Microbial enzymes as powerful natural anti-biofilm candidates

. 2024 Dec 23 ; 23 (1) : 343. [epub] 20241223

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid39710670
Odkazy

PubMed 39710670
PubMed Central PMC11664836
DOI 10.1186/s12934-024-02610-y
PII: 10.1186/s12934-024-02610-y
Knihovny.cz E-zdroje

Bacterial biofilms pose significant challenges, from healthcare-associated infections to biofouling in industrial systems, resulting in significant health impacts and financial losses globally. Classic antimicrobial methods often fail to eradicate sessile microbial communities within biofilms, requiring innovative approaches. This review explores the structure, formation, and role of biofilms, highlighting the critical importance of exopolysaccharides in biofilm stability and resistance mechanisms. We emphasize the potential of microbial enzymatic approaches, particularly focusing on glycosidases, proteases, and deoxyribonucleases, which can disrupt biofilm matrices effectively. We also delve into the importance of enzymes such as cellobiose dehydrogenase, which disrupts biofilms by degrading polysaccharides. This enzyme is mainly sourced from Aspergillus niger and Sclerotium rolfsii, with optimized production strategies enhancing its efficacy. Additionally, we explore levan hydrolase, alginate lyase, α-amylase, protease, and lysostaphin as potent antibiofilm agents, discussing their microbial origins and production optimization strategies. These enzymes offer promising avenues for combating biofilm-related challenges in healthcare, environmental, and industrial settings. Ultimately, enzymatic strategies present environmentally friendly solutions with high potential for biofilm management and infection control.

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Lahiri D, Dey A, Sarkar T, Rani R, Maksim R, Shariati MA, et al. Immobilized enzymes as potent antibiofilm agents. Biotechnol Prog. 2022;38(5):e3281. 10.1002/btpr.3281. PubMed DOI PMC

Muhammad MH, Idris AL, Fan X, Guo Y, Yu Y, Jin X, et al. Beyond risk: bacterial biofilms and their regulating approaches. Front Microbiol. 2020;11:928. 10.3389/fmicb.2020.00928. PubMed DOI PMC

Lahiri D, Nag M, Banerjee R, Mukherjee D, Garai S, Sarkar T, et al. Amylases: Biofilm inducer or biofilm inhibitor? Front Cell Infect Microbiol. 2021;11:660048. 10.3389/fcimb.2021.660048. PubMed DOI PMC

Leroy C, Delbarre C, Ghillebaert F, Compere C, Combes D. Effects of commercial enzymes on the adhesion of a marine biofilm-forming bacterium. Biofouling. 2008;24(1):11–22. 10.1080/08927010701784912. PubMed DOI

Lahiri D, Dash S, Dutta R, Nag M. Elucidating the effect of anti-biofilm activity of bioactive compounds extracted from plants. J Biosci. 2019;44(2):52. PMID: 31180065. PubMed

Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Annu Rev Microbiol. 1995;49:711–45. 10.1146/annurev.mi.49.100195.003431. PubMed DOI

Yang L, Liu Y, Wu H, Song Z, Høiby N, Molin S, et al. Combating biofilms. FEMS Immunol Med Microbiol. 2012;65(2):146–57. 10.1111/j.1574-695X.2011.00858.x. PubMed DOI

Ray RR, Nag M, Lahiri D. Biofilm-mediated diseases: causes and controls. Biofilm-Mediated Diseases: Causes Controls. 2021;1–284 p.

Lahiri D, Nag M, Sarkar T, Dutta B, Ray RR. Antibiofilm activity of α-amylase from PubMed DOI

Akbarian M, Chen SH, Kianpour M, Farjadian F, Tayebi L, Uversky VN. A review on biofilms and the currently available antibiofilm approaches: matrix-destabilizing hydrolases and anti-bacterial peptides as promising candidates for the food industries. Int J Biol Macromol. 2022;219:1163–79. 10.1016/j.ijbiomac.2022.08.192. PubMed DOI

Barceló AM, Cortina IC, Rodríguez AIA, Ballesteros CR. Climatología Del Balneario De Villavieja. La Real Acad Nac Farm. 2016;82(5):108–26.

Holden ER, Yasir M, Turner AK, Wain J, Charles IG, Webber MA. Massively parallel transposon mutagenesis identifies temporally essential genes for biofilm formation in PubMed DOI PMC

Guo M, Tan S, Zhu J, Sun A, Du P, Liu X. Genes involved in biofilm matrix formation of the food spoiler PubMed DOI PMC

Lee S, Chen J. Genes of DOI

Kaur I, Sharma C. A review: role of bacterial exopolysaccharides in biofilm formation. J Res Appl Sci Biotechnol. 2022;1(3):222–8. 10.55544/jrasb.1.3.29. DOI

Plakunov VK, Mart’yanov SV, Teteneva NA, Zhurina MV. Controlling microbial biofilm formation: Anti- and probiofilm agents. Microbiol (Russian Fed). 2017;86(4):423–38. 10.1134/S0026261717040129. DOI

Richards JJ, Melander C. Controlling bacterial biofilms. ChemBioChem. 2009;10(14):2287–94. 10.1002/cbic.200900317. PubMed DOI

Drenkard E, Ausubel FM. PubMed DOI

Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. Extracellular DNA required for bacterial biofilm formation. Science. 2002;295(5559):1487. 10.1126/science.295.5559.1487. PubMed DOI

Arias CA, Murray BE. Antibiotic-resistant bugs in the 21st century — a clinical super-challenge. N Engl J Med. 2009;360(5):439–43. 10.1056/NEJMp0804651. PubMed DOI

Zhao X, Yu Z, Ding T. Quorum-sensing regulation of antimicrobial resistance in bacteria. Microorganisms. 2020;8(3):425. 10.3390/microorganisms8030425. PubMed DOI PMC

Lahiri D, Nag M, Dutta B, Sarkar T, Ray RR. Artificial neural network and response surface methodology-mediated optimization of bacteriocin production by DOI

Kumar CG, Takagi H. Microbial alkaline proteases: from a bioindustrial viewpoint. Biotechnol Adv. 1999;17(7):561–94. 10.1016/s0734-9750(99)00027-0. PubMed DOI

Rasouli R, Navidinia M, Ghahfarokhi MS, Roudsari RV, Adabian S, Baghestani AR. Antibiofilm activity of cellobiose dehydrogenase enzyme (cdh) isolated from DOI

Gutiérrez TJ. Antibiofilm enzymes as an emerging technology for food quality and safety. Enzymes in Food Biotechnology: production, applications, and future prospects. Elsevier Inc.; 2018. pp. 321–42. 10.1016/B978-0-12-813280-7.00019-0.

Olsen SM, Pedersen LT, Laursen MH, Kiil S, Dam-Johansen K. Enzyme-based antifouling coatings: a review. Biofouling. 2007;23(5):369–83. 10.1080/08927010701566384. PubMed DOI

Khan F, Oloketuyi SF. Diversity of bacteria and bacterial products as antibiofilm and antiquorum sensing drugs against pathogenic bacteria. Curr Drug Target. 2019;20(11):1156–79. 10.2174/1389450120666190423161249. PubMed DOI

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 Biomater [Internet]. 2016;44:313–22. 10.1016/j.actbio.2016.08.010. PubMed DOI

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. Sci Rep. 2018;8:2254. 10.1038/s41598-018-20485-z. PubMed DOI PMC

Villa F, Secundo F, Polo A, Cappitelli F. Immobilized hydrolytic enzymes exhibit Antibiofilm Activity against PubMed DOI

Koch G. Medicinal Chemistry. Chimia (Aarau). 2017;71(10):643. https://pubmed.ncbi.nlm.nih.gov/29070408/. PubMed

Grover N, Plaks JG, Summers SR, Chado GR, Schurr MJ, Kaar JL. Acylase-containing polyurethane coatings with anti-biofilm activity. Biotechnol Bioeng. 2016;113(12):2535–43. 10.1002/bit.26019. PubMed DOI

Andreani ES, Villa F, Cappitelli F, Krasowska A, Biniarz P, Łukaszewicz M, et al. Coating polypropylene surfaces with protease weakens the adhesion and increases the dispersion of Candida albicans cells. Biotechnol Lett. 2017;39(3):423–8. 10.1007/s10529-016-2262-5. PubMed DOI

Fanaei Pirlar R, Emaneini M, Beigverdi R, Banar M, van Leeuwen B, Jabalameli W. Combinatorial effects of antibiotics and enzymes against dual-species PubMed DOI PMC

Kaplan JB, Sukhishvili SA, Sailer M, Kridin K, Ramasubbu N. PubMed DOI PMC

Abeleda HEP, Javier AP, Murillo AQM, Baculi RQ. Alpha-amylase conjugated biogenic silver nanoparticles as innovative strategy against biofilm-forming multidrug resistant bacteria. Biocatal Agric Biotechnol [Internet]. 2020;29:101784. 10.1016/j.bcab.2020.101784. DOI

Li S, Wang Y, Li X, Lee BS, Jung S, Lee MS. Enhancing the thermo-stability and anti-biofilm activity of alginate lyase by immobilization on low molecular weight chitosan nanoparticles. Int J Mol Sci. 2019;20(18):4565. 10.3390/ijms20184565. PubMed DOI PMC

Fischer C, Krause A, Kleinschmidt T. Optimization of production, purification and lyophilisation of cellobiose dehydrogenase by PubMed PMC

Prabhawathi V, Boobalan T, Sivakumar PM, Doble M. Antibiofilm properties of interfacially active lipase immobilized porous polycaprolactam prepared by LB technique. PLoS ONE. 2014;9(5):e96152. 10.1371/journal.pone.0096152. PubMed DOI PMC

Thallinger B, Brandauer M, Burger P, Sygmund C, Ludwig R, Ivanova K, et al. Cellobiose dehydrogenase functionalized urinary catheter as novel antibiofilm system. J Biomed Mater Res - Part B Appl Biomater. 2016;104(7):1448–56. 10.1002/jbm.b.33491. PubMed DOI

Chaudhary A, Gupta JK, Gupta LK, Banerjee UC. Production of Levanase by Rhodotorula Sp. Folia Microbiol (Praha). 1996;41(4):353–6. DOI

Dahech I, Ayed H, Ben, Belghith KS, Belghith H, Mejdoub H. Microbial production of levanase for specific hydrolysis of levan. Int J Biol Macromol [Internet]. 2013;60:128–33. 10.1016/j.ijbiomac.2013.05.002 PubMed

Ethica SN, Zilda DS, Oedjijono O, Nurgayah W, Muhtadi M. Bioprospection of alginate lyase from bacteria associated with brown algae Hydroclathrus sp. as antibiofilm agent: a review. AACL Bioflux. 2021;14(4):1974–89.

Barzkar N, Sheng R, Sohail M, Jahromi ST, Babich O, Sukhikh S, et al. Alginate Lyases from Marine Bacteria: an enzyme ocean for sustainable future. Molecules. 2022;27(11):3375. 10.3390/molecules27113375. PubMed DOI PMC

Daboor SM, Raudonis R, Cohen A, Rohde JR, Cheng Z. Marine bacteria, a source for alginolytic enzyme to disrupt PubMed DOI PMC

Zhu X, Li X, Shi H, Zhou J, Tan Z, Yuan M, et al. Characterization of a novel alginate lyase from marine bacterium PubMed DOI PMC

Vaikundamoorthy R, Rajendran R, Selvaraju A, Moorthy K, Perumal S. Development of thermostable amylase enzyme from Bacillus cereus for potential antibiofilm activity [Internet]. Vol. 77, Bioorganic Chemistry. Elsevier Inc.; 2018. 494–506 p. 10.1016/j.bioorg.2018.02.014 PubMed

AboKamer AM, AbdElsalam IS, Mostafa FA, Mustafa AA. And AlMadboly L. A. A promising microbial αamylase production, and purification from PubMed DOI PMC

Thallinger B, Prasetyo EN, Nyanhongo GS, Guebitz GM. Antimicrobial enzymes: an emerging strategy to fight microbes and microbial biofilms. Biotechnol J. 2013;8(1):97–109. 10.1002/biot.201200313. PubMed DOI

Tarek H, Nam K, Bin, Kim YK, Suchi SA, Yoo JC. Biochemical characterization and application of a detergent stable, antimicrobial and Antibiofilm potential protease from PubMed DOI PMC

Contesini FJ, de Melo RR, Sato HH. An overview of Bacillus proteases: from production to application. Crit Rev Biotechnol [Internet]. 2018;38(3):321–34. 10.1080/07388551.2017.1354354. PubMed DOI

Anandharaj M, Sivasankari B, Siddharthan N, Rani RP, Sivakumar S. Production, purification, and biochemical characterization of Thermostable Metallo-protease from novel PubMed DOI

Nguyen UT, Burrows LL. DNase I and proteinase K impair Listeria monocytogenes biofilm formation and induce dispersal of pre-existing biofilms. Int J Food Microbiol. 2014;187:26–32. 10.1016/j.ijfoodmicro.2014.06.025. PubMed DOI

Shukla SK, Rao TS. Dispersal of Bap-mediated Staphylococcus aureus biofilm by proteinase K. J Antibiot. 2013;66:55–60. 10.1038/ja.2012.98. PubMed DOI

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. Sci Rep. 2019;9:9920. 10.1038/s41598-019-46363-w. PubMed DOI PMC

Eladawy M, El-Mowafy M, El-Sokkary MMA, Barwa R. Effects of Lysozyme, proteinase K, and Cephalosporins on Biofilm formation by clinical isolates of PubMed DOI PMC

Yang H, Zhai C, Yu X, Li Z, Tang W, Liu Y, Ma X, Zhong X, Li G, Wu D, Ma L. High-level expression of proteinase K from Tritirachium album limber in Pichia pastoris using multi-copy expression strains. Protein Expr Purif. 2016;122:38–44. 10.1016/j.pep.2016.02.006. PubMed DOI

Ruiz-Sorribas A, Poilvache H, Kamarudin NHN, Braem A, Van Bambeke F. Hydrolytic enzymes as potentiators of antimicrobials against an inter-kingdom biofilm model. Microbiol Spectr. 2022;10:e02589–2621. 10.1128/spectrum.02589-21. PubMed DOI PMC

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 Res Int. 2017;95:101–7. 10.1016/j.foodres.2017.02.016. PubMed DOI

Mnif S, Jardak M, Yaich A, Aifa S. Enzyme-based strategy to eradicate monospecies Macrococcus caseolyticus biofilm contamination in dairy industries. Int Dairy J. 2020;100:104560. 10.1016/j.idairyj.2019.104560. DOI

Shettar SS, Bagewadi ZK, Kolvekar HN, Yunus Khan TM, Shamsudeen SM. Optimization of subtilisin production from PubMed DOI PMC

SCHINDLER CA, SCHUHARDT VT. Lysostaphin: a New Bacteriolytic Agent for the PubMed DOI PMC

Szweda P, Gorczyca G, Filipkowski P, Zalewska M, Milewski S. Efficient production of PubMed DOI

Wu JA, Kusuma C, Mond JJ, Kokai-kun JF. Lysostaphin Disrupts PubMed PMC

American Journal of Infection Control. Vol. Am J Infect Control. 2009;37:A10.

Szweda P, Kotłowski R, Kur J. New effective sources of the Staphylococcus simulans lysostaphin. J Biotechnol. 2005;117(2):203–13. 10.1016/j.jbiotec. PubMed DOI

Kerr DE, Plaut K, Bramley AJ, Williamson CM, Lax AJ, Moore K, et al. Lysostaphin expression in mammary glands confers protection against PubMed DOI

Climo MW, Patron RL, Goldstein BP, Archer GL. Lysostaphin treatment of experimental methicillin-resistant Staphylococcus aureus aortic valve endocarditis. Antimicrob Agents Chemother. 1998;42(6):1355–60. 10.1128/AAC.42.6.1355. PubMed DOI PMC

Huber MM, Huber TW. Susceptibility of methicillin-resistant Staphylococcus aureus to lysostaphin. J Clin Microbiol. 1989;27(5):1122–4. 10.1128/jcm.27.5.1122-1124.1989. PubMed DOI PMC

Duman ZE, Ünlü A, Çakar MM, Ünal H. Enhanced production of recombinant Staphylococcus simulans lysostaphin using medium engineering. Prep Biochem Biotechnol [Internet]. 2019;0(0):1–8. 10.1080/10826068.2019.1599393 PubMed

Márová I, Kovář J. Spectrophotometric detection of bacteriolytic activity of diluted lysostaphin solutions. Folia Microbiol (Praha). 1993;38(2):153–8. 10.1007/BF02891699. PubMed DOI

Khan J, Tarar M, Gul I, Nawaz U, Arshad M. Challenges of antibiotic resistance biofilms and potential combating strategies: a review. 3 Biotech. 2021;11(4):169. 10.1007/s13205-021-02707-w. PubMed DOI PMC

Sikdar R, Elias M. Quorum quenching enzymes and their effects on virulence, biofilm, and microbiomes: a review of recent advances. Expert Rev Anti Infect Ther. 2020;18(12):1221–33. 10.1080/14787210.2020.1794815. PubMed DOI PMC

Sompiyachoke K, Elias MH. Engineering Quorum Quenching Acylases with Improved Kinetic and Biochemical Properties. bioRxiv [Preprint]. 2023 Sep 1:2023.09.01.555929. 10.1101/2023.09.01.555929. Update in: Protein Sci. 2024;33(4):e4954. doi: 10.1002/pro.4954. PubMed PMC

Deng W, Lei Y, Tang X, Li D, Liang J, Luo J, Liu L, Zhang W, Ye L, Kong J, Wang K, Chen Z. DNase inhibits early biofilm formation in PubMed DOI PMC

Quan Lin M, Sheng Y, Tian B, Li Z, Kang Y, Yang Z, Xu T, Soteyome L, Guo H, Sun Y, Gao L, Yu. Qiang Pan, Yulong Tan, Antibiofilm activity and synergistic effects of DNase I and lysostaphin against DOI

Vafina G, Zainutdinova E, Bulatov E, Filimonova MN. Endonuclease from Gram-negative Bacteria PubMed DOI PMC

Khwen NN. 2021. Purification and Characterization of Thermo Stable DNase of Staphylococcus Aureus Isolated from Different Clinical Source. 2021; 21(10.37506/mlu.v21i2.2879):1352–1358 DOI:10.37506/mlu.v21i2.2879.

Chandra P, Enespa, Singh R, Arora PK. Microbial lipases and their industrial applications: a comprehensive review. Microb Cell Fact. 2020;19(1):169. 10.1186/s12934-020-01428-8. PubMed DOI PMC

Ameri A, Shakibaie M, Sahami Z, Khoobi M, Forootanfar H. Statistical optimization of cultural medium composition of thermoalkalophilic lipase produced by a chemically induced mutant strain of Bacillus atrophaeus FSHM2. 3 Biotech. 2019;9(7):268. 10.1007/s13205-019-1789-2. PubMed DOI PMC

Wang S, Zhao Y, Breslawec AP, Liang T, Deng Z, Kuperman LL, Yu Q. Strategy to combat biofilms: a focus on biofilm dispersal enzymes. NPJ Biofilms Microbiomes. 2023;9(1):63. 10.1038/s41522-023-00427-y. PubMed DOI PMC

Kaur H, Kaur A, Soni SK, Rishi P. Microbially-derived cocktail of carbohydrases as an anti-biofouling agents: a ‘green approach’. Biofouling. 2022;38(5):455–81. 10.1080/08927014.2022.2085566. PubMed DOI

Zhang Y, Wei W, Wen H, Cheng Z, Mi Z, Zhang J, Liu X, Fan X. Targeting Multidrug-Recalcitrant Pseudomonas aeruginosa Biofilms: combined-enzyme treatment enhances antibiotic efficacy. Antimicrob Agents Chemother. 2023;67(1):e0135822. 10.1128/aac.01358-22. PubMed DOI PMC

Watters. C, Dickson BT, Nancy K, Millenbaugh J. Enzymatic degradation of in vitro Staphylococcus aureus biofilms supplemented with human plasma. Infect Drug Resist. 2016;9(1):71–8. 10.2147/IDR.S103101. PubMed DOI PMC

Ellis JR, Paul RPA. (2024). An apparent lack of synergy between degradative enzymes against Staphylococcus aureus biofilms. microPublication biology, 2024 10.17912/micropub.biology.001119 PubMed PMC

Pavlukhina SV, Kaplan JB, Xu L, Chang W, Yu X, Madhyastha S, Yakandawala N, Mentbayeva A, Khan B, Sukhishvili SA. Noneluting enzymatic antibiofilm coatings. ACS Appl Mater Interfaces. 2012;4(9):4708–16. 10.1021/am3010847. PubMed DOI PMC

Zhou Z, Li S, Wei G, Liu W, Zhang Y, Zhu C, Liu S, Li T, Wei H. 3. Cerium-Based Metal-Organic Framework with intrinsic haloperoxidase‐like activity for Antibiofilm formation. Adv Funct Mater. 2022. 10.1002/adfm.202206294. DOI

Khani M, Hansen MF, Knøchel S, Rasekh B, Ghasemipanah K, Zamir SM, Nosrati M, Burmølle M. Antifouling potential of enzymes applied to reverse osmosis membranes. Biofilm. 2023;5:100119. 10.1016/j.bioflm.2023.100119. PubMed DOI PMC

Devlin H, Fulaz S, Hiebner DW, O’Gara JP, Casey E. Enzyme-functionalized mesoporous silica nanoparticles to target PubMed DOI PMC

Grooters KE, Ku JC, Richter DM, Krinock MJ, Minor A, Li P, Kim A, Sawyer R, Li Y. Strategies for combating antibiotic resistance in bacterial biofilms. Front Cell Infect Microbiol. 2024;14:1352273. 10.3389/fcimb.2024.1352273. PubMed DOI PMC

Karyani TZ, Ghattavi S, Homaei A. Application of enzymes for targeted removal of biofilm and fouling from fouling-release surfaces in marine environments: a review. Int J Biol Macromol. 2023;253(Pt 5):127269. 10.1016/j.ijbiomac.2023.127269. PubMed DOI

Zhang Y, Liu X, Wen H, Cheng Z, Zhang Y, Zhang H, Mi Z, Fan X. Anti-biofilm enzymes-assisted antibiotic therapy against burn Wound infection by Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2023;67(7):e0030723. 10.1128/aac.00307-23. PubMed DOI PMC

Li Y, Dong R, Ma L, Qian Y, Liu Z. Combined Anti-biofilm enzymes strengthen the Eradicate Effect of Vibrio parahaemolyticus Biofilm: mechanism on cpsA-J expression and application on different carriers. Foods. 2022;11(9):1305. 10.3390/foods11091305. PubMed DOI PMC

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. 2017;71:94–100. 10.1016/j.foodcont.2016.06.038. DOI

Fang K, Park OJ, Hong SH. Controlling biofilms using synthetic biology approaches. Biotechnol Adv 2020 May-Jun;40:107518. 10.1016/j.biotechadv.2020.107518 PubMed PMC

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