Skip to main content
Springer Nature Link
Log in

Analysis of Black Fungal Biofilms Occurring at Domestic Water Taps (II): Potential Routes of Entry

  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

Formation of tenacious and massive black biofilms was occasionally observed at the water–air interphase of water taps and in associated habitats at several locations in Germany. Exophiala lecanii-corni was proven to be the dominant component of these biofilms. Water utility companies were interested to understand by which route fungi building these black biofilms enter their habitat at affected sites in domestic sanitary. A wide variety of fungi is known to be common in wet indoor environments, as well as in the drinking water resources. Two possible routes of entry are therefore considered as follows: (a) distribution by the drinking water system or (b) a retrograde route of colonisation. Previous compositional analysis revealed that the black constituents of biofilms primarily belong to the herpotrichiellaceous black yeast and relatives. Therefore, a systematic search for black fungi in the drinking water system was performed using Sabouraud’s glucose agar medium with chloramphenicol and erythritol–chloramphenicol agar as isolation media. Cadophora malorum was the dominant fungus in the investigated drinking water systems, and samples taken from the house connections (n = 50; 74 %, <200 cfu/L), followed by a so far undescribed Alternaria sp. (28 %; <10 cfu/L) and E. castellanii (26 %; <10 cfu/L). Of note, C. malorum was not present in any previously analysed biofilm. Since E. lecanii-corni was not found in any water sample from the distribution system tested, but represented the most abundant species in dark biofilms previously analysed, a retrograde route of contamination in case of E. lecanii-corni can be assumed.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Heinrichs G, Hübner I, Schmidt CK, de Hoog, GS, Haase G. Analysis of black fungal biofilms occurring at domestic water taps (1)—Compositional analysis using tag-encoded FLX amplicon pyrosequencing. Mycopathologia. 2013; xx:xx–xx.

  2. van der Mee-Marquet N, Bloc D, Briand L, Besnier JM, Quentin R. Non-touch fittings in hospitals: a procedure to eradicate Pseudomonas aeruginosa contamination. J Hosp Infect. 2005;60:235–9.

    Article  PubMed  Google Scholar 

  3. Lian X, de Hoog GS. Indoor wet cells harbour melanized agents of cutaneous infection. Med Mycol. 2010;48:622–8.

    Article  PubMed  CAS  Google Scholar 

  4. Hamada N, Abe N. Physiological characteristics of 13 common fungal species in bathrooms. Mycoscience. 2009;50:421–9.

    Article  Google Scholar 

  5. Hamada N. Characteristics of recent fungal contamination in bathrooms. Seikatsu Eisei. 2008;52:98–106.

    CAS  Google Scholar 

  6. Hinzelin F, Block JC. Yeasts and filamentous fungi in drinking water. Environ Technol Lett. 1985;6:101–6.

    Article  Google Scholar 

  7. West PR. Isolation rates and characterization of fungi in drinking water distribution systems. In: Proceedings of the water quality technical conference; Portland, Oregon: Am Water Works Ass; 1986. p. 457–73.

  8. Omeroed KS. Heterotrophic microorganisms in distribution systems for drinking water. Vatten. 1987;43:262–8.

    Google Scholar 

  9. Lahti K. Microbial quality of drinking water in some Finnish distribution systems. Water Sci Technol. 1993;27:151–4.

    Google Scholar 

  10. Franková E, Horecká M. Filamentous soil fungi and unidentified bacteria in drinking water from wells and water mains near Bratislava. Microbiol Res. 1995;150:311–3.

    Article  PubMed  Google Scholar 

  11. Göttlich E, van der Lubbe W, Lange B, Fieler S, Melchert I, Reifenrath M, et al. Fungal flora in groundwater-derived public drinking water. Int J Hyg Environ Heal. 2002;205:269–79.

    Article  Google Scholar 

  12. Hageskal G, Knutsen AK, Gaustad P, de Hoog GS, Skaar I. Diversity and significance of mould species in Norwegian drinking water. Appl Environ Microbiol. 2006;72:7586–93.

    Article  PubMed  CAS  Google Scholar 

  13. Paterson R, Gonçalves A, Lima N. Mycological examination and biofilm formation in drinking water. 8th international mycological congress; Cairns, Australia, August 20–25, 2006.

  14. Gonçalves A, Paterson R, Lima N. Survey and significance of filamentous fungi from tap water. Int J Hyg Environ Heal. 2006;209:257–64.

    Article  Google Scholar 

  15. Hageskal G, Gaustad P, Heier BT, Skaar I. Occurrence of moulds in drinking water. J Appl Microbiol. 2007;102:774–80.

    Article  PubMed  CAS  Google Scholar 

  16. Kanzler D, Buzina W, Paulitsch A, Haas D, Platzer S, Marth E, et al. Occurrence and hygienic relevance of fungi in drinking water. Mycoses. 2008;51:165–9.

    Article  PubMed  CAS  Google Scholar 

  17. Hageskal G, Lima N, Skaar I. The study of fungi in drinking water. Mycol Res. 2009;113:165–72.

    Article  PubMed  Google Scholar 

  18. Kinsey GC, Paterson RR, Kelley J. Methods for the determination of filamentous fungi in treated and untreated waters. J Appl Microbiol Symp Suppl. 1999;85:214S–24S.

    Article  Google Scholar 

  19. de Hoog GS, Vicente VA, Najafzadeh MJ, Harrak MJ, Badali H, Seyedmousavi S. Waterborne Exophiala species causing disease in cold-blooded animals. Persoonia. 2011;27:46–72.

    Article  PubMed  Google Scholar 

  20. de Hoog GS, Guarro J, Gené J, Figueras MJ. Atlas of clinical fungi. 3rd ed. Utrecht: Centraalbureau voor Schimmelcultures; 2011.

    Google Scholar 

  21. de Hoog GS, Haase G. Nutritional physiology and selective isolation of Exophiala dermatitidis. Ant Leeuw Int J G. 1993;64:17–26.

    Article  Google Scholar 

  22. de Hoog GS. Gerrits van den Ende AHG. Molecular diagnostics of clinical strains of filamentous Basidiomycetes. Mycoses. 1998;41:183–9.

    Article  PubMed  Google Scholar 

  23. Mascleaux F, Guého E, de Hoog GS, Christen R. Phylogenetic relationships of human-pathogenic Cladosporium (Xylohypha) species inferred from partial LS rRNA sequences. J Med Vet Mycol. 1995;33:327–38.

    Article  Google Scholar 

  24. White TJ, Burns T, Lee S, Taylor J. Amplification and sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innies AM, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols. A guide to methods and applications. San Diego, Calif.: Academic Press, Inc.; 1990. p. 315–22.

  25. Hall TA. Bio edit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid Symp Ser. 1999;41:95–8.

    CAS  Google Scholar 

  26. Heinrichs G, de Hoog GS, Haase G. Barcode identifiers as a practical tool for reliable species assignment of medically important black yeast species. J Clin Microbiol. 2012;50:3023–30.

    Article  PubMed  CAS  Google Scholar 

  27. Tan XM, Chen XM, Wang CL, Jin XH, Cui JL, Chen J, et al. Isolation and identification of endophytic fungi in roots of nine Holcoglossum plants (Orchidaceae) collected from Yunnan, Guangxi, and Hainan provinces of China. Curr Microbiol. 2012;64:140–7.

    Article  PubMed  CAS  Google Scholar 

  28. de Hoog GS, Mayser P, Haase G, Horré R, Horrevorts AM. A new species, Phialophora europaea, causing superficial infections in humans. Mycoses. 2000;43:409–16.

    Article  PubMed  Google Scholar 

  29. Doggett MS. Characterization of fungal biofilms within a municipal water distribution system. Appl Environ Microbiol. 2000;66:1249–51.

    Article  PubMed  CAS  Google Scholar 

  30. Grabińska-Łoniewska A, Koniłłowicz-Kowalska T, Wardzyńska G. Occurrence of fungi in water distribution system. Pol J Environ Stud. 2007;16:539–47.

    Google Scholar 

  31. Nagy LA, Olson BH. The occurrence of filamentous fungi in drinking water distribution systems. Can J Microbiol. 1982;28:667–71.

    Article  PubMed  CAS  Google Scholar 

  32. Yamaguchi MU, de Cássia Pontello Rampazzo R, Yamada-Ogatta SF, Nakamura CV, Ueda-Nakamura T, Prado Dias Filho B. Yeasts and filamentous fungi in bottled mineral water and tap water from municipal supplies. Braz Arch Biol Technol. 2007;50:1–9.

  33. Arvanitidou M, Kanellou K, Constantinides TC, Katsouyannopoulos V. The occurrence of fungi in hospital and community potable waters. Lett Appl Microbiol. 1999;29:81–4.

    Article  PubMed  CAS  Google Scholar 

  34. Sammon NB, Harrower KM, Fabbro LD, Reed RH. Three potential sources of microfungi in a treated municipal water supply system in sub-tropical Australia. Int J Environ Res Publ Health. 2011;8:713–32.

    Article  Google Scholar 

  35. Sammon NB, Harrower KM, Fabbro LD, Reed RH. Microfungi in drinking water: the role of the frog Litoria caerulea. Int J Environ Res Publ Health. 2010;7:3225–34.

    Article  Google Scholar 

  36. Gunkel G, Scheideler M. Wasserasseln in Trinkwasser Verteilungssystemen. GWF Wasser Abwasser. 2011;152:380–8.

    CAS  Google Scholar 

  37. Ramage G, Mowat E, Jones B, Williams C, Lopez-Ribot JL. Our current understanding of fungal biofilms. Crit Rev Microbiol. 2009;35:340–55.

    Article  PubMed  CAS  Google Scholar 

  38. Ramage G, Wickes BL, López-Ribot JL. A seed and feed model for the formation of Candida albicans biofilms under flow conditions using an improved modified Robbins device. Rev Iberoam Micol. 2008;25:37–40.

    Article  PubMed  Google Scholar 

  39. Chandra J, Mukherjee PK, Ghannoum MA. Fungal biofilms in the clinical lab setting. Curr Fungal Infect Rep. 2010;4:137–44.

    Article  Google Scholar 

  40. Douglas LJ. Candida biofilms and their role in infection. Trends Microbiol. 2003;11:30–6.

    Article  PubMed  CAS  Google Scholar 

  41. de Hoog GS, Queiroz-Telles F, Haase G, Fernandez-Zeppenfeldt G, Attili-Angelis D. Gerrits van den Ende AHG, et al. Black fungi: clinical and pathogenic approaches. Med Mycol. 2000;38:243–50.

    PubMed  Google Scholar 

  42. Imamura Y, Chandra J, Mukherjee PK, Lattif AA, Szczotka-Flynn LB, Pearlman E, et al. Fusarium and Candida albicans biofilms on soft contact lenses: model development, influence of lens type, and susceptibility to lens care solutions. Antimicrob Agents Chemother. 2008;52:171–82.

    Article  PubMed  CAS  Google Scholar 

  43. Singh R, Shivaprakash MR, Chakrabarti A. Biofilm formation by zygomycetes: quantification, structure and matrix composition. Microbiology. 2011;157:2611–8.

    Article  PubMed  CAS  Google Scholar 

  44. Haase G, Sonntag L, Melzer-Krick B, de Hoog GS. Phylogenetic inference by SSU-gene analysis of members of the Herpotrichiellaceae with special reference to human pathogenic species. Stud Mycol. 1999;43:80–97.

    Google Scholar 

  45. Woertz JR, Kinney KA, McIntosh NDP, Szaniszlo PJ. Removal of toluene in a vapor-phase bioreactor containing a strain of the dimorphic black yeast Exophiala lecanii-corni. Biotechnol Bioeng. 2001;75:550–8.

    Article  PubMed  CAS  Google Scholar 

  46. Hamada N, Nakamura M. Growth of fungi on various surfactants inside washing machines. Seikatsu Eisei. 2005;49:365–71.

    CAS  Google Scholar 

  47. Pirnie-Fisker EF, Woertz JR. Degradation of ethanol plant by-products by Exophiala lecanii-corni and Saccharomyces cerevisiae in batch studies. Appl Microbiol Biotechnol. 2006;74:902–10.

    Article  PubMed  Google Scholar 

  48. Short DP, O’Donnell K, Zhang N, Juba JH, Geiser DM. Widespread occurrence of diverse human pathogenic types of the fungus Fusarium detected in plumbing drains. J Clin Microbiol. 2011;49:4264–72.

    Article  PubMed  Google Scholar 

  49. Accettola F, Guebitz GM, Schoeftner R. Siloxane removal from biogas by biofiltration: biodegradation studies. Clean Technol Environ. 2008;10:211–8.

    Article  CAS  Google Scholar 

  50. Moe WM, Qi B. Performance of a fungal biofilter treating gas-phase solvent mixtures during intermittent loading. Water Res. 2004;38:2258–67.

    Article  PubMed  Google Scholar 

  51. Arriaga S, Munoz R, Hernández S, Guieysse B, Revah S. Gaseous hexane biodegradation by Fusarium solani in two liquid phase packed-bed and stirred-tank bioreactors. Environ Sci Technol. 2006;40:2390–5.

    Article  PubMed  CAS  Google Scholar 

  52. Tosi S, Casado B, Gerdol R, Caretta G. Fungi isolated from Antarctic mosses. Polar Biol. 2002;25:262–8.

    Google Scholar 

  53. Nyaoke A, Weber ES, Innis C, Stremme D, Dowd C, Hinckley L, et al. Disseminated phaeohyphomycosis in weedy seadragons (Phyllopteryx taeniolatus) and leafy seadragons (Phycodurus eques) caused by species of Exophiala, including a novel species. J Vet Diagn Invest. 2009;21:69–79.

    Article  PubMed  Google Scholar 

  54. Otis EJ, Wolke RE, Blazer VS. Infection of Exophiala salmonis in Atlantic salmon (Salmo salar L.). J Wildl Dis. 1985;21:61–4.

    PubMed  CAS  Google Scholar 

  55. Porteous NB, Grooters AM, Redding SW, Thompson EH, Rinaldi MG, de Hoog GS, et al. Identification of Exophiala mesophila isolated from treated dental unit waterlines. J Clin Microbiol. 2003;41:3885–9.

    Article  PubMed  CAS  Google Scholar 

  56. Hamada N, Abe N. Comparison of fungi found in bathrooms and sinks. Biocontrol Sci. 2010;15:51–6.

    Article  PubMed  Google Scholar 

  57. Saunte DM, Tarazooie B, Arendrup MC, de Hoog GS. Black yeast-like fungi in skin and nail: it probably matters. Mycoses. 2011;55:161–7.

    PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a research grant from RheinEnergie AG, Cologne. We also want to thank Manfred Bovi from the Institute of Pathology, RWTH Aachen University Hospital for performing the scanning electron microscopy and Kittipan Samerpitak from the CBS-KNAW Fungal Biodiversity Centre for kindly checking the DNA sequences of Ochroconis strains.

Author information

Authors and Affiliations

  1. Institute of Medical Microbiology, RWTH Aachen University Hospital, Pauwelsstraße 30, 52074, Aachen, Germany

    Guido Heinrichs & Gerhard Haase

  2. RheinEnergie AG, Parkgürtel 24, 50823, Cologne, Germany

    Iris Hübner & Carsten K. Schmidt

  3. Centraalbureau voor Schimmelcultures KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT, Utrecht, The Netherlands

    G. Sybren de Hoog

  4. The Netherlands and Institute of Biodiversity and Ecosystem Dynamics (IBED), Sciencepark 904, 1098 XH, Amsterdam, The Netherlands

    G. Sybren de Hoog

Authors
  1. Guido Heinrichs
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Iris Hübner
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Carsten K. Schmidt
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. G. Sybren de Hoog
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Gerhard Haase
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Gerhard Haase.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heinrichs, G., Hübner, I., Schmidt, C.K. et al. Analysis of Black Fungal Biofilms Occurring at Domestic Water Taps (II): Potential Routes of Entry. Mycopathologia 175, 399–412 (2013). https://doi.org/10.1007/s11046-013-9619-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-013-9619-2

Keywords