Analysis of Black Fungal Biofilms Occurring at Domestic Water Taps (I): Compositional Analysis Using Tag-Encoded FLX Amplicon Pyrosequencing

Mycopathologia

Volumn 175, Issue 5-6, 2013, Pages 387-397

  Heinrichs, Guido ^a   Hübner, Iris ^b   Schmidt, Carsten K ^b   de Hoog, G Sybren ^c,d   Haase, Gerhard ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b RHEINENERGIE AG   (Germany)

^c CBS KNAW FUNGAL BIODIVERSITY CENTRE   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Black biofilms; Exophiala lecanii corni; Fungal metagenome; Tag Encoded FLX Amplicon Pyrosequencing; Water taps

Indexed keywords

DRINKING WATER; FUNGAL DNA; RIBOSOMAL SPACER DNA;

ARTICLE; BIOFILM; BIOTA; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; FUNGUS; GENETICS; GERMANY; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; METAGENOMICS; MICROBIOLOGY; MYCOLOGY;

BIOFILMS; BIOTA; DNA, FUNGAL; DNA, RIBOSOMAL SPACER; DRINKING WATER; ENVIRONMENTAL MICROBIOLOGY; FUNGI; GERMANY; HUMANS; METAGENOMICS; MYCOLOGY; SEQUENCE ANALYSIS, DNA;

ALTERNARIA; CANDIDA ALBICANS; EXOPHIALA; EXOPHIALA DERMATITIDIS; EXOPHIALA LECANII-CORNI; FUNGI; FUSARIUM; OCHROCONIS;

EID: 84878599190     PISSN: 0301486X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11046-013-9618-3     Document Type: Article

References (54)

1. Lian X, de Hoog GS. Indoor wet cells harbour melanized agents of cutaneous infection. Med Mycol. 2010; 48: 622-8.
2. Hamada N, Abe N. Physiological characteristics of 13 common fungal species in bathrooms. Mycoscience. 2009; 50: 421-9.
3. Hamada N. Comparison of fungi found in bathrooms and sinks. Biocontrol Sci. 2010; 15: 51-6.
4. 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.
5. 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.
6. Nishimura K, Miyaji M, Taguchi H, Tanaka R. Fungi in bathwater and sludge of bathroom drainpipes 1. Frequent isolation of Exophiala species. Mycopathologia. 1987; 97: 17-23.
7. Matos T, de Hoog GS, De Boer AG, De Crom I, Haase G. High prevalence of the neurotrope Exophiala dermatitidis and related oligotrophic black yeasts in sauna facilities. Mycoses. 2002; 45: 373-7.
8. Zalar P, Novak M, de Hoog GS, Gunde-Cimerman N. Dishwashers-a man-made ecological niche accommodating human opportunistic fungal pathogens. Fungal Biol. 2011; 115: 997-1007.
9. Dowd SE, Wolcott RD, Sun Y, McKeehan T, Smith E, Rhoads D. Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS ONE. 2008; 3: e3326.
10. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, et al. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 2008; 8: 125-32.
11. Sun Y, Wolcott RD, Dowd SE. Tag-encoded FLX amplicon pyrosequencing for the elucidation of microbial and functional gene diversity in any environment. Methods Mol Biol. 2011; 733: 129-41.
12. Jünemann S, Prior K, Szczepanowski R, Harks I, Ehmke B, Goesmann A, et al. Bacterial community shift in treated periodontitis patients revealed by Ion Torrent 16S rRNA gene amplicon sequencing. PLoS ONE. 2012; 7: e41606.
13. Jumpponen A, Jones KL. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpaphyllosphere. New Phytol. 2009; 184: 438-48.
14. Buée M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, et al. 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol. 2009; 184: 449-56.
15. Lumini E, Orgiazzi A, Borriello R, Bonfante P, Bianciotto V. Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol. 2010; 12: 2165-79.
16. Öpik M, Metsis M, Daniell TJ, Zobel M, Moora M. Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytol. 2009; 184: 424-37.
17. Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, et al. 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol. 2010; 188: 291-301.
18. Wallander H, Johansson U, Sterkenburg E, Brandström Durling M, Lindahl BD. Production of ectomycorrhizal mycelium peaks during canopy closure in Norway spruce forests. New Phytol. 2010; 187: 1124-34.
19. Jumpponen A, Jones KL, Blair J. Vertical distribution of fungal communities in tallgrass prairie soil. Mycologia. 2010; 102: 1027-41.
20. Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, et al. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 2010; 4: 1340-51.
21. Amend AS, Seifert KA, Bruns TD. Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol. 2010; 19: 5555-65.
22. Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, Naqvi A, et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog. 2010; 6: e1000713.
23. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci USA. 2012; 109: 6241-6.
24. Haase G, de Hoog GS. Nutritional physiology and selective isolation of Exophiala dermatitidis. Ant Leeuw. 1993; 64: 17-26.
25. Kõljalg U, Larsson K, Abarenkov K, Nilsson R, Alexander I, Eberhardt U, et al. UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol. 2005; 166: 1063-8.
26. Abarenkov K, Nilsson RH, Larsson K-H, Alexander IJ, Eberhardt U, Erland S, et al. The UNITE database for molecular identification of fungi-recent updates and future perspectives. New Phytol. 2010; 186: 281-5.
27. 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.
28. Hageskal G, Lima N, Skaar I. The study of fungi in drinking water. Mycol Res. 2009; 113: 165-72.
29. Müller FMC, Seidler M, Beauvais A. Aspergillus fumigatus biofilms in the clinical setting. Med Mycol. 2011; 49: S96-100.
30. Rooney AP, Ward TJ. Evolution of a large ribosomal RNA multigene family in filamentous fungi: birth and death of a concerted evolution paradigm. Proc Natl Acad Sci USA. 2005; 102: 5084-9.
31. Feinstein LM, Sul WJ, Blackwood CB. Assessment of bias associated with incomplete extraction of microbial DNA from soil. Appl Environ Microbiol. 2009; 75: 5428-33.
32. DeSantis TZ, Stone CE, Murray SR, Moberg JP, Andersen GL. Rapid quantification and taxonomic classification of environmental DNA from both prokaryotic and eukaryotic origins using a microarray. FEMS Microbiol Lett. 2005; 245: 271-8.
33. Engelbrektson A, Kunin V, Wrighton KC, Zvenigorodsky N, Chen F, Ochman H, et al. Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME J. 2010; 4: 642-7.
34. Polz MF, Cavanaugh CM. Bias in template-to-product ratios in multitemplate PCR. Appl Environ Microbiol. 1998; 64: 3724-30.
35. Jumpponen A. Soil fungal communities underneath willow canopies on a primary successional glacier forefront: rDNA sequence results can be affected by primer selection and chimeric data. Microb Ecol. 2007; 53: 233-46.
36. Kunin V, Engelbrektson A, Ochman H, Hugenholtz P. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol. 2010; 12: 118-23.
37. Kangawa T. Bias and artifacts in multitemplate polymerase chain reactions (PCR). J Biosci Bioeng. 2003; 96: 317-23.
38. Gonzalez JM, Portillo MC, Belda-Ferre P, Mira A. Amplification by PCR artificially reduces the proportion of the rare biosphere in microbial communities. PLoS ONE. 2012; 7: e29973-83.
39. 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.
40. 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.
41. 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.
42. Zeng JS, Sutton DA, Fothergill AW, Rinaldi MG, Harrak MJ, de Hoog GS. Spectrum of clinically relevant Exophiala species in the United States. J Clin Microbiol. 2007; 45: 3713-20.
43. 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.
44. Richards RH, Holliman A, Helgason S. Exophiala salmonis infection in Atlantic salmon Salmo salar L. J Fish Dis. 1978; 1: 357-68.
45. Blazer VS, Wolke RE. An Exophiala-like fungus as the cause of a systemic mycosis of marine fish. J Fish Dis. 1979; 2: 145-52.
46. Otis EJ, Wolke RE, Blazer VS. Infection of Exophiala salmonis in Atlantic salmon (Salmo salar L.). J Wildl Dis. 1985; 21: 61-4.
47. 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.
48. Porteous NB, Redding SW, Thompson EH, Grooters AM, de Hoog GS, Sutton DA. Isolation of an unusual fungus in treated dental unit waterlines. J Am Dent Assoc. 2003; 134: 853-8.
49. de Hoog GS, Guarro J, Gené J, Figueras MJ. Atlas of clinical fungi. 3rd ed. Utrecht: Centraalbureau voor Schimmelcultures; 2011.
50. Ge YP, Lv GX, Shen YN, Li M, Deng SW, de Hoog S, et al. First report of subcutaneous phaeohyphomycosis caused by Ochroconis tshawytschae in an immunocompetent patient. Med Mycol. 2012; 50: 637-40.
51. Faisal M, Elsayed E, Fitzgerald SD, Silva V, Mendoza L. Outbreaks of phaeohyphomycosis in the chinook salmon (Oncorhynchus tshawytscha) caused by Phoma herbarum. Mycopathologia. 2007; 163: 41-8.
52. Armougom F, Raoult D. Exploring microbial diversity using 16S rRNA high-throughput methods. J Comput Sci Syst Biol. 2009; 2: 69-92.
53. Tan XM, Chen XM, Wang CL, Jin XH, Cui JL, Chen J, Guo SX, Zhao LF. 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.
54. Heinrichs G, Hübner I, Schmidt CK, de Hoog GS, Haase G. Analysis of black fungal biofilms occurring at domestic water taps (II): potential routes of entry. Mycopathologia. 2013. doi: 10. 1007/s11046-013-9619-2.