Abstract
Despite feather fungi being an important component of the Arctic fungal flora, their ecological role and diversity are not fully known. In the current study, fungal cultures were isolated from feathers (barnacle goose, common eider, and glaucous gull) collected in the Ny-Ålesund region, Svalbard. Isolates were identified by ITS region sequences, which include the ITS1, ITS2, and 5.8S rRNA. The result showed culturable yeast and filamentous fungi belonging to three classes: Ascomycota (Pyrenochaetopsis pratorum, Cladosporium herbarum, Thelebolus microsporus, Aspergillus versicolor, Penicillium commune, and Venturia sp.), Basidiomycota (Mrakia blollopis and Rhodotorula mucilaginosa), and Zygomycota (Mucor flavus). Most of the fungal isolates appeared to be cold-tolerant, and about 60 % of the isolates showed keratinase activity. The reasonably low fungal diversity colonizing feathers indicates that the birds of Svalbard are casual carriers of fungi which may result in a negligible impact on their health. To the best of our knowledge, this is the first record of fungal communities present on the feathers of birds in the high Arctic.
Similar content being viewed by others
References
Aarnæs J-O (2002) Katalog over makro- og mikrosopp angitt for Norge og Svalbard [Catalogue of macro-and micromycetes recorded for Norway and Svalbard]. In Norwegian with an English summary. Synopsis Fungorum 16. Fungiflora A/S. Oslo, Norway
Barnett JA, Payne RW, Yarrow D (2000) Yeasts: characteristics and identification, 3rd edn. Cambridge University Press, Cambridge
Barron GL (1977) The genera of Hyphomycetes from soil. Robert E. Krieger Publishing Huntington, New York
Bergero R, Girlanda M, Varese GC, Intili D, Luppi AM (1999) Psychrooligotrophic fungi from Arctic soils of Franz Joseph Land. Polar Biol 21:361–368
Böckle B, Galunsky B, Müller R (1995) Characterization of a keratinolytic serine proteinase from Streptomyces pactum DMS-40530. Appl Environ Microbiol 61:3705–3710
Böhme H, Ziegler H (1969) The distribution of geophilic dermatophytes and other keratinophilic fungi in relation to the ph of the soil. Mycopathol Mycol Appl 38:247–255
Buck JD (1983) Occurrence of Candida albicans in fresh gull feces in temperate and subtropical areas. Microb Ecol 9:171–176
Buck AM, Chabasse D (1998) Isolation of Candida albicans and halophilic Vibrio spp. from aquatic birds in Connecticut and Florida. Appl Environ Microb 56:826–828
Butinar L, Spencer-Martins I, Gunde-Cimerman N (2007) Yeasts in high Arctic glaciers: the discovery of a new habitat for eukaryotic microorganisms. A Van Leeuw J Microb 91:277–289
Butinar L, Strmole T, Gunde-Cimerman N (2011) Relative incidence of ascomycetous yeasts in arctic coastal environments. Microb Ecol 61:832–843
Buzzini P, Branda E, Goretti M, Turchetti B (2012) Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential. FEMS Microbiol Ecol 82:217–241
Cafarchia C, Camarda A, Romito D, Campolo M, Quaglia NC, Tullio D, Otronto D (2006) Occurrence of yeasts in cloacae of migratory birds. Mycopathol 161:229–234
Callaghan TV, Björn LO, Chernov Y, Chapin T, Christensen TR, Huntley B, Ims RA et al (2004) Biodiversity, distributions and adaptations of Arctic species in the context of environmental change. Ambio 33:404–417
Carmichael JW, BryceKendrick W, Conners IL, Sigler L (1980) Genera of hyphomycetes. The University of Alberta Press, Canada
Connell L, Redman R, Craig S, Scorzetti G, Iszard M, Rodriguez R (2008) Diversity of soil yeasts isolated from South Victoria Land, Antarctica. Microb Ecol 56:448–459
Cooke RC, Whipps JM (1993) Ecophysiology of fungi. Blackwell Scientific Publications, Edinburgh
Czeczuga B, Godlewska A, Kiziewicz B (2004) Aquatic fungi growing on feathers of wild and domestic bird species in limnologically different water bodies. Pol J Environ Stud 131:21–31
de Gruyter J, Woudenberg JHC, Aveskamp MM, Verkley GJM, Groenewald JZ, Crous PW (2010) Systematic reappraisal of species in Phoma section Paraphoma, Pyrenochaeta and Pleurophoma. Mycologia 102:1066–1081
De Hoog GS, Gottlich E, Platas G, Genilloud O, Leotta G, van Brummelen J (2005) Evolution, taxonomy and ecology of the genus Thelebolus in Antarctica. Stud Mycol 51:33–76
De Vries GA (1962) Keratinophilic fungi and their action. A Van Leeuw J Microb 28:121–133
Del Frate G, Caretta G (1990) Fungi isolated from Antarctic material. Polar Biol 11:1–7
Dominik T, Inhatowicz A, Kopylow H, Mietkiewsky R (1973) Mycoflore of sand boxes in kindergardens in Szczecin. Ekol Pol 21:901–923
Domsch KH, Gams W, Anderson T-H (1980) Compendium of soil fungi. Academic Press, London
Dupont C, Carrier M, Higgins R (1994) Bacterial and fungal flora in healthy eyes of birds of prey. Can Vet J 35:699–701
Dynowska M, Kisicka I (2005a) Fungi isolated from selected birds potentially pathogenic to humans. Acta Mycol 40:141–147
Dynowska M, Kisicka I (2005b) Participation of birds in the circulation of pathogenic fungi descend from water environments: a case study of two species of Charadriiformes birds. Ecohydrol Hydrobiol 5:173–178
Dynowska M, Wojczulanis-Jakubas K, Pacynśka JA, Jakubas D, Ejdys E (2013) Potentially pathogenic yeast isolated from the throat and cloaca of an Arctic colonial seabird: the little auk (Alle alle). Polar Biol 36:343–348
Ellis MB (1971) Dematiaceous hyphomycetes. CMI, Kew
Ellis MB (1976) More dematiaceous hyphomycetes. CMI, Kew
Elvebakk A, Gjaerum HB, Sivertsen S (1996) Myxomycota, Oomycota, Chytridiomycota, Zygomycota, Ascomycota, Deuteromycota, Basidiomycota: Uredinales and Ustilaginales. In: Elvebakk A, Prestrud P (eds) A catalogue of Svalbard plants, fungi, algae and cyanobacteria. Part 4. Fungi II. Oslo, pp 207–259
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Filipello Marchisio V (1986) Keratinolytic and keratinophilic fungi of children’s sandpits in the city of Turin. Mycopathologia 94:163–172
Filipello Marchisio V (2000) Keratinophilic fungi: their role in nature and degradation of keratinic substrates. Revista Iberoamericana de Micología Apdo. 699, E-48080 Bilbao (Spain), pp 86–92
Filipello Marchisio V, Curetti V, Cassinelli C, Bordese C (1991) Keratinolytic and keratinophilic fungi in the soil of Papua New Guinea. Mycopathologia 115:113–120
Filipello Marchisio V, Fusconi A, Rigo S (1994) Keratinolysis and its morphological expression in hair digestion by airborne fungi. Mycopathologia 127:103–115
Friedrich J, Gradisar H, Mandin D, Chaumont JP (1999) Screening of fungi for synthesis of keratinolytic enzymes. Lett Appl Microbiol 28:127–130
Ghannuaum AM, Abu-Elteen KH (1990) Pathogenicity determinants of candida. Mycoses 33:265–282
Griffin DM (1960) Fungal colonization of sterile hair in contact with soil. Trans Br Mycol Soc 43:583–596
Gungnani HC, Sharma S, Gupta B (2012) Keratinophilic fungi recovered from feathers of different species of birds in St Kitts and Nevis. West Indian Med J 61:912–915
Hawksworth DL (1991) The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol Res 95:641–655
Holding AJ (1981) The microflora of tundra. In: Bliss LC, Heal OW, Moore JJ (eds) Tundra ecosystems: a comparative analysis. Cambridge University Press, Cambridge, pp 561–585
Hoog GS (1996) Risk assessment of fungi reported from humans and animals. Mycoses 39:407–417
Hoshino T, Tojo M, Okada G, Kanda H, Ohgiya S, Ishizaki K (1999) A filamentous fungus, Pythium ultimum Throw var. ultimum, isolated from moribund moss colonies from Svalbard, northern island of Norway. Polar Biosci 12:68–75
IPCC (2007) Climate change 2007: the physical science basis. Summary for policy makers. In: Contribution of working group I to the fourth assessment report of the inter-governmental panel on climate change. Cambridge University Press, Cambridge
Ivarson KC (1965) The microbiology of some permafrost soils in the McKenzie Valley. NWT Arctic 18:256–260
Karsten PF (1872) Fungi in insulis Spetsbergen et Beeren Eiland collecti. Öfvers. Kungliga Vetensk -Akad Förh 2:91–108
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Ainsworth and Bisby’s dictionary of the fungi, 10th edn. CABI Publishing, UK
Kunert J (1972) Keratin decomposition by dermatophytes: evidence of the sulphitolysis of the protein. Sabouraudia 10:1025–1026
Kurek E, Korniłowicz-Kowalska T, Słomka A, Melke J (2007) Characteristics of soil filamentous fungi communities isolated from various micro relief forms in the high Arctic tundra (Bellsund region, Spitsbergen). Polish Polar Res 28:57–73
Kurtzman CP, Fell JW, Boekhout T (2011) The yeasts, a taxonomic study, 5th edn. Elsevier, Tokyo
Kutty SN, Philip R (2008) Marine yeasts: a review. Yeast 25:465–483
Kytöviita MM (2005) Asymmetric symbiont adaptation to Arctic conditions could explain why high Arctic plants are non-mycorrhizal. FEMS Microbiol Ecol 53:27–32
Lehninger AL (1984) Biochimica. Bologna, Zanichelli
Majchrowicz I, Dominik T (1969) Further contribution to the knowledge of keratinolytic and keratinophilic soil fungi of the region of Szczecin—Keratinolytic and keratinophilic fungi in the immediate surroundings of cattle. Ekol Pol 17:87–116
Malviya HK, Rajak RC, Hasija SK (1992) Purification and partial characterization of extracellular keratinases of Scopulariopsis brevicaulis. Mycopathologia 119:161–165
Mancianti F, Nardoni S, Ceccherelli R (2002) Occurrence of yeasts in psittacines droppings from captive birds in Italy. Mycopathol 153:121–124
Mandeel Q, Nardoni S, Mancianti F (2011) Keratinophilic fungi on feathers of common clinically healthy birds in Bahrain. Mycoses 54:71–77
McAleer R (1980) Investigation of keratinophilic fungi from soil in Western-Australia: a preliminary survey. Mycopathologia 72:155–166
Miljković B, Pavlovski Z, Jovičić D, Radanović O, Kureljušić B (2011) Fungi on feathers of common clinically healthy birds in Belgrade. Biotech Anim Husbandry 27:45–54
Nygaard EJ (2009) Ny-Ålesund, International Arctic Research and Monitoring Station at 79°N. Kings Bay AS, Ny-Ålesund
Ogbonna CIC, Pugh GJF (1987) Keratinophilic fungi from Nigerian soil. Mycopathologia 99:115–118
Ozerskaya S, Kochkina G, Ivanushkina N, Gilichinsky DA (2009) Fungi in permafrost. In: Margesin R (ed) Permafrost soils. Soil Biology 16. Springer, Berlin, pp 85–95
Pang KL, Chiang MW, Vrijmoed LLP (2008) Havispora longyearbyenensis gen. et sp. nov.: an arctic marine fungus from Svalbard, Norway. Mycologia 100:291–295
Pang KL, Chiang MW, Vrijmoed LLP (2009) Remispora spitsbergenensis sp. nov., a marine lignicolous ascomycete from Svalbard, Norway. Mycologia 101:531–534
Pathan AAK, Bhadra B, Begum Z, Shivaji S (2009) Diversity of yeasts from puddles in the vicinity of Midre Lovénbreen glacier, Arctic and bioprospecting for enzymes and fatty acids. Curr Microbiol 60:307–314
Peay KG, Kennedy PG, Bruns TD (2008) Fungal community ecology: a hybrid beast with a molecular master. Bioscience 58:799–810
Piontelli E, Caretta G (1974) Considerazioni ecologiche su alcuni geomiceti isolati su substrati cheratinici in località montagnose delle Ande del Cile. Rivista Patol Veg 10:261–314
Pitt JI (1979) The genus Penicillium and its teleomorphic states Eupenicillium and Talaromyces. Academic Press, London
Pugh GJF, Evans MD (1970) Keratinophilic fungi associated with birds. II. Physiological studies. Trans Br Mycoi Soc 54:241–250
Rapper KB, Fennell DI (1965) The Aspergillus. The Williams & Wilkins Company, Baltimore
Reeve JN, Christner BC, Kvitko BH, Mosley-Thompson E, Thompson LG (2002) Life in glacial ice (Abstract). In: Rossi M, Bartolucci S, Ciaramella M, Moracci M (eds) Extremophiles 2002. 4th international congress on extremophiles, September 2002, Naples, Italy 27, pp 22–26
Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Samson RA, Frisvad JC (2004) Penicillium Subgenus Penicillium: new taxonomic schemes, mycotoxins and other extrolites. Stud Mycol 49:1–251
Säwström C, Mumford P, Marshall W, Hodson A, Laybourn-Parry J (2002) The microbial communities and primary productivity of cryoconite holes in an Arctic glacier (Svalbard 79°N). Polar Biol 25:591–596
Schneider R (1979) Die Gattung Pyrenochaeta De Notaris. Mitt Biol Bundesanst Land Forstw 189:1–73
Singh P, Singh SM (2012) Characterization of yeast and filamentous fungi isolated from cryoconite holes of Svalbard, Arctic. Polar Biol 35:575–583
Singh SM, Singh PN, Singh SK, Sharma PK (2014) Pigment, fatty acid and extracellular enzyme analysis of a fungal strain Thelebolus microsporus from Larsemann Hills, Antarctica. Polar Rec 50:31–36
Singh SM, Singh SK, Yadav L, Singh PN, Ravindra R (2012) Filamentous soil fungi from Ny-Ålesund, Spitsbergen, and screening for extracellular enzymes. Arctic 65:35–55
Singh P, Tsuji M, Singh SM, Roy U, Hoshino T (2013) Taxonomic characterization, adaptation strategies and biotechnological potential of cryophilic yeasts from ice cores of Midre Lovénbreen glacier, Svalbard, Arctic. Cryobiology 66:167–175
Sjolund M, Bonnedahl J, Hernandez J, Bengtsson S, Cederbrant G, Pinhassi J, Kahlmeter G, Olsen B (2008) Dissemination of multidrug-resistant bacteria into the Arctic. Emerg Infect Dis 14:70–72
Takiuchi I, Sei I, Takagi H, Negi M (1984) Partial characterization of the extracellular keratinase from Microsporum canis. J Med Vet Mycol 22:219–224
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. doi:10.1093/molbev/msr121
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. doi:10.1093/molbev/mst197
Thomas-Hall SR, Turchetti B, Buzzini P, Branda E, Boekhout T, Theelen B, Watson K (2010) Cold-adapted yeasts from Antarctica and the Italian Alps-description of three novel species: Mrakia robertii sp. nov., Mrakia blollopis sp. nov. and Mrakiella niccombsii sp. nov. Extremophiles 14:47–59
Tsiodras S, Kelesidis T, Kelesidis I, Bauchinger V, Falagas ME (2008) Human infections associated with wild birds. J Infect 56:83–98
Tsuji M, Fujiu S, Xiao N, Hanada Y, Kudoh S, Kondo H, Tsuda S, Hoshino T (2013a) Cold adaptation of fungi obtained from soil and lake sediment in the Skarvsnes ice-free area, Antarctica. FEMS Microbiol Lett 346:121–130
Tsuji M, Goshima T, Matsushika A, Kudoh S, Hoshino T (2013b) Direct ethanol fermentation from lignocellulosic biomass by Antarctic basidiomycetous yeast Mrakia blollopis under a low temperature condition. Cryobiology 67:241–243
Ulfig K, Ulfig A (1990) Keratinophilic fungi in bottom sediments of surface waters. J Med Vet Mycol 28:261–268
Wawrzkiewicz K, Wolski T, Lobarzewski J (1991) Screening the keratinolytic activity of dermatophytes in vitro. Mycopathologia 114:1–8
Wojczulanis-Jakubas K, Dynowska M, Jakubas D (2011) Fungi prevalence in breeding pairs of monogamous seabird: little auk, Alle alle. Ethol Ecol Evol 23:240–247
Yu RJ, Harmon SR, Blank F (1969) Hair digestion by a keratinase of Trichophyton mentagrophytes. J Invest Dermatol 5:166–171
Acknowledgments
Authors are thankful to Directors NCAOR—India, NIPR—Japan, AIST—Japan, Arctic Centre, University of Groningen and King Bay—Norway for facilities. Authors are also thankful to Mr. Gary Stanley Fernandes and Dr. Dominique Paré, Consorminex Inc. (Canada), for English corrections. The publication compliance with Ethical Standards of journal of Polar Biology. This is NCAOR Publication no. 31/2015.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Singh, S.M., Tsuji, M., Gawas-Sakhalker, P. et al. Bird feather fungi from Svalbard Arctic. Polar Biol 39, 523–532 (2016). https://doi.org/10.1007/s00300-015-1804-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-015-1804-y