Skip to main content
Log in

Extracellular matrix-degrading enzymes as a biofilm control strategy for food-related microorganisms

  • Review
  • Published:
Food Science and Biotechnology Aims and scope Submit manuscript

Abstract

Biofilm is one of the major problems in food industries and is difficult to be removed or prevented by conventional sanitizers. In this review, we discussed the extracellular matrix-degrading enzymes as a strategy to control biofilms of foodborne pathogenic and food-contaminating bacteria. The biofilms can be degraded by using the enzymes targeting proteins, polysaccharides, extracellular DNA, or lipids which mainly constitute the extracellular polymeric substances of biofilms. However, the efficacy of enzymes varies by the growth medium, bacterial species, strains, or counterpart microorganisms due to a high variation in the composition of extracellular polymeric substances. Several studies demonstrated that the combined treatment using conventional sanitizers or multiple enzymes can synergistically enhance the biofilm removal efficacies. In this review, the application of the immobilized enzymes on solid substrates is also discussed as a potential strategy to prevent biofilm formation on food contact surfaces.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Alkan-Tas B, Durmus-Sayar A, Duman ZE, Sevinis-Ozbulut EB, Unlu A, Binay B, Unal S, Unal, H. Antibacterial hybrid coatings from halloysite-immobilized lysostaphin and waterborne polyurethanes. Progress in Organic Coatings. 156: 106248 (2021)

    Article  CAS  Google Scholar 

  • Alves D, Magalhães A, Grzywacz D, Neubauer D, Kamysz W, Pereira MO. Co-immobilization of Palm and DNase I for the development of an effective anti-infective coating for catheter surfaces. Acta Biomaterialia. 44: 313-322 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Araújo PA, Machado I, Meireles A, Leiknes T, Mergulhão F, Melo LF, Simões M. Combination of selected enzymes with cetyltrimethylammonium bromide in biofilm inactivation, removal and regrowth. Food Research International. 95: 101-107 (2017)

    Article  PubMed  Google Scholar 

  • Asker D, Awad TS, Raju D, Sanchez H, Lacdao I, Gilbert S, Sivarajah P, Andes DR, Sheppard DC, Howell PL, Hatton BD. Preventing Pseudomonas aeruginosa biofilms on indwelling catheters by surface-bound enzymes. ACS Applied Bio Materials. 4: 8248-8258 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baelo A, Levato R, Julián E, Crespo A, Astola J, Gavaldà J, Engel E, Mateos-Timoneda MA, Torrents E. Disassembling bacterial extracellular matrix with DNase-coated nanoparticles to enhance antibiotic delivery in biofilm infections. Journal of Controlled Release. 209: 150-158 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Baidamshina DR, Koroleva VA, Olshannikova SS, Trizna EY, Bogachev MI, Artyukhov VG, Holyavka MG, Kayumov AR. Biochemical properties and anti-biofilm activity of chitosan-immobilized papain. Marine Drugs. 19: 197 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker P, Hill PJ, Snarr BD, Alnabelseya N, Pestrak MJ, Lee MJ, Jennings LK, Tam J, Melnyk RA, Parsek MR, Sheppard DC, Wozniak DJ, Howell PL. Exopolysaccharide biosynthetic glycoside hydrolases can be utilized to disrupt and prevent Pseudomonas aeruginosa biofilms. Science Advances. 2: e1501632 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  • Bales PM, Renke EM, May SL, Shen Y, Nelson DC. Purification and characterization of biofilm-associated EPS exopolysaccharides from ESKAPE organisms and other pathogens. PLoS One. 8: e67950 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benomar S, Venanzio GD, Feldman MF. Plasmid-encoded H-NS controls extracellular matrix composition in a modern Acinetobacter baumannii urinary isolate. Journal of Bacteriology. 203: e00277-21 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bridier A, Sanchez-Vizuete P, Guilbaud M, Piard J-C, Naïtali M, Briandet R. Biofilm-associated persistence of food-borne pathogens. Food Microbiology. 45: 167-178 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Brown HL, Hanman K, Reuter M, Betts RP, van Vliet AHM. Campylobacter jejuni biofilms contain extracellular DNA and are sensitive to DNase I treatment. Frontiers in Microbiology. 6: 699 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  • Cattò C, Secundo F, James G, Villa F, Cappitelli F. α-Chymotrypsin immobilized on a low-density polyethylene surface successfully weakens Escherichia coli biofilm formation. International Journal of Molecular Sciences. 19: 4003 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Chaignon P, Sadovskaya I, Ragunah C, Ramasubbu N, Kaplan JB, Jabbouri S. Susceptibility of staphylococcal biofilms to enzymatic treatments depends on their chemical composition. Applied Microbiology and Biotechnology. 75: 125-132 (2007)

    Article  CAS  PubMed  Google Scholar 

  • Chandra M, Thakur S, Narang D, Kaur G, Sharma NS. Evaluation of Salmonella Typhimurium biofilm against some antibiotics. Indian Journal of Experimental Biology. 55: 562-567 (2017)

    CAS  Google Scholar 

  • Chiang WC, Nilsson M, Jensen PØ, Høiby N, Nielsen TE, Givskov M, Tolker-Nielsen T. Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrobial Agents and Chemotherapy. 57: 2352-2361 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colvin KM, Irie Y, Tart CS, Urbano R, Whitney JC, Ryder C, Howell PL, Wozniak DJ, Parsek MR. The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environmental Microbiology. 14: 1913-1928 (2012)

    Article  CAS  PubMed  Google Scholar 

  • Cordeiro AL, Hippius C, Werner C. Immobilized enzymes affect biofilm formation. Biotechnology Letters. 33: 1897-1904 (2011)

    Article  CAS  PubMed  Google Scholar 

  • Craigen B, Dashiff A, Kadouri DE. The use of commercially available alpha-amylase compounds to inhibit and remove Staphylococcus aureus biofilms. The Open Microbiology Journal. 5: 21-31 (2011)

    Article  PubMed  PubMed Central  Google Scholar 

  • Devlin H, Fulaz S, Hiebner DW, O’Gara JP, Casey E. Enzyme-functionalized mesoporous silica nanoparticles to target Staphylococcus aureus and disperse biofilms. International Journal of Nanomedicine. 16: 1929-1942 (2021)

    Article  PubMed  PubMed Central  Google Scholar 

  • Dobrynina OY, Bolshakova TN, Umyarov AM, Boksha IS, Lavrova NV, Grishin AV, Lyashchuk AM, Galushkina ZM, Avetisian LR, Chernukha MY, Shaginian IA, Lunin VG, Karyagina AS. Disruption of bacterial biofilms using recombinant dispersin B. Microbiology. 84: 498-501 (2015)

    Article  CAS  Google Scholar 

  • Elamary R, Salem WM. Optimizing and purifying extracellular amylase from soil bacteria to inhibit clinical biofilm-forming bacteria. PeerJ. 8: e10288 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  • Erskine E, MacPhee CE, Stanley-Wall NR. Functional amyloid and other protein fibers in the biofilm matrix. Journal of Molecular Biology. 430: 3642-3656 (2018)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flemming HC, van Hullebusch ED, Neu TR, Nielsen PH, Seviour T, Stoodley P, Wingender J, Wuertz S. The biofilm matrix: multitasking in a shared space. Nature Reviews Microbiology. https://doi.org/https://doi.org/10.1038/s41579-022-00791-0 (2022)

    Article  PubMed  Google Scholar 

  • Flemming HC, Wingender J. The biofilm matrix. Nature Reviews Microbiology. 8: 623-633 (2010)

    Article  CAS  PubMed  Google Scholar 

  • Flemming HC, Wuertz S. Bacteria and archaea on Earth and their abundance in biofilms. Nature Reviews Microbiology. 17: 247-260 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Galié S, García-Gutiérrez C, Miguélez EM, Villar CJ, Lombó F. Biofilms in the food industry: health aspects and control methods. Frontiers in Microbiology. 9: 898 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Gallo PM, Rapsinski GJ, Wilson RP, Oppong GO, Sriram U, Goulian M, Buttaro B, Caricchio R, Gallucci S, Tükel C. Amyloid-DNA composites of bacterial biofilms stimulate autoimmunity. Immunity. 42: 1171-1184 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hobley L, Harkins C, MacPhee CE, Stanley-Wall NR. Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes. FEMS Microbiology Reviews. 39: 649-669 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu H, Kang X, Shan Z, Yang X, Bing W, Wu L, Ge H, Ji H. A DNase-mimetic artificial enzyme for the eradication of drug-resistant bacterial biofilm infections. Nanoscale. 14: 2676-2685 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Ivanova K, Fernandes MM, Francesko A, Mendoza E, Guezguez J, Burnet M, Tzanov T. Quorum-quenching and matrix-degrading enzymes in multilayer coatings synergistically prevent bacterial biofilm formation on urinary catheters. ACS Applied Materials & Interfaces. 7: 27066-27077 (2015)

    Article  CAS  Google Scholar 

  • Joseph B, Otta SK, Karunasagar I, Karunasagar I. Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. International Journal of Food Microbiology. 64: 367-372 (2001)

    Article  CAS  PubMed  Google Scholar 

  • Kalpana BJ, Aarthy S, Pandian SK. Antibiofilm activity of α-amylase from Bacillus subtilis S8-18 against biofilm forming human bacterial pathogens. Applied Biochemistry and Biotechnology. 167: 1778-1794 (2012)

    Article  CAS  PubMed  Google Scholar 

  • Kilic T. Biofilm-forming ability and effect of sanitation agents on biofilm-control of thermophile Geobacillus sp. D413 and Geobacillus toebii E134. Polish Journal of Microbiology. 69: 411-419 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim M, Shin MK, Sung JS, Kadam AA. Supermagnetic halloysite nanotubes surface-tuned with aminosilane for protease immobilization and applied for eradication of bacterial biofilm. Applied Surface Science. 593: 153469 (2022)

    Article  CAS  Google Scholar 

  • Kim MJ, Kim JS. Enhanced inactivation of Salmonella enterica Enteritidis biofilms on the stainless steel surface by proteinase K in the combination with chlorine. Food Control. 132: 108519 (2022)

    Article  CAS  Google Scholar 

  • Kim MJ, Lim ES, Kim JS. Enzymatic inactivation of pathogenic and nonpathogenic bacteria in biofilms in combination with chlorine. Journal of Food Protection. 82: 605-614 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Kim SH, Park C, Lee EJ, Bang WS, Kim YJ, Kim JS. Biofilm formation of Campylobacter strains isolated from raw chickens and its reduction with DNase I treatment. Food Control. 71: 94-100 (2017)

    Article  CAS  Google Scholar 

  • Kiran GS, Lipton AN, Kennedy J, Dobson ADW, Selvin J. A halotolerant thermostable lipase from the marine bacterium Oceanobacillus sp. PUMB02 with an ability to disrupt bacterial biofilms. Bioengineered. 5: 305-318 (2014)

    Article  Google Scholar 

  • Kumari S, Sarkar PK. Optimisation of Bacillus cereus biofilm removal in the dairy industry using an in vitro model of cleaning-in-place incorporating serine protease. International Journal of Dairy Technology. 71: 512-518 (2018)

    Article  CAS  Google Scholar 

  • Kwon M, Hussain MS, Oh DH. Biofilm formation of Bacillus cereus under food-processing-related conditions. Food Science and Biotechnology. 26: 1103-1111 (2017)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lahiri D, Nag M, Banerjee R, Mukherjee D, Garai S, Sarkar T, Dey A, Sheikh HI, Pathak SK, Edinur HA, Pati S, Ray RR. Amylases: biofilm inducer or biofilm inhibitor? Frontiers in Cellular and Infection Microbiology. 11: 660048 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lakshmi SA, Alexpandi R, Shafreen RMB, Tamilmuhilan K, Srivathsan A, Kasthuri T, Ravi AV, Shiburaj S, Pandian SK. Evaluation of antibiofilm potential of four-domain α-amylase from Streptomyces griseus against exopolysaccharides (EPS) of bacterial pathogens using Danio rerio. Archives of Microbiology. 204: 243 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Liaqat I, Hussain T, Qurashi AW, Saleem G, Bibi A, Qamar MF, Ali S, Ikram-ul-Haq. Antibiofilm activity of proteolytic enzymes against Salmonella Gallinarum isolates from commercial broiler chickens. Pakistan Journal of Zoology. 53: 1111-1118 (2021)

    Article  CAS  Google Scholar 

  • Lim ES, Baek SY, Oh T, Koo M, Lee JY, Kim HJ, Kim JS. Strain variation in Bacillus cereus biofilms and their susceptibility to extracellular matrix-degrading enzymes. PLoS One. 16: e0245708 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim ES, Koo OK, Kim MJ, Kim JS. Bio-enzymes for inhibition and elimination of Escherichia coli O157:H7 biofilm and their synergistic effect with sodium hypochlorite. Scientific Reports. 9: 9920 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  • Lim ES, Lee JE, Kim JS, Koo OK. Isolation of indigenous bacteria from a cafeteria kitchen and their biofilm formation and disinfectant susceptibility. LWT-Food Science and Technology. 77: 376-382 (2017)

    Article  CAS  Google Scholar 

  • Lim ES, Nam SJ, Koo OK, Kim JS. Protective role of Acinetobacter and Bacillus for Escherichia coli O157:H7 in biofilms against sodium hypochlorite and extracellular matrix-degrading enzymes. Food Microbiology. 109: 104125 (2023)

    Article  CAS  PubMed  Google Scholar 

  • Limoli DH, Jones CJ, Wozniak DJ. Bacterial extracellular polysaccharides in biofilm formation and function. Microbiology Spectrum. 3: 3.3.29 (2015)

  • Longhi C, Scoarughi GL, Poggiali F, Cellini A, Carpentieri A, Seganti L, Pucci P, Amoresano A, Cocconcelli PS, Artini M, Costerton JW, Selan L. Protease treatment affects both invasion ability and biofilm formation in Listeria monocytogenes. Microbial Pathogenesis. 45: 45-52 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Mahajan S, Sunsunwal S, Gautam V, Singh M, Ramya TNC. Biofilm inhibitory effect of alginate lyases on mucoid P. aeruginosa from a cystic fibrosis patient. Biochemistry and Biophysics Reports. 26: 101028 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manohar CM, Prabhawathi V, Sivakumar PM, Doble M. Design of a papain immobilized antimicrobial food package with curcumin as a crosslinker. PloS One. 10: e0121665 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  • Matias RR, Sepúlveda AMG, Batista BN, de Lucena JMVM, Albuquerque PM. Degradation of Staphylococcus aureus biofilm using hydrolytic enzymes produced by Amazonian endophytic fungi. Applied Biochemistry and Biotechnology. 193: 2145-2161 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Mayton HM, Walker SL, Berger BW. Disrupting irreversible bacterial adhesion and biofilm formation with an engineered enzyme. Applied and Environmental Microbiology. 87: e00265-21 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazaheri T, Ripolles-Avila C, Hascoët AS, Rodríguez-Jerez JJ. Effect of an enzymatic treatment on the removal of mature Listeria monocytogenes biofilms: A quantitative and qualitative study. Food Control. 114: 107266 (2020)

    Article  CAS  Google Scholar 

  • Mnif S, Jardak M, Yaich A, Aifa S. Enzyme-based strategy to eradicate monospecies Macrococcus caseolyticus biofilm contamination in dairy industries. International Dairy Journal. 100: 104560 (2020)

    Article  CAS  Google Scholar 

  • Molobela IP, Cloete TE, Beukes M. Protease and amylase enzymes for biofilm removal and degradation of extracellular polymeric substances (EPS) produced by Pseudomonas fluorescens bacteria. African Journal of Microbiology Research. 4: 1515-1524 (2010)

    CAS  Google Scholar 

  • Muslim SN, Al-Kadmy IMS, Hussein NH, Ali ANM, Taha BM, Aziz SN, Al Kheraif AA, Divakar DD, Ramakrishnaiah R. Chitosanase purified from bacterial isolate Bacillus licheniformis of ruined vegetables displays broad spectrum biofilm inhibition. Microbial Pathogenesis. 100: 257-262 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Nahar S, Jeong HL, Cho AJ, Park JH, Han SH, Kim Y, Park SH, Ha SD. Efficacy of ficin and peroxyacetic acid against Salmonella enterica serovar Thompson biofilm on plastic, eggshell, and chicken skin. Food Microbiology. 104: 103997 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Nahar S, Jeong HL, Kim Y, Ha AJW, Roy PK, Park SH, Ashrafudoulla M, Mizan MFR, Ha SD. Inhibitory effects of flavourzyme on biofilm formation, quorum sensing, and virulence genes of foodborne pathogens Salmonella Typhimurium and Escherichia coli. Food Research International. 147: 110461 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Nahar S, Mizan MFR, Ha AJW, Ha SD. Advances and future prospects of enzyme-based biofilm prevention approaches in the food industry. Comprehensive Reviews in Food Science and Food Safety. 17: 1484-1502 (2018)

    Article  PubMed  Google Scholar 

  • Nguyen UT, Burrows LL. DNase I and proteinase K impair Listeria monocytogenes biofilm formation and induce dispersal of pre-existing biofilms. International Journal of Food Microbiology. 187: 26-32 (2014)

    Article  CAS  PubMed  Google Scholar 

  • Okshevsky M, Meyer RL. Evaluation of fluorescent stains for visualizing extracellular DNA in biofilms. Journal of Microbiological Methods. 105: 102-104 (2014)

    Article  CAS  PubMed  Google Scholar 

  • Okshevsky M, Meyer RL. The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Critical Reviews in Microbiology. 41: 341-352 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Orgaz B, Neufeld RJ, SanJose C. Single-step biofilm removal with delayed release encapsulated Pronase mixed with soluble enzymes. Enzyme and Microbial Technology. 40: 1045-1051 (2007)

    Article  CAS  Google Scholar 

  • Oulahal-Lagsir N, Martial-Gros A, Bonneau M, Blum LJ. “Escherichia coli-milk” biofilm removal from stainless steel surfaces: Synergism between ultrasonic waves and enzymes. Biofouling. 19: 159-168 (2003)

    CAS  PubMed  Google Scholar 

  • Pan I. Exploration for thermostable ß-amylase of a Bacillus sp. isolated from compost soil to degrade bacterial biofilm. Microbiology Spectrum. 9: e00647-21 (2021)

  • Panlilio H, Rice CV. The role of extracellular DNA in the formation, architecture, stability, and treatment of bacterial biofilms. Biotechnology and Bioengineering. 118: 2129-2141 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park KM, Kim AY, Kim HJ, Cho YS, Koo M. Prevalence and characterization of toxigenic Bacillus cereus group isolated from low-moisture food products. Food Science and Biotechnology. 31: 1615-1629 (2022)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel KK, Tripathi M, Pandey N, Agrawal AK, Gade S, Anjum MM, Tilak R, Singh S. Alginate lyase immobilized chitosan nanoparticles of ciprofloxacin for the improved antimicrobial activity against the biofilm associated mucoid P. aeruginosa infection in cystic fibrosis. International Journal of Pharmaceutics. 563: 30-42 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Perwez M, Mazumder JA, Noori R, Sardar M. Magnetic combi CLEA for inhibition of bacterial biofilm: A green approach. International Journal of Biological Macromolecules. 186: 780-787 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Poilvache H, Ruiz-Sorribas A, Cornu O, Van Bambeke F. In vitro study of the synergistic effect of an enzyme cocktail and antibiotics against biofilms in a prosthetic joint infection model. Antimicrobial Agents and Chemotherapy. 65: e01699-20 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puga CH, Rodríguez-López P, Cabo ML, SanJose C, Orgaz B. Enzymatic dispersal of dual-species biofilms carrying Listeria monocytogenes and other associated food industry bacteria. Food Control. 94: 222-228 (2018)

    Article  CAS  Google Scholar 

  • Ramírez MDF, Smid EJ, Abee T, Groot MNN. Characterisation of biofilms formed by Lactobacillus plantarum WCFS1 and food spoilage isolates. International Journal of Food Microbiology. 207: 23-29 (2015)

    Article  Google Scholar 

  • Randrianjatovo-Gbalou I, Rouquette P, Lefebvre D, Girbal-Neuhauser E, Marcato-Romain CE. In situ analysis of Bacillus licheniformis biofilms: amyloid-like polymers and eDNA are involved in the adherence and aggregation of the extracellular matrix. Journal of Applied Microbiology. 122: 1262-1274 (2017)

    Article  CAS  PubMed  Google Scholar 

  • Ripolles-Avila C, Ríos-Castillo AG, Fontecha-Umana F, Rodríguez-Jerez JJ. Removal of Salmonella enterica serovar Typhimurium and Cronobacter sakazakii biofilms from food contact surfaces through enzymatic catalysis. Journal of Food Safety. 40: e12755 (2020)

    Article  Google Scholar 

  • Rodríguez-López P, Carballo-Justo A, Draper LA, Cabo ML. Removal of Listeria monocytogenes dual-species biofilms using combined enzyme-benzalkonium chloride treatments. Biofouling. 33: 45-58 (2017)

    Article  PubMed  Google Scholar 

  • Ronish LA, Sidner B, Yu Y, Piepenbrink KH. Recognition of extracellular DNA by type IV pili promotes biofilm formation by Clostridioides difficile. Journal of Biological Chemistry. 298: 102449 (2022)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Sorribas A, Poilvache H, Kamarudin NHN, Braem A, Van Bambeke F. Hydrolytic enzymes as potentiators of antimicrobials against an inter-kingdom biofilm model. Microbiology Spectrum. 10: e02589-21 (2022)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryu JH, Beuchat LR. Biofilm formation by Escherichia coli O157:H7 on stainless steel: effect of exopolysaccharide and curli production on its resistance to chlorine. Applied and Environmental Microbiology. 71: 247-254 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saggu SK, Jha G, Mishra PC. Enzymatic degradation of biofilm by metalloprotease from Microbacterium sp. SKS10. Frontiers in Bioengineering and Biotechnology. 7: 192 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  • Serra DO, Richter AM, Hengge R. Cellulose as an architectural element in spatially structured Escherichia coli biofilms. Journal of Bacteriology. 195: 5540-5554 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheffield CL, Crippen TL, Poole TL, Beier RC. Destruction of single species biofilms of Escherichia coli or Klebsiella pneumoniae subsp. pneumoniae by dextranase, lactoferrin, and lysozyme. International Microbiology. 15: 183-187 (2012)

    Google Scholar 

  • Shukla SK, Rao TS. Dispersal of Bap-mediated Staphylococcus aureus biofilm by proteinase K. Journal of Antibiotics. 66: 55-60 (2013)

    Article  Google Scholar 

  • Silagyi K, Kim SH, Lo YM, Wei CI. Production of biofilm and quorum sensing by Escherichia coli O157:H7 and its transfer from contact surfaces to meat, poultry, ready-to-eat deli, and produce products. Food Microbiology. 26: 514-519 (2009)

    Article  CAS  PubMed  Google Scholar 

  • Solano C, García B, Valle J, Berasain C, Ghigo JM, Gamazo C, Lasa I. Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Molecular Microbiology. 43: 793-808 (2002)

    Article  CAS  PubMed  Google Scholar 

  • Song YJ, Yu HH, Kim YJ, Lee NK, Paik HD. The use of papain for the removal of biofilms formed by pathogenic Staphylococcus aureus and Campylobacter jejuni. LWT-Food Science and Technology. 127: 109383 (2020)

    Article  CAS  Google Scholar 

  • Srey S, Jahid IK, Ha SD. Biofilm formation in food industries: A food safety concern. Food Control. 31: 572-585 (2013)

    Article  Google Scholar 

  • Stiefel P, Mauerhofer S, Schneider J, Maniura-Weber K, Rosenberg U, Ren Q. Enzymes enhance biofilm removal efficiency of cleaners. Antimicrobial Agents and Chemotherapy. 60: 3647-3652 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugimoto S, Sato F, Miyakawa R, Chiba A, Onodera S, Hori S, Mizunoe Y. Broad impact of extracellular DNA on biofilm formation by clinically isolated Methicillin-resistant and -sensitive strains of Staphylococcus aureus. Scientific Reports. 8: 2254 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Swartjes JJ, Das T, Sharifi S, Subbiahdoss G, Sharma PK, Krom BP, Busscher HJ, van der Mei HC. A functional DNase I coating to prevent adhesion of bacteria and the formation of biofilm. Advanced Functional Materials. 23: 2843-2849 (2013)

    Article  CAS  Google Scholar 

  • Szymańska M, Karakulska J, Sobolewski P, Kowalska U, Grygorcewicz B, Böttcher D, Bornscheuer UT, Drozd R. Glycoside hydrolase (PelAh) immobilization prevents Pseudomonas aeruginosa biofilm formation on cellulose-based wound dressing. Carbohydrate polymers. 246: 116625 (2020)

    Article  PubMed  Google Scholar 

  • Taglialegna A, Lasa I, Valle J. Amyloid structures as biofilm matrix scaffolds. Journal of Bacteriology. 198: 2579-2588 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan Y, Ma S, Leonhard M, Moser D, Ludwig R, Schneider-Stickler B. Co-immobilization of cellobiose dehydrogenase and deoxyribonuclease I on chitosan nanoparticles against fungal/bacterial polymicrobial biofilms targeting both biofilm matrix and microorganisms. Materials Science and Engineering: C. 108: 110499 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Tang X, Flint SH, Bennett RJ, Brooks JD. The efficacy of different cleaners and sanitisers in cleaning biofilms on UF membranes used in the dairy industry. Journal of Membrane Science. 352: 71-75 (2010)

    Article  CAS  Google Scholar 

  • Taş BA, Berksun E, Taş CE, Ünal S, Ünal H. Lysostaphin-functionalized waterborne polyurethane/polydopamine coatings effective against S. aureus biofilms. ACS Applied Polymer Materials. 4: 4298-4305 (2022)

    Article  Google Scholar 

  • Tursi S, Tükel. Curli-containing enteric biofilms inside and out: matrix composition, immune recognition, and disease implications. Microbiology and Molecular Biology Reviews. 82: e00028-18 (2018)

  • Van Houdt R, Michiels CW. Biofilm formation and the food industry, a focus on the bacterial outer surface. Journal of Applied Microbiology. 109: 1117-1131 (2010)

    Article  PubMed  Google Scholar 

  • Veluchamy P, Sivakumar PM, Doble M. Immobilization of subtilisin on polycaprolactam for antimicrobial food packaging applications. Journal of Agricultural and Food Chemistry. 59: 10869-10878 (2011)

    Article  CAS  PubMed  Google Scholar 

  • Vilain S, Pretorius JM, Theron J, Brözel VS. DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Applied and Environmental Microbiology. 75: 2861-2868 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogeleer P, Tremblay YDN, Jubelin G, Jacques M, Harel J. Biofilm-forming abilities of shiga toxin-producing Escherichia coli isolates associated with human infections. Applied and Environmental Microbiology. 82: 1448-1458 (2016)

    Article  CAS  PubMed Central  Google Scholar 

  • Wagner EM, Fischel K, Rammer N, Beer C, Palmetzhofer AL, Conrady B, Roch FF, Hanson BT, Wagner M, Rychli K. Bacteria of eleven different species isolated from biofilms in a meat processing environment have diverse biofilm forming abilities. International Journal of Food Microbiology. 349: 109232 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Wang R, Kalchayanand N, King DA, Luedtke BE, Bosilevac JM, Arthur TM. Biofilm formation and sanitizer resistance of Escherichia coli O157:H7 strains isolated from “high event period” meat contamination. Journal of Food Protection. 77: 1982-1987 (2014)

    Article  PubMed  Google Scholar 

  • Wang HH, Wang HW, Xing T, Wu N, Xu XL, Zhou GH. Removal of Salmonella biofilm formed under meat processing environment by surfactant in combination with bio-enzyme. LWT-Food Science and Technology. 66: 298-304 (2016)

    Article  CAS  Google Scholar 

  • Xavier JB, Picioreanu C, Rani SA, van Loosdrecht MCM, Stewart PS. Biofilm-control strategies based on enzymic disruption of the extracellular polymeric substance matrix-a modelling study. Microbiology-SGM. 151: 3817-3832 (2005)

    Article  CAS  Google Scholar 

  • Xiong J, Cao Y, Zhao H, Chen J, Cai X, Li X, Liu Y, Xiao H, Ge J. Cooperative Antibacterial Enzyme-Ag-Polymer Nanocomposites. ACS Nano. 16: 19013-19024 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Yassein AS, Hassan MM, Elamary RB. Prevalence of lipase producer Aspergillus niger in nuts and anti-biofilm efficacy of its crude lipase against some human pathogenic bacteria. Scientific Reports. 11: 7981 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zetzmann M, Okshevsky M, Endres J, Sedlag A, Caccia N, Auchter M, Waidmann MS, Desvaux M, Meyer RL, Riedel CU. DNase-sensitive and -resistant modes of biofilm formation by Listeria monocytogenes. Frontiers in Microbiology. 6: 1428 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Li Q, Li X, Wu X, Yuan T, Yang Y. Simulated enzyme activity and efficient antibacterial activity of copper-doped single-atom nanozymes. Langmuir. 38: 6860-6870 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Molecular Microbiology. 39: 1452-1463 (2001)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the Main Research Program (E0210702-02) of the Korea Food Research Institute (KFRI), funded by the Ministry of Science and ICT.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joo-Sung Kim.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, JS., Lim, MC., Kim, SM. et al. Extracellular matrix-degrading enzymes as a biofilm control strategy for food-related microorganisms. Food Sci Biotechnol 32, 1745–1761 (2023). https://doi.org/10.1007/s10068-023-01373-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10068-023-01373-3

Keywords

Navigation