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Volume 170, Issue 1

Time-lapse mesoscopy of and dual-species biofilms reveals a structural role for the hyphae of in biofilm formation Open Access

Abstract

Polymicrobial infection with and may result in a concomitant increase in virulence and resistance to antimicrobial drugs. This enhanced pathogenicity phenotype is mediated by numerous factors, including metabolic processes and direct interaction of with hyphae. The overall structure of biofilms is known to contribute to their recalcitrance to treatment, although the dynamics of direct interaction between species and how it contributes to pathogenicity is poorly understood. To address this, a novel time-lapse mesoscopic optical imaging method was developed to enable the formation of / whole dual-species biofilms to be followed. It was found that yeast-form or hyphal-form in the biofilm founder population profoundly affects the structure of the biofilm as it matures. Different sub-populations of and arise within each biofilm as a result of the different morphotypes, resulting in distinct sub-regions. These data reveal that cell morphology is pivotal in the development of global biofilm architecture and the emergence of colony macrostructures and may temporally influence synergy in infection.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): biofilm , Candida albicans , co-infection and Staphylococcus aureus
Funding
This study was supported by the:
  • Daphne Jackson Trust (Award n/a)
    • Principle Award Recipient: KatherineJ Baxter
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-01-23
2024-05-04
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References

  1. Penesyan A, Paulsen IT, Kjelleberg S, Gillings MR. Three faces of biofilms: a microbial lifestyle, a nascent multicellular organism, and an incubator for diversity. NPJ Biofilms Microbiomes 2021; 7:80 [View Article] [PubMed]
     [Google Scholar]
  2. Flemming HC, Wuertz S. Bacteria and archaea on Earth and their abundance in biofilms. Nat Rev Microbiol 2019; 17:247–260 [View Article] [PubMed]
     [Google Scholar]
  3. Yin W, Wang Y, Liu L, He J. Biofilms: the microbial “Protective Clothing” in extreme environments. Int J Mol Sci 2019; 20:3423 [View Article] [PubMed]
     [Google Scholar]
  4. Bamford NC, MacPhee CE, Stanley-Wall NR. Microbial Primer: an introduction to biofilms - what they are, why they form and their impact on built and natural environments. Microbiology 2023; 169:001338 [View Article] [PubMed]
     [Google Scholar]
  5. Olsen I. Biofilm-specific antibiotic tolerance and resistance. Eur J Clin Microbiol Infect Dis 2015; 34:877–886 [View Article]
     [Google Scholar]
  6. Doroshenko N, Tseng BS, Howlin RP, Deacon J, Wharton JA et al. Extracellular DNA impedes the transport of vancomycin in Staphylococcus epidermidis biofilms preexposed to subinhibitory concentrations of vancomycin. Antimicrob Agents Chemother 2014; 58:7273–7282 [View Article]
     [Google Scholar]
  7. Rather MA, Gupta K, Bardhan P, Borah M, Sarkar A et al. Microbial biofilm: a matter of grave concern for human health and food industry. J Basic Microbiol 2021; 61:380–395 [View Article] [PubMed]
     [Google Scholar]
  8. Peterson BW, He Y, Ren Y, Zerdoum A, Libera MR et al. Viscoelasticity of biofilms and their recalcitrance to mechanical and chemical challenges. FEMS Microbiol Rev 2015; 39:234–245 [View Article] [PubMed]
     [Google Scholar]
  9. Allegrucci M, Sauer K. Formation of Streptococcus pneumoniae non-phase-variable colony variants is due to increased mutation frequency present under biofilm growth conditions. J Bacteriol 2008; 190:6330–6339 [View Article] [PubMed]
     [Google Scholar]
  10. France MT, Cornea A, Kehlet-Delgado H, Forney LJ. Spatial structure facilitates the accumulation and persistence of antibiotic-resistant mutants in biofilms. Evol Appl 2019; 12:498–507 [View Article] [PubMed]
     [Google Scholar]
  11. Michaelis C, Grohmann E. Horizontal gene transfer of antibiotic resistance genes in biofilms. Antibiotics 2023; 12:328 [View Article] [PubMed]
     [Google Scholar]
  12. Haiko J, Saeedi B, Bagger G, Karpati F, Özenci V. Coexistence of Candida species and bacteria in patients with cystic fibrosis. Eur J Clin Microbiol Infect Dis 2019; 38:1071–1077 [View Article]
     [Google Scholar]
  13. Janssen AWM, Stienstra R, Jaeger M, van Gool AJ, Joosten LAB et al. Understanding the increased risk of infections in diabetes: innate and adaptive immune responses in type 1 diabetes. Metabolism 2021; 121:154795 [View Article] [PubMed]
     [Google Scholar]
  14. Budea CM, Pricop M, Bratosin F, Bogdan I, Saenger M et al. Antibacterial and antifungal management in relation to the clinical characteristics of elderly patients with infective endocarditis: a retrospective analysis. Antibiotics 2022; 11:956 [View Article] [PubMed]
     [Google Scholar]
  15. Di Domenico EG, Cavallo I, Capitanio B, Ascenzioni F, Pimpinelli F et al. Staphylococcus aureus and the cutaneous microbiota biofilms in the pathogenesis of atopic dermatitis. Microorganisms 2019; 7:301 [View Article] [PubMed]
     [Google Scholar]
  16. Kwiecinski JM, Horswill AR. Staphylococcus aureus bloodstream infections: pathogenesis and regulatory mechanisms. Curr Opin Microbiol 2020; 53:51–60 [View Article] [PubMed]
     [Google Scholar]
  17. Todd OA, Peters BM. Candida albicans and Staphylococcus aureus pathogenicity and polymicrobial interactions: lessons beyond Koch’s postulates. J Fungi 2019; 5:81 [View Article] [PubMed]
     [Google Scholar]
  18. Carolus H, Van Dyck K, Van Dijck P. Candida albicans and Staphylococcus species: a threatening twosome. Front Microbiol 2019; 10: [View Article]
     [Google Scholar]
  19. Qu Y, McGiffin D, Kure C, Ozcelik B, Fraser J et al. Biofilm formation and migration on ventricular assist device drivelines. J Thorac Cardiovasc Surg 2020; 159:491–502 [View Article] [PubMed]
     [Google Scholar]
  20. Qu Y, Peleg AY, McGiffin D. Ventricular assist device-specific infections. J Clin Med 2021; 10:453 [View Article] [PubMed]
     [Google Scholar]
  21. Fernandes A, Dias M. The microbiological profiles of infected prosthetic implants with an emphasis on the organisms which form biofilms. J Clin Diagn Res 2013; 7:219–223 [View Article] [PubMed]
     [Google Scholar]
  22. Cobo F, Rodríguez-Granger J, López EM, Jiménez G, Sampedro A et al. Candida-induced prosthetic joint infection. A literature review including 72 cases and a case report. Infect Dis 2017; 49:81–94 [View Article] [PubMed]
     [Google Scholar]
  23. Todd OA, Fidel PL Jr, Harro JM, Hilliard JJ, Tkaczyk C et al. Candida albicans augments Staphylococcus aureus virulence by engaging the Staphylococcal agr quorum sensing system. mBio 2019; 10:e00910-19 [View Article] [PubMed]
     [Google Scholar]
  24. Todd OA, Noverr MC, Peters BM. Candida albicans impacts Staphylococcus aureus alpha-toxin production via extracellular alkalinization. mSphere 2019; 4:e00780-19 [View Article] [PubMed]
     [Google Scholar]
  25. Krause J, Geginat G, Tammer I. Prostaglandin E2 from Candida albicans stimulates the growth of Staphylococcus aureus in mixed biofilms. PLoS One 2015; 10:e0135404 [View Article] [PubMed]
     [Google Scholar]
  26. Kong EF, Tsui C, Kucharíková S, Andes D, Van Dijck P et al. Commensal protection of Staphylococcus aureus against antimicrobials by Candida albicans biofilm matrix. mBio 2016; 7:e01365-16 [View Article] [PubMed]
     [Google Scholar]
  27. Peters BM, Ovchinnikova ES, Krom BP, Schlecht LM, Zhou H et al. Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p. Microbiology 2012; 158:2975–2986 [View Article] [PubMed]
     [Google Scholar]
  28. Cassat JE, Lee CY, Smeltzer MS. Investigation of biofilm formation in clinical isolates of Staphylococcus aureus. Methicillin-resistant Staphylococcus aureus (MRSA) protocols 2007; 127: [View Article] [PubMed]
     [Google Scholar]
  29. Harriott MM, Noverr MC. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother 2009; 53:3914–3922 [View Article]
     [Google Scholar]
  30. Soll DR. The role of phenotypic switching in the basic biology and pathogenesis of Candida albicans. J Oral Microbiol 2014; 6: [View Article] [PubMed]
     [Google Scholar]
  31. McConnell G, Trägårdh J, Amor R, Dempster J, Reid E et al. A novel optical microscope for imaging large embryos and tissue volumes with sub-cellular resolution throughout. Elife 2016; 5:e18659 [View Article] [PubMed]
     [Google Scholar]
  32. Rooney LM, Amos WB, Hoskisson PA, McConnell G. Intra-colony channels in E. coli function as a nutrient uptake system. ISME J 2020; 14:2461–2473 [View Article] [PubMed]
     [Google Scholar]
  33. Bottura B, Rooney LM, Hoskisson PA, McConnell G. Intra-colony channel morphology in Escherichia coli biofilms is governed by nutrient availability and substrate stiffness. Biofilm 2022; 4:100084 [View Article] [PubMed]
     [Google Scholar]
  34. Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H et al. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. The Lancet 2001; 357:1225–1240 [View Article]
     [Google Scholar]
  35. de Jong NWM, van der Horst T, van Strijp JAG, Nijland R. Fluorescent reporters for markerless genomic integration in Staphylococcus aureus. Sci Rep 2017; 7:43889 [View Article] [PubMed]
     [Google Scholar]
  36. Barelle CJ, Manson CL, MacCallum DM, Odds FC, Gow NAR et al. GFP as a quantitative reporter of gene regulation in Candida albicans. Yeast 2004; 21:333–340 [View Article] [PubMed]
     [Google Scholar]
  37. Kaito C, Sekimizu K. Colony spreading in Staphylococcus aureus. J Bacteriol 2007; 189:2553–2557 [View Article] [PubMed]
     [Google Scholar]
  38. Schniete J, Franssen A, Dempster J, Bushell TJ, Amos WB et al. Fast optical sectioning for widefield fluorescence mesoscopy with the mesolens based on HiLo microscopy. Sci Rep 2018; 8:16259 [View Article] [PubMed]
     [Google Scholar]
  39. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012; 9:676–682 [View Article] [PubMed]
     [Google Scholar]
  40. Bolte S, Cordelières FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 2006; 224:213–232 [View Article] [PubMed]
     [Google Scholar]
  41. European Committee for Antimicrobial Susceptibility Testing (EUCAST) of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID) Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by broth dilution. Clin Microbiol Infect 2003; 9:ix–xv [View Article]
     [Google Scholar]
  42. Adam B, Baillie GS, Douglas LJ. Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. J Med Microbiol 2002; 51:344–349 [View Article] [PubMed]
     [Google Scholar]
  43. Agrawal A, Sinha S, Mukherjee R, Mampallil D. Dynamics of bacterial deposition in evaporating drops. Phys Fluids 2020; 32:093308 [View Article]
     [Google Scholar]
  44. Yunker PJ, Durian DJ, Yodh AG. Coffee rings and coffee disks: physics on the edge. Phys Today 2013; 66:60–61 [View Article]
     [Google Scholar]
  45. Schlecht LM, Peters BM, Krom BP, Freiberg JA, Hänsch GM et al. Systemic Staphylococcus aureus infection mediated by Candida albicans hyphal invasion of mucosal tissue. Microbiology 2015; 161:168–181 [View Article] [PubMed]
     [Google Scholar]
  46. Peters BM, Jabra-Rizk MA, Scheper MA, Leid JG, Costerton JW et al. Microbial interactions and differential protein expression in Staphylococcus aureus -Candida albicans dual-species biofilms. FEMS Immunol Med Microbiol 2010; 59:493–503 [View Article] [PubMed]
     [Google Scholar]
  47. Kean R, Rajendran R, Haggarty J, Townsend EM, Short B et al. Candida albicans mycofilms support Staphylococcus aureus colonization and enhances miconazole resistance in dual-species interactions. Front Microbiol 2017; 8:258 [View Article] [PubMed]
     [Google Scholar]
  48. Zago CE, Silva S, Sanitá PV, Barbugli PA, Dias CMI et al. Dynamics of biofilm formation and the interaction between Candida albicans and methicillin-susceptible (MSSA) and -resistant Staphylococcus aureus (MRSA). PLoS One 2015; 10:e0123206 [View Article] [PubMed]
     [Google Scholar]
  49. Yunker PJ, Lohr MA, Still T, Borodin A, Durian DJ et al. Effects of particle shape on growth dynamics at edges of evaporating drops of colloidal suspensions. Phys Rev Lett 2013; 110:035501 [View Article] [PubMed]
     [Google Scholar]
  50. Xu X-L, Lee RTH, Fang H-M, Wang Y-M, Li R et al. Bacterial peptidoglycan triggers Candida albicans hyphal growth by directly activating the adenylyl cyclase Cyr1p. Cell Host & Microbe 2008; 4:28–39 [View Article]
     [Google Scholar]
  51. Hu Y, Niu Y, Ye X, Zhu C, Tong T et al. Staphylococcus aureus synergized with Candida albicans to increase the pathogenesis and drug resistance in cutaneous abscess and peritonitis murine models. Pathogens 2021; 10:1036 [View Article] [PubMed]
     [Google Scholar]
  52. Eichelberger KR, Paul S, Peters BM, Cassat JE. Candida-bacterial cross-kingdom interactions. Trends Microbiol 2023; 31:1287–1299 [View Article] [PubMed]
     [Google Scholar]
  53. Bouza E, Burillo A, Muñoz P, Guinea J, Marín M et al. Mixed bloodstream infections involving bacteria and Candida spp. J Antimicrob Chemother 2013; 68:1881–1888 [View Article] [PubMed]
     [Google Scholar]
  54. Eichelberger KR, Cassat JE. Metabolic adaptations during Staphylococcus aureus and Candida albicans co-infection. Front Immunol 2021; 12:797550 [View Article]
     [Google Scholar]
  55. Ovchinnikova ES, Krom BP, Busscher HJ, van der Mei HC. Evaluation of adhesion forces of Staphylococcus aureus along the length of Candida albicans hyphae. BMC Microbiol 2012; 12:1–7 [View Article] [PubMed]
     [Google Scholar]
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Time-lapse mesoscopy of Candida albicans and Staphylococcus aureus dual-species biofilms reveals a structural role for the hyphae of C. albicans in biofilm formation
Microbiology 170, 001426 (2024); https://doi.org/10.1099/mic.0.001426
/content/journal/micro/10.1099/mic.0.001426
/content/journal/micro/10.1099/mic.0.001426
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