Skip to main content

Advertisement

SpringerLink
Log in

Advancing understanding of microbial biofilms through machine learning-powered studies

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

Abstract

Microbial biofilms are prevalent in various environments and pose significant challenges to food safety and public health. The biofilms formed by pathogens can cause food spoilage, foodborne illness, and infectious diseases, which are difficult to treat due to their enhanced antimicrobial resistance. While the composition and development of biofilms have been widely studied, their profound impact on food, the food industry, and public health has not been sufficiently recapitulated. This review aims to provide a comprehensive overview of microbial biofilms in the food industry and their implication on public health. It highlights the existence of biofilms along the food-producing chains and the underlying mechanisms of biofilm-associated diseases. Furthermore, this review thoroughly summarizes the enhanced understanding of microbial biofilms achieved through machine learning approaches in biofilm research. By consolidating existing knowledge, this review intends to facilitate developing effective strategies to combat biofilm-associated infections in both the food industry and public health.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abdallah M, Benoliel C, Drider D, Dhulster P, Chihib N-E. Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments. Archives of Microbiology. 196: 453-472 (2014)

    Article  CAS  PubMed  Google Scholar 

  • Abebe GM. The role of bacterial biofilm in antibiotic resistance and food contamination. International Journal of Microbiology. 2020: 1705814 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  • Addis, MF, Cubeddu T, Pilicchi Y, Rocca S, Piccinini R. Chronic intramammary infection by Listeria monocytogenes in a clinically healthy goat–a case report. BMC Veterinary Research 15: 1-7 (2019)

    Article  CAS  Google Scholar 

  • Ahmed MN, Porse A, Sommer MOA, Høiby N, Ciofu O. Evolution of antibiotic resistance in biofilm and planktonic Pseudomonas aeruginosa populations exposed to subinhibitory levels of ciprofloxacin. Antimicrobial Agents and Chemotherapy. 62: e00320-00318 (2018)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderl JN, Zahller J, Roe F, Stewart PS. Role of nutrient limitation and stationary-phase existence in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrobial Agents and Chemotherapy. 47: 1251-1256 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrade KM, Silva BPM, De Oliveira LR, Cury PR. Automatic dental biofilm detection based on deep learning. Journal of Clinical Periodontol. 50: 571-581 (2023)

    Article  Google Scholar 

  • Artini M, Patsilinakos A, Papa R, Bozovic M, Sabatino M, Garzoli S, Vrenna G, Tilotta M, Pepi F, Ragno R, Selan L. Antimicrobial and antibiofilm activity and machine learning classification analysis of essential oils from different mediterranean plants against Pseudomonas aeruginosa. Molecules. 23:482 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Auger S, Ramarao N, Faille C, Fouet A, Aymerich S, Gohar M. Biofilm formation and cell surface properties among pathogenic and nonpathogenic strains of the Bacillus cereus group. Applied and Environmental Microbiology. 75: 6616-6618 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Battin TJ, Sloan WT, Kjelleberg S, Daims H, Head IM, Curtis TP, Eberl L. Microbial landscapes: new paths to biofilm research. Nature Reviews Microbiology. 5: 76-81 (2007)

    Article  CAS  PubMed  Google Scholar 

  • Baumgartner M, Lang M, Holley H, Crepaz D, Hausmann B, Pjevac P, Moser D, Haller F, Hof F, Beer A, Orgler E, Frick A, Khare V, Evstatiev R, Strohmaier S, Primas C, Dolak W, Kocher T, Klavins K, Rath T, Neurath MF, Berry D, Makristathis A, Muttenthaler M, Gasche C. Mucosal Biofilms Are an Endoscopic Feature of Irritable Bowel Syndrome and Ulcerative Colitis. Gastroenterology. 161: 1245-1256 e1220 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Berg S, Kutra D, Kroeger T, Straehle CN, Kausler BX, Haubold C, Schiegg M, Ales J, Beier T, Rudy M, Eren K, Cervantes JI, Xu B, Beuttenmueller F, Wolny A, Zhang C, Koethe U, Hamprecht FA, Kreshuk A. ilastik: interactive machine learning for (bio)image analysis. Nature Methods. 16: 1226-1232 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Berne C, Ellison CK, Ducret A, Brun YV. Bacterial adhesion at the single-cell level. Nature Reviews Microbiology. 16: 616-627 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Bottone EJ. Bacillus cereus, a volatile human pathogen. Clinical Microbiology Reviews. 23: 382-398 (2010)

    Article  PubMed  PubMed Central  Google Scholar 

  • Breiman L. Random forests. Mach Learning. 45: 5-32 (2001)

    Google Scholar 

  • Breiman L, Friedman JH, Olshen RA, Stone CJ. Classification and Regression Trees. 1st ed. Wadsworth, New York, NY, USA (1984)

    Google Scholar 

  • Cámara M, Green W, Macphee CE, Rakowska PD, Raval R, Richardson MC, Slater-Jefferies J, Steventon K, Webb JS. Economic significance of biofilms: a multidisciplinary and cross-sectoral challenge. npj Biofilms and Microbiomes. 8: 42 (2022)

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao Y, Li X, Li F, Song H. CRISPRi-sRNA: transcriptional-translational regulation of extracellular electron transfer in Shewanella oneidensis. ACS Synthetic Biology. 6: 1679-1690 (2017)

    Article  CAS  PubMed  Google Scholar 

  • Carniello V, Peterson BW, Van Der Mei HC, Busscher HJ. Physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth. Advances in Colloid and Interface Science. 261: 1-14 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Carrascosa C, Raheem D, Ramos F, Saraiva A, Raposo A. Microbial biofilms in the food industry-A comprehensive review. International Journal of Environmental Research and Public Health. 18: 2014 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciofu O, Johansen HK, Aanaes K, Wassermann T, Alhede M, Von Buchwald C, Høiby N. P. aeruginosa in the paranasal sinuses and transplanted lungs have similar adaptive mutations as isolates from chronically infected CF lungs. Journal of Cystic Fibrosis. 12: 729-736 (2013)

    Article  PubMed  Google Scholar 

  • Ciofu O, Moser C, Jensen PØ, Høiby N. Tolerance and resistance of microbial biofilms. Nature Reviews Microbiology. 20: 621-635 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Costerton J, Lam J, Lam K, Chan R. The role of the microcolony mode of growth in the pathogenesis of Pseudomonas aeruginosa infections. Reviews of Infectious Diseases. 5: S867-S873 (1983)

    Article  PubMed  Google Scholar 

  • Cover TM, Hart PE. Nearest Neighbor Pattern Classification. Ieee Transactions on Inform Theory. 13: 21-27 (1967)

    Article  Google Scholar 

  • Cox DR, The Regression-Analysis of Binary Sequences. Journal of Royal Statistical Society. 20: 215-242 (1958)

    Google Scholar 

  • Cruz CD, Shah S, Tammela P. Defining conditions for biofilm inhibition and eradication assays for Gram-positive clinical reference strains. BMC Microbiology. 18: 1-9 (2018)

    Article  Google Scholar 

  • Cutler NA, Chaput DL, Oliver AE, Viles HA. The spatial organization and microbial community structure of an epilithic biofilm. FEMS Microbiology Ecology. 91: fiu027 (2015)

    Article  PubMed  Google Scholar 

  • Dar D, Dar N, Cai L, Newman DK. Spatial transcriptomics of planktonic and sessile bacterial populations at single-cell resolution. Science. 373: eabi4882 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dasgupta D, Ghosh R, Sengupta TK. Biofilm-mediated enhanced crude oil degradation by newly isolated Pseudomonas species. International Scholarly Research Notices. 2013: 250749 (2013)

    Google Scholar 

  • Delcaru C, Alexandru I, Podgoreanu P, Grosu M, Stavropoulos E, Chifiriuc MC, Lazar V. Microbial biofilms in urinary tract infections and prostatitis: Etiology, pathogenicity, and combating strategies. Pathogens. 5: 65 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  • Donlan RM. Biofilms: microbial life on surfaces. Emerging Infectious Diseases. 8: 881 (2002)

    Article  PubMed  PubMed Central  Google Scholar 

  • Dourou D, Ammor MS, Skandamis PN, Nychas G-JE. Growth of Salmonella enteritidis and Salmonella typhimurium in the presence of quorum sensing signalling compounds produced by spoilage and pathogenic bacteria. Food Microbiology. 28: 1011-1018 (2011)

    Article  CAS  PubMed  Google Scholar 

  • Dourou D, Beauchamp CS, Yoon Y, Geornaras I, Belk KE, Smith GC, Nychas G-JE, Sofos JN. Attachment and biofilm formation by Escherichia coli O157: H7 at different temperatures, on various food-contact surfaces encountered in beef processing. International Journal of Food Microbiology. 149: 262-268 (2011)

    Article  PubMed  Google Scholar 

  • El-Naggar NE, Dalal SR, Zweil AM, Eltarahony M. Artificial intelligence-based optimization for chitosan nanoparticles biosynthesis, characterization and in‑vitro assessment of its anti-biofilm potentiality. Scientific Reports. 13: 4401 (2023)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El Hag M, Feng Z, Su Y, Wang X, Yassin A, Chen S, Peng D, Liu X. Contribution of the csgA and bcsA genes to Salmonella enterica serovar Pullorum biofilm formation and virulence. Avian Pathology. 46: 541-547 (2017)

    Article  PubMed  Google Scholar 

  • Fallah Atanaki F, Behrouzi S, Ariaeenejad S, Boroomand A, Kavousi K. BIPEP: Sequence-based prediction of biofilm inhibitory peptides using a combination of NMR and physicochemical descriptors. ACS Omega. 5: 7290–7297 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fleming D, Rumbaugh KP. Approaches to dispersing medical biofilms. Microorganisms. 5: 15 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Flores-Mireles AL, Walker JN, Bauman TM, Potretzke AM, Schreiber HL, Park AM, Pinkner JS, Caparon MG, Hultgren SJ, Desai A. Fibrinogen release and deposition on urinary catheters placed during urological procedures. The Journal of Urology. 196: 416-421 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  • Frederick MR, Kuttler C, Hense BA, Eberl HJ. A mathematical model of quorum sensing regulated EPS production in biofilm communities. Theoretical Biology and Medical Modelling. 8: 1-29 (2011)

    Article  Google Scholar 

  • Friedman JH. Greedy function approximation: A gradient boosting machine. The Annals of Statistics 29: 1189-1232 (2001)

    Article  Google Scholar 

  • Galie 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 

  • Garvey M. Mycobacterium avium paratuberculosis: a disease burden on the dairy industry. Animals. 10: 1773 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  • Giaouris E, Heir E, Desvaux M, Hébraud M, Møretrø T, Langsrud S, Doulgeraki A, Nychas G-J, Kačániová M, Czaczyk K. Intra-and inter-species interactions within biofilms of important foodborne bacterial pathogens. Frontiers in Microbiology. 6: 841 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  • González JF, Alberts H, Lee J, Doolittle L, Gunn JS. Biofilm formation protects Salmonella from the antibiotic ciprofloxacin in vitro and in vivo in the mouse model of chronic carriage. Scientific reports. 8: 222 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Götz F. MicroReview: Staphylococcus and biofilms. Molelular Microbiology. 43: 1367-1378 (2002)

    Article  Google Scholar 

  • Grigore-Gurgu L, Bucur FI, Borda D, Alexa E-A, Neagu C, Nicolau AI. Biofilms formed by pathogens in food and food processing environments. pp. 213-230. In: Bacterial Biofilms. Dincer S, Özdenefe MS, Arkut A (eds). IntechOpen (2019)

    Google Scholar 

  • Gupta S, Sharma AK, Jaiswal SK, Sharma VK. Prediction of biofilm inhibiting peptides: an in silico approach. Frontiers in Microbiolology. 7: 949 (2016)

    Google Scholar 

  • Hahn MM, Gunn JS. Salmonella extracellular polymeric substances modulate innate phagocyte activity and enhance tolerance of biofilm-associated bacteria to oxidative stress. Microorganisms. 8: 253 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nature Reviews Microbiology. 2: 95-108 (2004)

    Article  CAS  PubMed  Google Scholar 

  • Hall-Stoodley L, Stoodley P. Developmental regulation of microbial biofilms. Current Opinion in Biotechnology. 13: 228-233 (2002)

    Article  CAS  PubMed  Google Scholar 

  • Haney EF, Brito-Sanchez Y, Trimble MJ, Mansour SC, Cherkasov A, Hancock REW. Computer-aided discovery of peptides that specifically attack bacterial biofilms. Scientific Reports. 8: 1871 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Harrell JE, Hahn MM, D’souza SJ, Vasicek EM, Sandala JL, Gunn JS, Mclachlan JB. Salmonella biofilm formation, chronic infection, and immunity within the intestine and hepatobiliary tract. Frontiers in Cellular and Infection Microbiology. 10: 624622 (2021)

    Article  PubMed  PubMed Central  Google Scholar 

  • Hartman TW, Radichev E, Ali HM, Alaba MO, Hoffman M, Kassa G, Sani R, Gadhamshetty V, Ragi S, Messerli SM, De La Puente P, Sandhurst ES, Do T, Lushbough C, Gnimpieba EZ. BASIN: A semi-automatic workflow, with machine learning segmentation, for objective statistical analysis of biomedical and biofilm image datasets. Journal of Molecular Biology. 435: 167895 (2023)

    Article  CAS  PubMed  Google Scholar 

  • Hausner M, Wuertz S. High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Applied and Environmental Microbiology. 65: 3710-3713 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heimisdottir LH, Lin BM, Cho H, Orlenko A, Ribeiro AA, Simon-Soro A, Roach J, Shungin D, Ginnis J, Simancas-Pallares MA, Spangler HD, Zandona AGF, Wright JT, Ramamoorthy P, Moore JH, Koo H, Wu D, Divaris K. Metabolomics insights in early childhood caries. Journal of Dental Research. 100: 615-622 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hensen S, Pavičić M, Lohuis J, De Hoog J, Poutrel B. Location of Staphylococcus aureus within the experimentally infected bovine udder and the expression of capsular polysaccharide type 5 in situ. Journal of Dairy Science. 83: 1966-1975 (2000)

    Article  CAS  PubMed  Google Scholar 

  • Hogardt M, Heesemann J. Microevolution of Pseudomonas aeruginosa to a chronic pathogen of the cystic fibrosis lung. Between Pathogenicity and Commensalism. 91-118 (2012)

    Article  Google Scholar 

  • Høiby N, Bjarnsholt T, Moser C, Bassi G, Coenye T, Donelli G, Hall-Stoodley L, Holá V, Imbert C, Kirketerp-Møller K. ESCMID guideline for the diagnosis and treatment of biofilm infections 2014. Clinical Microbiology and Infection. 21: S1-S25 (2015)

    Article  PubMed  Google Scholar 

  • Hopfield JJ. Neural networks and physical systems with emergent collective computational abilities. Proceeding of the National Academy of Science. 79: 2554-2558 (1982)

    Article  CAS  Google Scholar 

  • Jacques M, Aragon V, Tremblay YD. Biofilm formation in bacterial pathogens of veterinary importance. Animal Health Research Reviews. 11: 97-121 (2010)

    Article  PubMed  Google Scholar 

  • Jiao Y, Qian F, Li Y, Wang G, Saltikov CW, Gralnick JA. Deciphering the electron transport pathway for graphene oxide reduction by Shewanella oneidensis MR-1. Journal of Bacteriology. 193: 3662-3665 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaplan JÁ. Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. Journal of Dental Research. 89: 205-218 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khoury ZH, Vila T, Puthran TR, Sultan AS, Montelongo-Jauregui D, Melo MaS, Jabra-Rizk MA. The role of Candida albicans secreted polysaccharides in augmenting Streptococcus mutans adherence and mixed biofilm formation: in vitro and in vivo studies. Frontiers in Microbiology. 11: 307 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  • Klein RD, Hultgren SJ. Urinary tract infections: microbial pathogenesis, host–pathogen interactions and new treatment strategies. Nature Reviews Microbiology. 18: 211-226 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konieczny M, Rhein P, Czaczyk K, Bialas W, Juzwa W. Imaging flow cytometry to study biofilm-associated microbial aggregates. Molecules. 26: 7096 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kostakioti M, Hadjifrangiskou M, Hultgren SJ. Bacterial biofilms: development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harbor Perspectives in Medicine. 3: a010306 (2013)

    Article  PubMed  PubMed Central  Google Scholar 

  • Kovatcheva‐Datchary P, Egert M, Maathuis A, Rajilić‐Stojanović M, De Graaf AA, Smidt H, De Vos WM, Venema K. Linking phylogenetic identities of bacteria to starch fermentation in an in vitro model of the large intestine by RNA‐based stable isotope probing. Environmental Microbiology. 11: 914-926 (2009)

    Article  CAS  PubMed  Google Scholar 

  • Kranjec C, Morales Angeles D, Torrissen Mårli M, Fernández L, García P, Kjos M, Diep DB. Staphylococcal biofilms: Challenges and novel therapeutic perspectives. Antibiotics. 10: 131 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuroki R, Kawakami K, Qin L, Kaji C, Watanabe K, Kimura Y, Ishiguro C, Tanimura S, Tsuchiya Y, Hamaguchi I. Nosocomial bacteremia caused by biofilm-forming Bacillus cereus and Bacillus thuringiensis. Internal Medicine. 48: 791-796 (2009)

    Article  PubMed  Google Scholar 

  • Lakicevic B, Nastasijevic I, Raseta M. Sources of Listeria monocytogenes contamination in retail establishments. Procedia Food Science. 5: 160-163 (2015)

    Article  Google Scholar 

  • Latorre A, Van Kessel J, Karns J, Zurakowski M, Pradhan A, Boor K, Jayarao B, Houser B, Daugherty C, Schukken Y. Biofilm in milking equipment on a dairy farm as a potential source of bulk tank milk contamination with Listeria monocytogenes. Journal of Dairy Science. 93: 2792-2802 (2010)

    Article  CAS  PubMed  Google Scholar 

  • Lee K, Yoon SS. Pseudomonas aeruginosa biofilm, a programmed bacterial life for fitness. Journal of Microbiology and Biotechnology. 28: 1053-1064 (2017)

    Article  Google Scholar 

  • Li F, Li Y, Sun L, Chen X, An X, Yin C, Cao Y, Wu H, Song H. Modular engineering intracellular NADH regeneration boosts extracellular electron transfer of Shewanella oneidensis MR-1. ACS Synthetic Biology. 7: 885-895 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Li F, Yin C, Sun L, Li Y, Guo X, Song H. Synthetic Klebsiella pneumoniae‐Shewanella oneidensis consortium enables glycerol‐fed high‐performance microbial fuel cells. Biotechnology Journal. 13: 1700491 (2018)

    Article  Google Scholar 

  • Li G, Tang JX. Accumulation of microswimmers near a surface mediated by collision and rotational Brownian motion. Physical Review Letters. 103: 078101 (2009)

    Article  PubMed  PubMed Central  Google Scholar 

  • Liaqat M, Mahmood M, Akram M, Arshad M, Aslam R, Khan M, Khan M, Fatima N, Ali S. Bacterial biofilms and their regulatory approaches. One Health Triad, Unique Scientific Publishers, Faisalabad, Pakistan. 2: 8-17 (2023)

    Google Scholar 

  • Lieke T, Meinelt T, Hoseinifar SH, Pan B, Straus DL, Steinberg CE. Sustainable aquaculture requires environmental‐friendly treatment strategies for fish diseases. Reviews in Aquaculture. 12: 943-965 (2020)

    Article  Google Scholar 

  • Lim JY, La HJ, Sheng H, Forney LJ, Hovde CJ. Influence of plasmid pO157 on Escherichia coli O157: H7 Sakai biofilm formation. Applied and Environmental Microbiology. 76: 963-966 (2010)

    Article  CAS  PubMed  Google Scholar 

  • Luck SN, Bennett-Wood V, Poon R, Robins-Browne RM, Hartland EL. Invasion of epithelial cells by locus of enterocyte effacement-negative enterohemorrhagic Escherichia coli. Infection and Immunity. 73: 3063-3071 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macia M, Rojo-Molinero E, Oliver A. Antimicrobial susceptibility testing in biofilm-growing bacteria. Clinical Microbiology and Infection. 20: 981-990 (2014)

    Article  CAS  PubMed  Google Scholar 

  • Magill DJ, Skvortsov TA. DePolymerase Predictor (DePP): a machine learning tool for the targeted identification of phage depolymerases. BMC Bioinformatics. 24: 208 (2023)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maric S. Characteristics and significance of microbial biofilm formation. Periodicum Biologorum. 109: 1-7 (2007)

    Google Scholar 

  • Marin C, Hernandiz A, Lainez M. Biofilm development capacity of Salmonella strains isolated in poultry risk factors and their resistance against disinfectants. Poultry Science. 88: 424-431 (2009)

    Article  CAS  PubMed  Google Scholar 

  • Massé J, Dufour S, Archambault M. Characterization of Klebsiella isolates obtained from clinical mastitis cases in dairy cattle. Journal of Dairy Science. 103: 3392-3400 (2020)

    Article  PubMed  Google Scholar 

  • Mcdougald D, Rice SA, Barraud N, Steinberg PD, Kjelleberg S. Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nature Reviews Microbiology. 10: 39-50 (2012)

    Article  CAS  Google Scholar 

  • Mei X, Xing D, Yang Y, Liu Q, Zhou H, Guo C, Ren N. Adaptation of microbial community of the anode biofilm in microbial fuel cells to temperature. Bioelectrochemistry. 117: 29-33 (2017)

    Article  CAS  PubMed  Google Scholar 

  • Merino L, Procura F, Trejo FM, Bueno DJ, Golowczyc MA. Biofilm formation by Salmonella sp. in the poultry industry: Detection, control and eradication strategies. Food Research International. 119: 530-540 (2019)

    Article  PubMed  Google Scholar 

  • Min D, Cheng L, Zhang F, Huang X-N, Li D-B, Liu D-F, Lau T-C, Mu Y, Yu H-Q. Enhancing extracellular electron transfer of Shewanella oneidensis MR-1 through coupling improved flavin synthesis and metal-reducing conduit for pollutant degradation. Environmental Science & Technology. 51: 5082-5089 (2017)

    Article  CAS  Google Scholar 

  • Moormeier DE, Bayles KW. Staphylococcus aureus biofilm: a complex developmental organism. Molecular Microbiology. 104: 365-376 (2017)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muhammad MH, Idris AL, Fan X, Guo Y, Yu Y, Jin X, Qiu J, Guan X, Huang T. Beyond risk: bacterial biofilms and their regulating approaches. Frontiers in Microbiology. 11: 928 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  • Ono K, Oka R, Toyofuku M, Sakaguchi A, Hamada M, Yoshida S, Nomura N. cAMP signaling affects irreversible attachment during biofilm formation by Pseudomonas aeruginosa PAO1. Microbes and Environments. 29: 104-106 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  • Oyewole OA, Raji RO, Yakubu JG. The Role of Quorum Sensing in Microbial Biofilm Formation. pp. 47-63. In: Microbial Biofilms. Maddela NR, Abiodun AS. (eds). CRC Press, Inc., Boca Raton, FL, USA (2022)

    Chapter  Google Scholar 

  • Ozkocaman V, Ozcelik T, Ali R, Ozkalemkas F, Ozkan A, Ozakin C, Akalin H, Ursavas A, Coskun F, Ener B. Bacillus spp. among hospitalized patients with haematological malignancies: clinical features, epidemics and outcomes. Journal of Hospital Infection. 64: 169–176 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Pagán R, García-Gonzalo D. Influence of environmental factors on bacterial biofilm formation in the food industry: a review. Journal of Postdoctoral Research. 3: 3-13 (2015)

    Google Scholar 

  • Park S-H, Cheon H-L, Park K-H, Chung M-S, Choi SH, Ryu S, Kang D-H. Inactivation of biofilm cells of foodborne pathogen by aerosolized sanitizers. International Journal of Food Microbiology. 154: 130-134 (2012)

    Article  CAS  PubMed  Google Scholar 

  • Patsilinakos A, Artini M, Papa R, Sabatino M, Bozovic M, Garzoli S, Vrenna G, Buzzi R, Manfredini S, Selan L, Ragno R. Machine learning analyses on data including essential oil chemical composition and in vitro experimental antibiofilm activities against Staphylococcus species. Molecules. 24: 890 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  • Pedersen RR, Krömker V, Bjarnsholt T, Dahl-Pedersen K, Buhl R, Jørgensen E. Biofilm research in bovine mastitis. Frontiers in Veterinary Science. 8: 656810 (2021)

    Article  PubMed  PubMed Central  Google Scholar 

  • Preda VG, Săndulescu O. Communication is the key: biofilms, quorum sensing, formation and prevention. Discoveries. 7: e100 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  • Quinlan JR. Induction of decision trees. Machine Learning. 1: 81-106 (1986)

    Article  Google Scholar 

  • Rajput A, Thakur A, Sharma S, Kumar M. aBiofilm: a resource of anti-biofilm agents and their potential implications in targeting antibiotic drug resistance. Nucleic Acids Research. 46: D894-D900 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Rice LB. Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE. Vol. 197, pp. 1079-1081. In: The Journal of Infectious Diseases. The University of Chicago Press. (2008)

    Article  PubMed  Google Scholar 

  • Römling U, Galperin MY, Gomelsky M. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiology and Molecular Biology Reviews. 77: 1-52 (2013)

    Article  PubMed  PubMed Central  Google Scholar 

  • Rothrock Jr MJ, Davis ML, Locatelli A, Bodie A, Mcintosh TG, Donaldson JR, Ricke SC. Listeria occurrence in poultry flocks: detection and potential implications. Frontiers in Veterinary Science. 4: 125 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  • Rudenko P, Sachivkina N, Vatnikov Y, Shabunin S, Engashev S, Kontsevaya S, Karamyan A, Bokov D, Kuznetsova O, Vasilieva E. Role of microorganisms isolated from cows with mastitis in Moscow region in biofilm formation. Veterinary World. 14: 40 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruegg PL. A 100-Year Review: Mastitis detection, management, and prevention. Journal of Dairy Science. 100: 10381-10397 (2017)

    Article  CAS  PubMed  Google Scholar 

  • Rumbaugh KP, Sauer K. Biofilm dispersion. Nature Reviews Microbiology. 18: 571-586 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santajit S, Indrawattana N. Mechanisms of antimicrobial resistance in ESKAPE pathogens. BioMed Research International. 2016: 2475067 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  • Sauer K, Stoodley P, Goeres DM, Hall-Stoodley L, Burmølle M, Stewart PS, Bjarnsholt T. The biofilm life cycle: expanding the conceptual model of biofilm formation. Nature Reviews Microbiology. 20: 608-620 (2022)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savage VJ, Chopra I, O'neill AJ. Staphylococcus aureus biofilms promote horizontal transfer of antibiotic resistance. Antimicrobial Agents and Chemotherapy. 57: 1968-1970 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scholkopf B, Smola AJ, Williamson RC, Bartlett PL. New support vector algorithms. Neural Computation. 12: 1207-1245 (2000)

    Article  CAS  PubMed  Google Scholar 

  • Schönborn S, Krömker V. Detection of the biofilm component polysaccharide intercellular adhesin in Staphylococcus aureus infected cow udders. Veterinary Microbiology. 196: 126-128 (2016)

    Article  PubMed  Google Scholar 

  • Sela S, Hammer-Muntz O, Krifucks O, Pinto R, Weisblit L, Leitner G. Phenotypic and genotypic characterization of Pseudomonas aeruginosa strains isolated from mastitis outbreaks in dairy herds. Journal of Dairy Research. 74: 425-429 (2007)

    Article  CAS  PubMed  Google Scholar 

  • Seneviratne C, Jin L, Samaranayake L. Biofilm lifestyle of Candida: a mini review. Oral Diseases. 14: 582-590 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Sharma A, Gupta P, Kumar R, Bhardwaj A. dPABBs: A Novel in silico Approach for Predicting and Designing Anti-biofilm Peptides. Scientific Reports. 6: 21839 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheffield C, Crippen T, Andrews K, Bongaerts R, Nisbet D. Planktonic and biofilm communities from 7-day-old chicken cecal microflora cultures: characterization and resistance to Salmonella colonization. Journal of Food Protection. 72: 1812-1820 (2009)

    Article  CAS  PubMed  Google Scholar 

  • Sheng H, Xue Y, Zhao W, Hovde CJ, Minnich SA. Escherichia coli O157: H7 curli fimbriae promotes biofilm formation, epithelial cell invasion, and persistence in cattle. Microorganisms. 8: 580 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi H, Shi Q, Grodner B, Lenz JS, Zipfel WR, Brito IL, De Vlaminck I. Highly multiplexed spatial mapping of microbial communities. Nature. 588: 676-681 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh R, Paul D, Jain RK. Biofilms: implications in bioremediation. Trends in Microbiology. 14: 389-397 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Sonawane JM, Rai AK, Sharma M, Tripathi M, Prasad R. Microbial biofilms: Recent advances and progress in environmental bioremediation. Science of The Total Environment. 824: 153843 (2022)

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Srivastava GN, Malwe AS, Sharma AK, Shastri V, Hibare K, Sharma VK. Molib: A machine learning based classification tool for the prediction of biofilm inhibitory molecules. Genomics. 112: 2823-2832 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Srivastava S, Bhargava A. Biofilms and human health. Biotechnology letters. 38: 1-22 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Su Y, Yrastorza JT, Matis M, Cusick J, Zhao S, Wang G, Xie J. Biofilms: formation, research models, potential targets, and methods for prevention and treatment. Advanced Science. 9: 2203291 (2022)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Subramanian D, Natarajan J. Integrated meta-analysis and machine learning approach identifies acyl-CoA thioesterase with other novel genes responsible for biofilm development in Staphylococcus aureus. Infection, Genetics and Evolution. 88: 104702 (2021)

    Article  CAS  Google Scholar 

  • Terlizzi ME, Gribaudo G, Maffei ME. UroPathogenic Escherichia coli (UPEC) infections: virulence factors, bladder responses, antibiotic, and non-antibiotic antimicrobial strategies. Frontiers in Microbiology. 8: 1566 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  • Toyofuku M, Inaba T, Kiyokawa T, Obana N, Yawata Y, Nomura N. Environmental factors that shape biofilm formation. Bioscience, Biotechnology and Biochemistry. 80: 7-12 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Upadhyayula VK, Gadhamshetty V. Appreciating the role of carbon nanotube composites in preventing biofouling and promoting biofilms on material surfaces in environmental engineering: a review. Biotechnology Advances. 28: 802-816 (2010)

    Article  CAS  PubMed  Google Scholar 

  • Valm AM, Mark Welch JL, Rieken CW, Hasegawa Y, Sogin ML, Oldenbourg R, Dewhirst FE, Borisy GG. Systems-level analysis of microbial community organization through combinatorial labeling and spectral imaging. Proceeding of the National Academy Sciences of the United States of America. 108: 4152-4157 (2011)

    Article  CAS  Google Scholar 

  • Van Houdt R, Michiels C. 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 

  • Vergara A, Normanno G, Di Ciccio P, Pedonese F, Nuvoloni R, Parisi A, Santagada G, Colagiorgi A, Zanardi E, Ghidini S. Biofilm formation and its relationship with the molecular characteristics of food‐related methicillin‐resistant Staphylococcus aureus (MRSA). Journal of Food Science. 82: 2364-2370 (2017)

    Article  CAS  PubMed  Google Scholar 

  • Vestby LK, Grønseth T, Simm R, Nesse LL. Bacterial biofilm and its role in the pathogenesis of disease. Antibiotics. 9: 59 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vu B, Chen M, Crawford RJ, Ivanova EP. Bacterial extracellular polysaccharides involved in biofilm formation. Molecules. 14: 2535-2554 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walters Iii MC, Roe F, Bugnicourt A, Franklin MJ, Stewart PS. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrobial Agents and Chemotherapy. 47: 317-323 (2003)

    Article  Google Scholar 

  • Wang J, Jiang Z, Wei Y, Wang W, Wang F, Yang Y, Song H, Yuan Q. Multiplexed identification of bacterial biofilm infections based on machine-learning-aided lanthanide encoding. ACS Nano. 16: 3300-3310 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Wang T, Shen P, He Y, Zhang Y, Liu J. Spatial transcriptome uncovers rich coordination of metabolism in E. coli K12 biofilm. Nature Chemical Biology. (2023)

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson M. Bacterial biofilms and human disease. Science Progress. 84: 235-254 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winter P, Schilcher F, Bago Z, Schoder D, Egerbacher M, Baumgartner W, Wagner M. Clinical and histopathological aspects of naturally occurring mastitis caused by Listeria monocytogenes in cattle and ewes. Journal of Veterinary Medicine, Series B. 51: 176-179 (2004)

    Article  CAS  PubMed  Google Scholar 

  • Witten IH, Frank E, Hall MA. Data mining : practical machine learning tools and techniques. 3rd ed. Morgan Kaufmann, Burlington, MA, USA (2011)

    Google Scholar 

  • Yang Y, Ding Y, Hu Y, Cao B, Rice SA, Kjelleberg S, Song H. Enhancing bidirectional electron transfer of Shewanella oneidensis by a synthetic flavin pathway. ACS Synthetic Biology. 4: 815-823 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Yaqoob SB. Role of microbial community in microbial fuel cells. pp. 139-166. In: Microbial Fuel Cells for Environmental Remediation. Ahmad A, Mohamad Ibrahim MN, Yaqoob AA, Mohd Setapar SH. (eds) Springer Nature, Singapore (2022)

    Google Scholar 

  • Zhao X, Zhao F, Wang J, Zhong N. Biofilm formation and control strategies of foodborne pathogens: food safety perspectives. RSC Advances. 7: 36670-36683 (2017)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This material is based upon the work that is supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture, under award numbers 2019-67021-29858 to K.C.J.

Funding

National Institute of Food and Agriculture, 2019-67021-29858, Kwangcheol Casey Jeong

Author information

Authors and Affiliations

  1. Emerging Pathogens Institute, University of Florida, 2055 Mowry Rd, Gainesville, FL, 32610, USA

    Ting Liu, Yuting Zhai & Kwangcheol Casey Jeong

  2. Department of Animal Sciences, University of Florida, 2250 Shealy Dr, Gainesville, FL, 32608, USA

    Ting Liu, Yuting Zhai & Kwangcheol Casey Jeong

Authors
  1. Ting Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuting Zhai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kwangcheol Casey Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kwangcheol Casey Jeong.

Ethics declarations

Conflict of interest

The authors declare no conflicts 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

Liu, T., Zhai, Y. & Jeong, K.C. Advancing understanding of microbial biofilms through machine learning-powered studies. Food Sci Biotechnol 32, 1653–1664 (2023). https://doi.org/10.1007/s10068-023-01415-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10068-023-01415-w

Keywords

Search

Navigation