemistry, 2021, 69(50):15279-15289.
[58] DEO D, DAVRAY D, KULKARNI R. A diverse repertoire of exopolysaccharide biosynthesis gene clusters in Lactobacillus revealed by comparative analysis in 106 sequenced genomes[J]. Microorganisms, 2019, 7(10):444.
[59] 纪亚楠. 环境胁迫对乳酸菌产生物膜、信号分子Al-2及胞外多糖的影响[D]. 呼和浩特: 内蒙古农业大学, 2020.
JI Y N. The effects of environmental stress on the production of biofilm, signal molecule AI-2 and EPS in lactic acid bacteria[D]. Hohhot: Inner Mongolia Agricultural University, 2020.
[60] GU Y, TIAN J J, ZHANG Y, et al. Dissecting signal molecule AI-2 mediated biofilm formation and environmental tolerance in Lactobacillus plantarum[J]. Journal of Bioscience and Bioengineering, 2021, 131(2):153-160.
[61] ALMEIDA O G G, PINTO U M, MATOS C B, et al. Does qorum snsing play a role in microbial shifts along spontaneous fermentation of cocoa beans? An in silico perspective[J]. Food Research International, 2020, 131:109034.
[62] GU Y, TIAN J J, ZHANG Y, et al. Effect of Saccharomyces cerevisiae cell-free supernatant on the physiology, quorum sensing, and protein synthesis of lactic acid bacteria[J]. LWT, 2022, 165:113732.
[63] FU C Y, LI L Q, YANG T, et al. Autoinducer-2 may be a new biomarker for monitoring neonatal necrotizing enterocolitis[J]. Frontiers in Cellular and Infection Microbiology, 2020, 10:140.
[64] STURBELLE R T, DA COSTA DE AVILA L F, ROOS T B, et al. The role of quorum sensing in Escherichia coli (ETEC) virulence factors[J]. Veterinary Microbiology, 2015, 180(3-4):245-252.
[65] ZHANG X J, LIU B B, DING X Y, et al. Regulatory mechanisms between quorum sensing and virulence in Salmonella[J]. Microorganisms, 2022, 10(11):2211.
[66] JUGDER B E, BATISTA J H, GIBSON J A, et al. Vibrio cholerae high cell density quorum sensing activates the host intestinal innate immune response[J]. Cell Reports, 2022, 40(12):111368.
[67] DARKOH C, DUPONT H L, NORRIS S J, et al. Toxin synthesis by Clostridium difficile is regulated through quorum signaling[J]. mBio, 2015, 6(2): e02569.
[68] REZZOAGLI C, GRANATO E T, KÜMMERLI R. In-vivo microscopy reveals the impact of Pseudomonas aeruginosa social interactions on host colonization[J]. The ISME Journal, 2019, 13(10):2403-2414.
[69] DENG Z X, DAI J Y, WEI Y S, et al. Comparison between Lactobacillus rhamnosus GG and LuxS-deficient strain in regulating gut barrier function and inflammation in early-weaned piglets[J]. Frontiers in Immunology, 2022, 13:1080789.
[70] LIU L, TAO Y F, LI Y F, et al. Isolation and characterization of bacteria that produce quorum sensing molecules during the fermentation and deterioration of pickles[J]. International Journal of Food Microbiology, 2022, 379:109869.
[71] PARK H, SHIN H, LEE K, et al. Autoinducer-2 properties of kimchi are associated with lactic acid bacteria involved in its fermentation[J]. International Journal of Food Microbiology, 2016, 225:38-42.
[72] IRAQUI I, VISSERS S, ANDRÉ B, et al. Transcriptional induction by aromatic amino acids in Saccharomyces cerevisiae[J]. Molecular and Cellular Biology, 1999, 19(5):3360-3371.
[73] IRAQUI I, VISSERS S, CARTIAUX M, et al. Characterisation of Saccharomyces cerevisiae ARO8 and ARO9 genes encoding aromatic aminotransferases I and II reveals a new aminotransferase subfamily[J]. Molecular and General Genetics MGG, 1998, 257(2):238-248.
[74] CHEN H, FINK G R. Feedback control of morphogenesis in fungi by aromatic alcohols[J]. Genes & Development, 2006, 20(9):1150-1161.
[75] AVBELJ M, ZUPAN J R, KRANJC L, et al. Quorum-sensing kinetics in Saccharomyces cerevisiae: A symphony of ARO genes and aromatic alcohols[J]. Journal of Agricultural and Food Chemistry, 2015, 63(38):8544-8550.
[76] BRITTON S J, NEVEN H, MASKELL D L. Microbial small-talk: Does quorum sensing play a role in beer fermentation?[J]. Journal of the American Society of Brewing Chemists, 2021, 79(3):231-239.
[77] GORI K, MOSLEHI-JENABIAN S, PURROTTI M, et al. Autoinducer-2 activity produced by bacteria found in smear of surface ripened cheeses[J]. International Dairy Journal, 2011, 21(1):48-53.
[78] IBACACHE-QUIROGA C, GONZÁLEZ-PIZARRO K, CHARIFEH M, et al. Metagenomic and functional characterization of two Chilean kefir beverages reveals a dairy beverage containing active enzymes, short-chain fatty acids, microbial β-amyloids, and bio-film inhibitors[J]. Foods, 2022, 11(7):900.
[79] YUAN L, SADIQ F A, BURMØLLE M, et al. Insights into bacterial milk spoilage with particular emphasis on the roles of heat-stable enzymes, biofilms, and quorum sensing[J]. Journal of Food Protection, 2018, 81(10):1651-1660.
[80] YUAN L, WANG N, SADIQ F A, et al. RNA sequencing reveals the involvement of quorum sensing in dairy spoilage caused by psychrotrophic bacteria[J]. LWT, 2020, 127:109384.
[81] LIN M, ZHOU G H, WANG Z G, et al. Functional analysis of AI-2/LuxS from bacteria in Chinese fermented meat after high nitrate concentration shock[J]. European Food Research and Technology, 2015, 240(1):119-127.
[82] SUSILO Y B, SIHTO H M, RÅDSTRÖM P, et al. Reduced enterotoxin D formation on boiled ham in Staphylococcus aureus δagr mutant[J]. Toxins, 2017, 9(9):263.
[83] ZHANG Y H, SHAN B, GONG J S, et al. Mechanism of biogenic amine synthesis of Enterococcus faecium isolated from Sanchun ham[J]. Food Science & Nutrition, 2022, 10(6):2036-2049.
[84] 李军, 张旭, 马长伟, 等. 群体感应信号肽介导的产细菌素乳杆菌在发酵肠中的应用[J]. 中国农业大学学报, 2015, 20(6):256-262.
LI J, ZHANG X, MA C W, et al. Lactobacillus paraplantarum producing AIP-regulated bacteriocin as starter cultures for fermented sausages[J]. Journal of China Agricultural University, 2015, 20(6):256-262.
[85] 黎凡. 基于AI-2/LuxS群体感应系统金华火腿优势菌群风味形成机制的研究[D]. 杭州: 浙江工商大学, 2020.
LI F. The mechanism of volatile compounds formation associated with predominant microbial community in Jinhua ham based on AI-2/LuxS quorum sensing system[D]. Hangzhou: Zhejiang Gongshang University, 2020.
[86] RUIZ-BARBA J L, CABALLERO-GUERRERO B, MALDONADO-BARRAGÁN A, et al. Coculture with specific bacteria enhances survival of Lactobacillus plantarum NC8, an autoinducer-regulated bacteriocin producer, in olive fermentations[J]. Food Microbiology, 2010, 27(3):413-417.
[87] RIPARI V, CECCHI T, BERARDI E. Microbiological characterisation and volatiles profile of model, ex-novo, and traditional Italian white wheat sourdoughs[J]. Food Chemistry, 2016, 205:297-307.
[88] 吴哲铭. 基于luxS/AI-2群体感应系统对鱼露发酵过程中增香降胺调控机理的研究[D]. 杭州: 浙江工商大学, 2020.
WU Z M. Study on the regulation mechanism of aromatizing and reducing amine in fishweed fermentation process based on luxS/AI-2 quorum sensing system[D]. Hangzhou: Zhejiang Gongshang University, 2020.
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