In vitro polymicrobial inter-kingdom three-species biofilm model: influence of hyphae on biofilm formation and bacterial physiology

References

• Archambault LS, Trzilova D, Gonia S, Gale C, Wheeler RT. 2019. Intravital imaging reveals divergent cytokine and cellular immune responses to Candida albicans and Candida parapsilosis. MBio. 10(3):1–18. doi:10.1128/mBio.00266-19
   Web of Science ®Google Scholar
• Arciola CR, Campoccia D, Montanaro L. 2018. Implant infections: adhesion, biofilm formation and immune evasion. Nat Rev Microbiol. 16:397–409. doi:10.1038/s41579-018-0019-y
   PubMed Web of Science ®Google Scholar
• Arendrup MC, Meletiadis J, Mouton JW, Lagrou K, Hamal P, Guinea J, Eucast-AFST. 2017. Method for the determination of broth dilution minimum inhibitory concentrations of antifungal agents for yeasts. Eucast Edef. 731:1–21.
   Google Scholar
• BioSurface Technologies Co. 2019. CDC Biofilm Reactor® (CBR) Operator’s Manual [accessed 2021 Feb]:[p. 1–17]. https://biofilms.biz/biosurfacetechnologies.com/wp-content/uploads/2021/03/CBR-Operators-Manual-Mar2021.pdf
   Google Scholar
• Blumer C, Kleefeld A, Lehnen D, Heintz M, Dobrindt U, Nagy G, Michaelis K, Emödy L, Polen T, Rachel R, et al. 2005. Regulation of type 1 fimbriae synthesis and biofilm formation by the transcriptional regulator LrhA of Escherichia coli. Microbiology. 151:3287–3298. doi:10.1099/mic.0.28098-0
   PubMed Web of Science ®Google Scholar
• Bronesky D, Wu Z, Marzi S, Walter P, Geissmann T, Moreau K, Vandenesch F, Caldelari I, Romby P. 2016. Staphylococcus aureus RNAIII and its regulon link quorum sensing, stress responses, metabolic adaptation, and regulation of virulence gene expression. Annu Rev Microbiol. 70:299–316. doi:10.1146/annurev-micro-102215-095708
   PubMed Web of Science ®Google Scholar
• De Brucker K, Tan Y, Vints K, De Cremer K, Braem A, Verstraeten N, Michiels J, Vleugels J, Cammue BPA, Thevissen K. 2015. Fungal β-1,3-glucan increases ofloxacin tolerance of Escherichia coli in a polymicrobial E. coli/Candida albicans biofilm. Antimicrob Agents Chemother. 59:3052–3058. doi:10.1128/AAC.04650-14
   PubMed Web of Science ®Google Scholar
• De Carvalho Dias K, Barbugli PA, De Patto F, Lordello VB, De Aquino Penteado L, Medeiros AI, Vergani CE. 2017. Soluble factors from biofilm of Candida albicans and Staphylococcus aureus promote cell death and inflammatory response. BMC Microbiol. 17:146. doi:10.1186/s12866-017-1031-5
   PubMed Web of Science ®Google Scholar
• Chupáčová J, Borghi E, Morace G, Los A, Bujdáková H. 2018. Anti-biofilm activity of antibody directed against surface antigen complement receptor 3-related protein—comparison of Candida albicans and Candida dubliniensis. Pathog Dis. 76(1):1–10.
   Web of Science ®Google Scholar
• Crabbé A, Jensen PØ, Bjarnsholt T, Coenye T. 2019. Antimicrobial tolerance and metabolic adaptations in microbial biofilms. Trends Microbiol. 27:850–863. doi:10.1016/j.tim.2019.05.003
   PubMed Web of Science ®Google Scholar
• Diaz Iglesias Y, Wilms T, Vanbever R, Van Bambeke F. 2019. Activity of antibiotics against Staphylococcus aureus in an in vitro model of biofilms in the context of cystic fibrosis: influence of the culture medium. Antimicrob Agents Chemother. 63:1–14. doi:10.1128/AAC.00602-19
   Web of Science ®Google Scholar
• Dige I, Nyvad B. 2019. Candida species in intact in vivo biofilm from carious lesions. Arch Oral Biol. 101:142–146. doi:10.1016/j.archoralbio.2019.03.017
   PubMed Web of Science ®Google Scholar
• Fisher RA, Gollan B, Helaine S. 2017. Persistent bacterial infections and persister cells. Nat Rev Microbiol. 15:453–464. doi:10.1038/nrmicro.2017.42
   PubMed Web of Science ®Google Scholar
• Förster TM, Mogavero S, Dräger A, Graf K, Polke M, Jacobsen ID, Hube B. 2016. Enemies and brothers in arms: Candida albicans and gram-positive bacteria. Cell Microbiol. 18:1709–1715. doi:10.1111/cmi.12657
   PubMed Web of Science ®Google Scholar
• Hall CW, Mah T-F. 2017. Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev. 41:276–301. doi:10.1093/femsre/fux010
   PubMed Web of Science ®Google Scholar
• Harriott MM, Noverr MC. 2010. Ability of Candida albicans mutants to induce Staphylococcus aureus vancomycin resistance during polymicrobial biofilm formation.AAC. 54:3746–3755. doi:10.1128/AAC.00573-10
   Google Scholar
• Houston P, Rowe SE, Pozzi C, Waters EM, O'Gara JP. 2011. Essential role for the major autolysin in the fibronectin-binding protein-mediated Staphylococcus aureus biofilm phenotype. Infect Immun. 79:1153–1165. doi:10.1128/IAI.00364-10
   PubMed Web of Science ®Google Scholar
• Kart D, Tavernier S, Van Acker H, Nelis HJ, Coenye T. 2014. Activity of disinfectants against multispecies biofilms formed by Staphylococcus aureus, Candida albicans and Pseudomonas aeruginosa. Biofouling. 30(3):377–383. doi:10.1080/08927014.2013.878333
   PubMed Web of Science ®Google Scholar
• Kojic EM, Darouiche RO. 2004. Candida infections of medical devices. CMR. 17:255–267. doi:10.1128/CMR.17.2.255-267.2004
   Google Scholar
• Kong EF, Tsui C, Kucharíková S, Andes D, Van Dijck P, Jabra-Rizk MA. 2016. Commensal protection of Staphylococcus aureus against antimicrobials by Candida albicans biofilm matrix. MBio. 7:e01365–16. doi:10.1128/mBio.01365-16
   PubMed Web of Science ®Google Scholar
• Kong EF, Tsui C, Kucharíková S, Van Dijck P, Jabra-Rizk MA. 2017. Modulation of Staphylococcus aureus response to antimicrobials by the Candida albicans quorum sensing molecule farnesol. Antimicrob Agents Chemother. 61:e01573–17. doi:10.1128/AAC.01573-17
   PubMed Web of Science ®Google Scholar
• Larsen MKS, Thomsen TR, Moser C, Høiby N, Nielsen PH. 2008. Use of cultivation-dependent and -independent techniques to assess contamination of central venous catheters: a pilot study. BMC Clin Pathol. 8:10. doi:10.1186/1472-6890-8-10
   PubMedGoogle Scholar
• Lazzell AL, Chaturvedi AK, Pierce CG, Prasad D, Uppuluri P, Lopez-Ribot JL. 2009. Treatment and prevention of Candida albicans biofilms with caspofungin in a novel central venous catheter murine model of candidiasis. J Antimicrob Chemother. 64:567–570. doi:10.1093/jac/dkp242
   PubMed Web of Science ®Google Scholar
• Li H, Gong H, Qi Y, Li J, Ji X, Sun J, Tian R, Bao H, Song X, Chen Q, Liu G. 2017. In vitro and in vivo antifungal activities and mechanism of heteropolytungstates against Candida species. Sci Rep. 7:16942. doi:10.1038/s41598-017-17239-8
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 25:402–408. doi:10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar
• Nistico L, Gieseke A, Stoodley P, Hall-Stoodley L, Kerschner JE, Ehrlich GD. 2009. Fluorescence “in situ” hybridization for the detection of biofilm in the middle ear and upper respiratory tract mucosa. In: Sokolowski B, editors. Methods in Molecular Biology. Hatfield (UK): Humana Press, Springer; p. 191–212.
   PubMedGoogle Scholar
• Nobile CJ, Fox EP, Nett JE, Sorrells TR, Mitrovich QM, Hernday AD, Tuch BB, Andes DR, Johnson AD. 2012. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell. 148:126–138. doi:10.1016/j.cell.2011.10.048
   PubMed Web of Science ®Google Scholar
• Nobile CJ, Johnson AD. 2015. Candida albicans biofilms and human disease. Annu Rev Microbiol. 69:71–92. doi:10.1146/annurev-micro-091014-104330
   PubMed Web of Science ®Google Scholar
• Pammi M, Liang R, Hicks J, Mistretta T-A, Versalovic J. 2013. Biofilm extracellular DNA enhances mixed species biofilms of Staphylococcus epidermidis and Candida albicans. BMC Microbiol. 13:257. doi:10.1186/1471-2180-13-257
   PubMed Web of Science ®Google Scholar
• Peters BM, Jabra-Rizk MA, Scheper MA, Leid JG, Costerton JW, Shirtliff ME. 2010. Microbial interactions and differential protein expression in Staphylococcus aureus-Candida albicans dual-species biofilms. FEMS Immunol Med Microbiol. 59:493–503. doi:10.1111/j.1574-695X.2010.00710.x
   PubMed Web of Science ®Google Scholar
• Peters BM, Noverr MC. 2013. Candida albicans-Staphylococcus aureus polymicrobial peritonitis modulates host innate immunity. Infect Immun. 81:2178–2189. doi:10.1128/IAI.00265-13
   PubMed Web of Science ®Google Scholar
• Peters BM, Ovchinnikova ES, Krom BP, Schlecht LM, Zhou H, Hoyer LL, Busscher HJ, van der Mei HC, Jabra-Rizk MA, Shirtliff ME. 2012. Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p. Microbiology. 158:2975–2986. doi:10.1099/mic.0.062109-0
   PubMed Web of Science ®Google Scholar
• Poilvache H, Ruiz-Sorribas A, Sakoulas G, Rodriguez-Villalobos H, Cornu O, Van Bambeke F. 2020. Synergistic effects of pulsed lavage and antimicrobial therapy against Staphylococcus aureus biofilms in an in-vitro Model. Front Med. 7:527.
   Web of Science ®Google Scholar
• Rimachi Hidalgo KJ, Cabrini Carmello J, Carolina Jordão C, Aboud Barbugli P, de Sousa Costa CA, Garcia de Oliveira Mima E, Pavarina AC. 2019. Antimicrobial photodynamic therapy in combination with nystatin in the treatment of experimental oral candidiasis induced by Candida albicans resistant to fluconazole. Pharmaceuticals. 12:140. doi:10.3390/ph12030140
   Web of Science ®Google Scholar
• Røder HL, Sørensen SJ, Burmølle M. 2016. Studying bacterial multispecies biofilms: where to start? Trends Microbiol. 24:503–513. doi:10.1016/j.tim.2016.02.019
   PubMed Web of Science ®Google Scholar
• Rogiers O, Holtappels M, Siala W, Lamkanfi M, Van Bambeke F, Lagrou K, Van Dijck P, Kucharíková S. 2018. Anidulafungin increases the antibacterial activity of tigecycline in polymicrobial Candida albicans/Staphylococcus aureus biofilms on intraperitoneally implanted foreign bodies. J Antimicrob Chemother. 73:2806–2814. doi:10.1093/jac/dky246
   PubMed Web of Science ®Google Scholar
• Schlecht LM, Peters BM, Krom BP, Freiberg JA, Hänsch GM, Filler SG, Jabra-Rizk MA, Shirtliff ME. 2015. Systemic Staphylococcus aureus infection mediated by Candida albicans hyphal invasion of mucosal tissue. Microbiology. 161:168–181. doi:10.1099/mic.0.083485-0
   PubMed Web of Science ®Google Scholar
• Schwartz K, Ganesan M, Payne DE, Solomon MJ, Boles BR. 2016. Extracellular DNA facilitates the formation of functional amyloids in Staphylococcus aureus biofilms. Mol Microbiol. 99:123–134. doi:10.1111/mmi.13219
   PubMed Web of Science ®Google Scholar
• Tan L, Li SR, Jiang B, Hu XM, Li S. 2018. Therapeutic targeting of the Staphylococcus aureus accessory gene regulator (agr) system. Front Microbiol. 9:55.
   Google Scholar
• Todd OA, Fidel PL, Harro JM, Hilliard JJ, Tkaczyk C, Sellman BR, Noverr MC, Peters BM. 2019. Candida albicans augments Staphylococcus aureus virulence by engaging the staphylococcal agr quorum sensing system. MBio. 10(3):1–16. doi:10.1128/mBio.00910-19
   Web of Science ®Google Scholar
• Xu Y, Rudkjøbing VB, Simonsen O, Pedersen C, Lorenzen J, Schønheyder HC, Nielsen PH, Thomsen TR. 2012. Bacterial diversity in suspected prosthetic joint infections: an exploratory study using 16S rRNA gene analysis. FEMS Immunol Med Microbiol. 65:291–304. doi:10.1111/j.1574-695X.2012.00949.x
   PubMedGoogle Scholar
• Xue T, You Y, Shang F, Sun B. 2012. Rot and Agr system modulate fibrinogen-binding ability mainly by regulating clfB expression in Staphylococcus aureus NCTC8325. Med Microbiol Immunol. 201:81–92. doi:10.1007/s00430-011-0208-z
   PubMed Web of Science ®Google Scholar
• Yang M, Du K, Hou Y, Xie S, Dong Y, Li D, Du Y. 2019. Synergistic antifungal effect of amphotericin B-loaded poly(lactic-co-glycolic acid) nanoparticles and ultrasound against Candida albicans biofilms. Antimicrob Agents Chemother. 63: 1–13.
   Web of Science ®Google Scholar
• Zago CE, Silva S, Sanitá PV ,Barbugli PA, Dias CMI, Lordello VB, Vergani CE. 2015. Dynamics of biofilm formation and the interaction between Candida albicans and methicillin-susceptible (MSSA) and -resistant Staphylococcus aureus (MRSA). PLoS One. 10:e0123206.
   Google Scholar
• Zheng Y, Joo H-S, Nair V, Le KY, Otto M. 2018. Do amyloid structures formed by Staphylococcus aureus phenol-soluble modulins have a biological function? Int J Med Microbiol. 308:675–682. doi:10.1016/j.ijmm.2017.08.010
   PubMed Web of Science ®Google Scholar
• Zmantar T, Chaieb K, Makni H, Miladi H, Abdallah F Ben, Mahdouani K, Bakhrouf A. 2008. Detection by PCR of adhesins genes and slime production in clinical Staphylococcus aureus. J Basic Microbiol. 48:308–314. doi:10.1002/jobm.200700289
   PubMed Web of Science ®Google Scholar