Abstract
Biofilm, a microbial community formed by especially pathogenic and spoilage bacterial species, is a critical problem in the food industries. It is an important cause of continued contamination by foodborne pathogenic bacteria. Therefore, removing biofilm is the key to solving the high pollution caused by foodborne pathogenic bacteria in the food industry. Lactobacillus, a commonly recognized probiotic that is healthy for consumer, have been proven useful for isolating the potential biofilm inhibitors. However, the addition of surface components and metabolites of Lactobacillus is not a current widely adopted biofilm control strategy at present. This review focuses on the effects and preliminary mechanism of action on biofilm inhibition of Lactobacillus-derived components including lipoteichoic acid, exopolysaccharides, bacteriocins, secreted protein, organic acids and some new identified molecules. Further, the review discusses several modern biofilm identification techniques and particularly interesting new technology of biofilm inhibition molecules. These molecules exhibit stronger inhibition of biofilm formation, playing a pivotal role in food preservation and storage. Overall, this review article discusses the application of biofilm inhibitors produced by Lactobacillus, which would greatly aid efforts to eradicate undesirable bacteria from environment in the food industries.
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References
Abdalla AK, Ayyash MM, Olaimat AN et al (2021) Exopolysaccharides as antimicrobial agents: Mechanism and spectrum of activity. Frontiers in Microbiology 12, 664395.https://ARTN66439510.3389/fmicb.2021.664395
Abdullah N, Al-Marzooq F, Mohamad S et al (2019) Intraoral appliances for in situ oral biofilm growth: a systematic review. J Oral Microbiol 11:1647757. https://doi.org/10.1080/20002297.2019.1647757
Abebe GM (2020) The role of bacterial biofilm in antibiotic resistance and food contamination. Int J Microbiol 2020(1705814). https://doi.org/10.1155/2020/1705814
Ahn KB, Baik JE, Yun CH et al (2018a) Lipoteichoic acid inhibits Staphylococcus aureus biofilm formation. Front Microbiol 9.https://ARTN32710.3389/fmicb.2018.00327
Ahn KB, Baik JE, Yun CH et al (2018b) Lipoteichoic acid inhibits Staphylococcus aureus biofilm formation. Frontiers in Microbiology 9, 327.https://ARTN32710.3389/fmicb.2018.00327
Ameer S, Ibrahim H, Yaseen MU et al (2023) Electrochemical impedance spectroscopy-based sensing of biofilms: a comprehensive review. Biosens (Basel) 13. https://doi.org/10.3390/bios13080777
Amrutha B, Sundar K, Shetty PH (2017) Effect of organic acids on biofilm formation and quorum signaling of pathogens from fresh fruits and vegetables. Microb Pathogenesis 111:156–162. https://doi.org/10.1016/j.micpath.2017.08.042
Barbosa A, Miranda S, Azevedo NF et al (2023) Imaging biofilms using fluorescence in situ hybridization: seeing is believing. Front Cell Infect Microbiol 13:1195803. https://doi.org/10.3389/fcimb.2023.1195803
Caputo P, Di Martino MC, Perfetto B et al (2018) Use of MALDI-TOF-MS to discriminate between biofilm-producer and non-producer strains of Staphylococcus epidermidis. Int J Environ Res Public Health 15. https://doi.org/10.3390/ijerph15081695
Carrascosa C, Raheem D, Ramos F et al (2021) Microbial biofilms in the food industry-a comprehensive review. Int J Environ Res Public Health 18. https://doi.org/10.3390/ijerph18042014
Chandrakasan G, Rodriguez-Hernandez AI, Lopez-Cuellar MD et al (2019) Bacteriocin encapsulation for food and pharmaceutical applications: advances in the past 20 years. Biotechnol Lett 41:453–469. https://doi.org/10.1007/s10529-018-02635-5
Ciandrini E, Campana R, Casettari L et al (2016) Characterization of biosurfactants produced by Lactobacillus spp and their activity against oral Streptococci biofilm. Appl Microbiol Biot 100:6767–6777. https://doi.org/10.1007/s00253-016-7531-7
Cicenia A, Scirocco A, Carabotti M et al (2014) Postbiotic activities of Lactobacilli-derived factors. J Clin Gastroenterol 48:S18–S22. https://doi.org/10.1097/Mcg.0000000000000231
Coughlan LM, Cotter PD, Hill C et al (2016) New weapons to fight old enemies: novel strategies for the (bio)control of bacterial biofilms in the food industry. Front Microbiol 7:1641. https://doi.org/10.3389/fmicb.2016.01641
Dar D, Dar N, Cai L et al (2021) Spatial transcriptomics of planktonic and sessile bacterial populations at single-cell resolution. Sci 373. https://doi.org/10.1126/science.abi4882
De Carvalho MP, Abraham WR (2012) Antimicrobial and biofilm inhibiting diketopiperazines. Curr Med Chem 19:3564–3577
Díaz MA, Alberto MR, Vega-Hissi EG et al (2022) Interference in Staphylococcus aureus biofilm and virulence factors production by human probiotic bacteria with antimutagenic activity. Arab J Sci Eng 47:241–253. https://doi.org/10.1007/s13369-021-05934-8
Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633. https://doi.org/10.1038/nrmicro2415
Gao QX, Gao Q, Min MH et al (2016) Ability of Lactobacillus plantarum lipoteichoic acid to inhibit Vibrio anguillarum-induced inflammation and apoptosis in silvery pomfret (pampus argenteus) intestinal epithelial cells. Fish Shellfish Immun 54:573–579. https://doi.org/10.1016/j.fsi.2016.05.013
Ghafoor Aamir Z-u-F, Javed Aqeel (2014) Pseudomonas aeruginosa biofilm: role of exopolysaccharides in the function and architecture of the biofilm. J Inf Mol Biol 2:61–73. https://doi.org/10.1128/AEM.00637-11
Giordani B, Parolin C, Vitali B (2021) Lactobacilli as anti-biofilm strategy in oral infectious diseases: a mini-review. Front Med Technol 3:769172. https://doi.org/10.3389/fmedt.2021.769172
Hor YY, Liong MT (2014) Use of extracellular extracts of lactic acid bacteria and bifidobacteria for the inhibition of dermatological pathogen Staphylococcus aureus. Dermatol Sin 32:141–147. https://doi.org/10.1016/j.dsi.2014.03.001
Hossain MI, Mizan MFR, Roy PK et al (2021) Listeria monocytogenes biofilm inhibition on food contact surfaces by application of postbiotics from Lactobacillus curvatus B.67 and Lactobacillus plantarum M.2. Food Res Int 148, 110595. https://doi.org/10.1016/j.foodres.2021.110595
İncili GK, Karatepe P, Akgöl M et al (2021) Characterization of Pediococcus acidilactici postbiotic and impact of postbiotic-fortified chitosan coating on the microbial and chemical quality of chicken breast fillets. Int J Biol Macromol 184:429–437. https://doi.org/10.1016/j.ijbiomac.2021.06.106
Islam ST, Lam JS (2014) Synthesis of bacterial polysaccharides via the Wzx/Wzy-dependent pathway. Can J Microbiol 60:697–716. https://doi.org/10.1139/cjm-2014-0595
Jung S, Park OJ, Kim AR et al (2019) Lipoteichoic acids of Lactobacilli inhibit Enterococcus faecalis biofilm formation and disrupt the preformed biofilm. J Microbiol 57:310–315. https://doi.org/10.1007/s12275-019-8538-4
Kang SS, Sim JR, Yun CH et al (2016) Lipoteichoic acids as a major virulence factor causing inflammatory responses via toll-like receptor 2. Arch Pharm Res 39:1519–1529. https://doi.org/10.1007/s12272-016-0804-y
Kang MS, Lim HS, Oh JS et al (2017) Antimicrobial activity of Lactobacillus salivarius and Lactobacillus fermentum against Staphylococcus aureus. Pathog Dis 75:ftx009. https://doi.org/10.1093/femspd/ftx009
Khalid AS, Niaz T, Zarif B et al (2022) Milk phospholipids-based nanostructures functionalized with rhamnolipids and bacteriocin: intrinsic and synergistic antimicrobial activity for cheese preservation. Food Biosci 47:101442. https://doi.org/10.1016/j.fbio.2021.101442
Kim AR, Ahn KB, Yun CH et al (2019) Lactobacillus plantarum lipoteichoic acid inhibits oral multispecies biofilm. J Endodont 45:310–315. https://doi.org/10.1016/j.joen.2018.12.007
Koohestani M, Moradi M, Tajik H et al (2018) Effects of cell-free supernatant of Lactobacillus acidophilus LA5 and Lactobacillus casei 431 against planktonic form and biofilm of Staphylococcus aureus. Vet Res Forum 9:301–306. https://doi.org/10.30466/vrf.2018.33086
Kumariya R, Garsa AK, Rajput YS et al (2019) Bacteriocins: classification, synthesis, mechanism of action and resistance development in food spoilage causing bacteria. Microb Pathogenesis 128:171–177. https://doi.org/10.1016/j.micpath.2019.01.002
Lee D, Im J, Park DH et al (2021) Lactobacillus plantarum lipoteichoic acids possess strain-specific regulatory effects on the biofilm formation of dental pathogenic bacteria. Frontiers in Microbiology 12, 758161.https://ARTN75816110.3389/fmicb.2021.758161
Li J, Wu Y, Zhang Q et al (2022a) Optimization of environmental factors in a dual in vitro biofilm model of Candida albicans-Streptococcus mutans. Lett Appl Microbiol 75:869–880. https://doi.org/10.1111/lam.13761
Li Y, Chen N, Wu Q et al (2022b) A flagella hook coding gene flge positively affects biofilm formation and cereulide production in emetic Bacillus cereus. Front Microbiol 13:897836. https://doi.org/10.3389/fmicb.2022.897836
Li J, Zhang Q, Zhao J et al (2022c) Streptococcus mutans and Candida albicans biofilm inhibitors produced by lactiplantibacillus plantarum CCFM8724. Curr Microbiol 79(143). https://doi.org/10.1007/s00284-022-02833-5
Liu Y, Zhang J, Ji YD (2020) Environmental factors modulate biofilm formation by Staphylococcus aureus. Sci Progress-Uk 103:1–14. https://doi.org/10.1177/0036850419898659
Liu T, Zhai Y, Jeong KC (2023) Advancing understanding of microbial biofilms through machine learning-powered studies. Food Sci Biotechnol 32:1653–1664. https://doi.org/10.1007/s10068-023-01415-w
Luo LL, Yi LH, Chen JX et al (2021) Antibacterial mechanisms of bacteriocin BM1157 against Escherichia coli and Cronobacter sakazakii. Food Control 123:107730. https://doi.org/10.1016/j.foodcont.2020.107730
Maffei B, Francetic O, Subtil A (2017) Tracking proteins secreted by bacteria: What’s in the toolbox. Front Cell Infect Mi 7, 221.https://ARTN22110.3389/fcimb.2017.00221
Mani-López E, Arrioja-Bretón D, López-Malo A (2022) The impacts of antimicrobial and antifungal activity of cell-free supernatants from lactic acid bacteria in vitro and foods. Compr Rev Food Sci Food Saf 21:604–641. https://doi.org/10.1111/1541-4337.12872
Mejia-Pitta A, Broset E, de la Fuente-Nunez CD (2021) Probiotic engineering strategies for the heterologous production of antimicrobial peptides. Adv Drug Deliver Rev 176, 113863.https://ARTN11386310.1016/j.addr.2021.113863
Merino L, Procura F, Trejo FM et al (2019) Biofilm formation by Salmonella sp In the poultry industry: Detection, control and eradication strategies. Food Res Int 119, 530–540. https://doi.org/10.1016/j.foodres.2017.11.024
Misra S, Pandey P, Dalbhagat CG et al (2022) Emerging technologies and coating materials for improved probiotication in food products: a review. Food Bioproc Tech 15:998–1039. https://doi.org/10.1007/s11947-021-02753-5
Moradi M, Mardani K, Tajik H (2019) Characterization and application of postbiotics of Lactobacillus spp. On Listeria monocytogenes in vitro and in food models. Lwt-Food Sci Technol 111:457–464. https://doi.org/10.1016/j.lwt.2019.05.072
Morillo-Lopez V, Sjaarda A, Islam I et al (2022) Corncob structures in dental plaque reveal microhabitat taxon specificity. Microbiome 10:145. https://doi.org/10.1186/s40168-022-01323-x
Neu TR, Lawrence JR (2015) Innovative techniques, sensors, and approaches for imaging biofilms at different scales. Trends Microbiol 23:233–242. https://doi.org/10.1016/j.tim.2014.12.010
Niaz T, Shabbir S, Noor T et al (2019) Antimicrobial and antibiofilm potential of bacteriocin loaded nano-vesicles functionalized with rhamnolipids against foodborne pathogens. LWT-Food Sci Technol 116, 108583.https://ARTN10858310.1016/j.lwt.2019.108583
Pang XY, Song XY, Chen MJ et al (2022) Combating biofilms of foodborne pathogens with bacteriocins by lactic acid bacteria in the food industry. Compr Rev Food Sci F 21:1657–1676. https://doi.org/10.1111/1541-4337.12922
Patel M, Siddiqui AJ, Hamadou WS et al (2021) Inhibition of bacterial adhesion and antibiofilm activities of a glycolipid biosurfactant from Lactobacillus rhamnosus with its physicochemical and functional properties. Antibiotics-Basel. 10.https://ARTN154610.3390/antibiotics10121546
Pelyuntha W, Chaiyasut C, Kantachote D et al (2020) Organic acids and 2,4-di-tert-butylphenol: major compounds of Weissella confusa WM36 cell-free supernatant against growth, survival and virulence of Salmonella typhi. PeerJ 8. https://doi.org/10.7717/peerj.8410
Pradeepa ADS, Koshi Matthews AR, Hegde B, Akshatha AB, Mathias S, Mutalik SM, Vidya (2016) Multidrug resistant pathogenic bacterial biofilm inhibition by Lactobacillus plantarum exopolysaccharide. Bioactive Carbohydr Diet Fibre 8:7–14
Rajoka MSR, Jin ML, Zhao HB et al (2018) Functional characterization and biotechnological potential of exopolysaccharide produced by Lactobacillus rhamnosus strains isolated from human breast milk. LWT-Food Sci Technol 89:638–647. https://doi.org/10.1016/j.lwt.2017.11.034
Rajoka MSR, Wu YG, Mehwish HM et al (2020) Exopolysaccharides: new perspectives on engineering strategies, physiochemical functions, and immunomodulatory effects on host health. Trends Food Sci Tech 103:36–48. https://doi.org/10.1016/j.tifs.2020.06.003
Relucenti M, Familiari G, Donfrancesco O et al (2021) Microscopy methods for biofilm imaging: focus on sem and vp-sem pros and cons. Biology (Basel). https://doi.org/10.3390/biology10010051
Renu A (2022) Biofilm. India: New India Publishing Agency. ISBN: 9789395319157
Renye JA, Somkuti GA (2008) Cloning of milk-derived bioactive peptides in Streptococcus thermophilus. Biotechnol Lett 30:723–730. https://doi.org/10.1007/s10529-007-9600-6
Romero-Luna HE, Hernández-Mendoza A, González-Córdova AF et al (2022) Bioactive peptides produced by engineered probiotics and other food-grade bacteria: a review. Food Chem X 13:100196. https://doi.org/10.1016/j.fochx.2021.100196
Said J, Walker M, Parsons D et al (2015) Development of a flow system for studying biofilm formation on medical devices with microcalorimetry. Methods 76:35–40. https://doi.org/10.1016/j.ymeth.2014.12.002
Sanchez B, Urdaci MC (2012) Extracellular proteins from Lactobacillus plantarum BMCM12 prevent adhesion of enteropathogens to mucin. Curr Microbiol 64:592–596. https://doi.org/10.1007/s00284-012-0115-6
Ser HL, Palanisamy UD, Yin WF et al (2015) Presence of antioxidative agent, pyrrolo [1,2-a] pyrazine-1,4-dione, hexahydro- in newly isolated Streptomyces mangrovisoli sp nov. Frontiers in Microbiology 6, 854.https://ARTN85410.3389/fmicb.2015.00354
Sharan M, Vijay D, Dhaka P et al (2022) Biofilms as a microbial hazard in the food industry: a scoping review. J Appl Microbiol 133:2210–2234. https://doi.org/10.1111/jam.15766
Shin JM, Luo T, Lee KH et al (2018) Deciphering endodontic microbial communities by next-generation sequencing. J Endod 44:1080–1087. https://doi.org/10.1016/j.joen.2018.04.003
Shiraishi T, Yokota S, Morita N et al (2013) Characterization of a Lactobacillus gasseri JCM 1131 lipoteichoic acid with a novel glycolipid anchor structure (79, Pg 3315, 2013). Appl Environ Microb 79:7931–7931. https://doi.org/10.1128/Aem.03100-13
Shokri D, Khorasgani MR, Mohkam M et al (2018) The inhibition effect of Lactobacilli against growth and biofilm formation of Pseudomonas aeruginosa. Probiotics Antimicro 10:34–42. https://doi.org/10.1007/s12602-017-9267-9
Silva NBS, Marques LA, Röder DDB (2021) Diagnosis of biofilm infections: current methods used, challenges and perspectives for the future. J Appl Microbiol 131:2148–2160. https://doi.org/10.1111/jam.15049
Sivasankar P, Seedevi P, Poongodi S et al (2018) Characterization, antimicrobial and antioxidant property of exopolysaccharide mediated silver nanoparticles synthesized by Streptomyces violaceus MM72. Carbohyd Polym 181:752–759. https://doi.org/10.1016/j.carbpol.2017.11.082
Soderling EM, Marttinen AM, Haukioja AL (2011) Probiotic lactobacilli interfere with Streptococcus mutans biofilm formation in vitro. Curr Microbiol 62:618–622. https://doi.org/10.1007/s00284-010-9752-9
Tomé AR, Carvalho FM, Teixeira-Santos R et al (2023) Use of probiotics to control biofilm formation in food industries. Antibiot (Basel) 12. https://doi.org/10.3390/antibiotics12040754
Vélez MP, Verhoeven TLA, Draing C et al (2007) Functional analysis of D-alanylation of lipoteichoic acid in the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microb 73:3595–3604. https://doi.org/10.1128/Aem.02083-06
Verderosa AD, Totsika M, Fairfull-Smith KE (2019) Bacterial biofilm eradication agents: A current review. Front Chem 7, 824.https://ARTN82410.3389/fchem.2019.00824
Wang R (2019) Biofilms and meat safety: a mini-review. J Food Prot 82:120–127. https://doi.org/10.4315/0362-028X.JFP-18-311
Wang YQ, Wu JT, Lv MX et al (2021) Metabolism characteristics of lactic acid bacteria and the expanding applications in food industry. Front Bioeng Biotech 9:612285. https://doi.org/10.3389/fbioe.2021.612285
Weidenmaier C, Peschel A (2008) Teichoic acids and related cell-wall glycopolymers in gram-positive physiology and host interactions. Nat Rev Microbiol 6:276–287. https://doi.org/10.1038/nrmicro1861
Winkelstroter LK, Tulini FL, De Martinis ECP (2015) Identification of the bacteriocin produced by cheese isolate Lactobacillus paraplantarum FT259 and its potential influence on Listeria monocytogenes biofilm formation. Lwt-Food Sci Technol 64:586–592. https://doi.org/10.1016/j.lwt.2015.06.014
Wright CJ, Shah MK, Powell LC et al (2010) Application of afm from microbial cell to biofilm. Scanning 32:134–149. https://doi.org/10.1002/sca.20193
Xu XQ, Peng Q, Zhang YW et al (2020) A novel exopolysaccharide produced by Lactobacillus coryniformis NA-3 exhibits antioxidant and biofilm-inhibiting properties in vitro. Food Nutr Res 64, 3744–3757.https://ARTN374410.29219/fnr.v64.3744
Xu ZQ, Yang QL, Zhu YL (2022) Transcriptome analysis reveals the molecular mechanisms of the novel Lactobacillus pentosus pentocin against Bacillus cereus. Food Res Int 151, 110840.https://ARTN11084010.1016/j.foodres.2021.110840
Yin W, Wang YT, Liu L et al (2019) Biofilms: The microbial protective clothing in extreme environments. Int J Mol Sci 20, 3423.https://ARTN342310.3390/ijms20143423
Zhang QQ, Zhang YH, Cai FY et al (2019) Comparative antibacterial and antibiofilm activities of garlic extracts, nisin, ε-polylysine, and citric acid on Bacillus subtilis. J Food Process Preserv 43. https://doi.org/10.1111/jfpp.14179
Acknowledgements
This work was supported by the National Natural Science Foundation of China (No. 32072197, 32021005), National First-class Discipline Program of Food Science and Technology (JUFSTR20180102), and Collaborative innovation center of food safety and quality control in Jiangsu Province.
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J.L. contributed to literature search, drafted and critically revised the manuscript. Q.Z. contributed to guide the topic of this article, critically reviewed and revised the manuscript. J.Z., H.Z., and W.C. Contributed to conception and critically revised the manuscript. All authors gave their final approval and agree to be accountable for all aspects of the work.
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Li, J., Zhang, Q., Zhao, J. et al. Lactobacillus-derived components for inhibiting biofilm formation in the food industry. World J Microbiol Biotechnol 40, 117 (2024). https://doi.org/10.1007/s11274-024-03933-z
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DOI: https://doi.org/10.1007/s11274-024-03933-z