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Fungal Diversity

, Volume 52, Issue 1, pp 123–139 | Cite as

A novel ascosporogenous yeast species, Zygosaccharomyces siamensis, and the sugar tolerant yeasts associated with raw honey collected in Thailand

  • Sujinan Saksinchai
  • Motofumi Suzuki
  • Panuwan Chantawannakul
  • Moriya Ohkuma
  • Saisamorn LumyongEmail author
Article

Abstract

Diversity of yeasts in association with bees and their food sources has been explored during the last decade. In Thailand, there has been no study of yeast identification in honey and bees. Hence, a total of 186 yeast strains were isolated from 37 honey samples of 12 different bee species. On the basis of morphological and physiological characteristics, 55 representative strains were chosen and identified by sequence analysis of the 26S rDNA D1/D2 domain and the ITS region. The data were compared with the published sequences and the results showed the occurrence of 19 ascomycetous and 1 basidiomycetous yeast species. Six strains of the new species were isolated. Phylogenetic analysis of the 26S rDNA D1/D2 sequence revealed that they were conspecific and most closely related to Zygosaccharomyces mellis. Based on the ITS sequence, the new species was clustered with the type β and clearly distinguished from the type α. Sequence analysis of combined ITS-26S rDNA D1/D2 showed similar results. The occurrence of these two types, with a divergence of more than 1% in their sequences, and low DNA relatedness among them suggested that members of the type β can be regarded as separate species. An analysis of the morphological and physiological characteristics was performed. Ascospore formation was observed on acetate agar and Gorodkowa agar. The new Zygosaccharomyces species differed physiologically from Z. mellis in 4 assimilation tests. This data supports the hypothesis that the new species, Zygosaccharomyces siamensis, is a novel ascosporogenous yeast. The type strain is JCM 16825T (=CBS 12273T) and a description is given here.

Keywords

Ascosporogenous yeast Zygosaccharomyces siamensis Sugar tolerant yeasts Raw honey Thailand 

Notes

Acknowledgements

This work was funded by the Thai Government Science and Technology Scholarship for Ph.D. Study, awarded to S. Saksinchai, grant RSA5280010 from the Thailand Research Fund, the National Research University, and Office of the Higher Education Commission. We acknowledge fellowships granted by the Graduate School, Chiang Mai University. We appreciate A. Sawatthum at Rajamangala Institute of Technology, Thanyaburi for collection assistance in Chantaburi and Chumphon provinces. Permission from various local authorities to collect in many sites is gratefully acknowledged. Appreciation goes to K. Kennedy for help with the article’s English.

References

  1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedGoogle Scholar
  2. Arias MC, Sheppard WS (2005) Phylogenetic relationships of honey bees (Hymenoptera:Apinae:Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol Phylogenet Evol 37:25–35. doi: 10.1016/j.ympev.2005.02.017 PubMedGoogle Scholar
  3. Asadzadeh M, Ahmad S, Al-Sweih N, Khan ZU (2009) Rapid molecular differentiation and genotypic heterogeneity among Candida parapsilosis and Candida orthopsilosis strains isolated from clinical specimens in Kuwait. J Med Microbiol 58:745–752. doi: 10.1099/jmm.0.008235-0 PubMedGoogle Scholar
  4. Bassetti M, Righi E, Costa A, Fasce R, Molinari MP, Rosso R, Pallavicini FB, Viscoli C (2006) Epidemiological trends in nosocomial candidemia in intensive care. BMC Infect Dis 6:21. doi: 10.1186/1471-2334-6-21 PubMedGoogle Scholar
  5. Benda ND, Boucias D, Tort B, Teal P (2008) Detection and characterization of Kodamaea ohmeri associated with small hive beetle Aethina tumida infesting honey bee hives. J Apic Res Bee World 47:194–201. doi: 0.3827/IBRA.I.47.3.07 Google Scholar
  6. Bhadra B, Rao RS, Singh PK, Sarkar PK, Shivaji S (2008a) Yeasts and yeast-like fungi associated with tree bark: diversity and identification of yeasts producing extracellular endoxylanases. Curr Microbiol 56:489–494. doi: 10.1007/s00284-008-9108-x PubMedGoogle Scholar
  7. Bhadra B, Singh PK, Rao RS, Shivaji S (2008b) Blastobotrys serpentis sp. nov., isolated from the intestine of a Trinket snake (Elaphe sp., Colubridae). FEMS Yeast Res 8:492–498. doi: 10.1111/j.1567-1364.2008.00356.x PubMedGoogle Scholar
  8. Billon-Grand G (1989) A new ascosporogenous yeast genus: Yamadazyma gen. nov. Mycotaxon 35:201–204Google Scholar
  9. Boontop Y, Malaipan S, Chareansom K, Wiwatwittaya D (2008) Diversity of stingless bees (Apidae: Meliponini) in Thong Pha Phum District, Kanchanaburi Province, Thailand. Kasetsart J (Nat Sci) 42:444–456Google Scholar
  10. Brysch-Herzberg M (2004) Ecology of yeasts in plant–bumblebee mutualism in Central Europe. FEMS Microbiol Ecol 50:87–100. doi: 10.1016/j.femsec.2004.06.003 PubMedGoogle Scholar
  11. Burgaud G, Arzur D, Durand L, Cambon-Bonavita MA, Barbier G (2010) Marine culturable yeasts in deep-sea hydrothermal vents: species richness and association with fauna. FEMS Microbiol Ecol 73:121–133. doi: 10.1111/j.1574-6941.2010.00881.x PubMedGoogle Scholar
  12. Čadež N, Zupan J, Raspor P (2010) The effect of fungicides on yeast communities associated with grape berries. FEMS Yeast Res 10:619–630. doi: 10.1111/j.1567-1364.2010.00635.x PubMedGoogle Scholar
  13. Chaiyawong T, Deowanish S, Wongsiri S, Sylvester HA, Rinderer TE, de Guzman L (2004) Multivariate morphometric study of Apis florea in Thailand. J Apic Res 43:123–127Google Scholar
  14. Cocolin L, Aggio D, Manzano M, Cantoni C, Comi G (2002) An application of PCR-DGGE analysis to profile the yeast populations in raw milk. Int Dairy J 12:407–411Google Scholar
  15. Correia A, Sampaio P, Almeida J, Pais C (2004) Study of molecular epidemiology of candidiasis in Portugal by PCR fingerprinting of Candida clinical isolates. J Clin Microbiol 42:5899–5903. doi: 10.1128/JCM.42.12.5899-5903.2004 PubMedGoogle Scholar
  16. Csoma H, Sipiczki M (2008) Taxonomic reclassification of Candida stellata strains reveals frequent occurrence of Candida zemplinina in wine fermentation. FEMS Yeast Res 8:328–336. doi: 10.1111/j.1567-1364.2007.00339.x PubMedGoogle Scholar
  17. Daniel HM, Meyer W (2003) Evaluation of ribosomal RNA and actin gene sequences for the identification of ascomycetous yeasts. Int J Food Microbiol 86:61–78. doi: 10.1016/S0168-1605(03)00248-4 PubMedGoogle Scholar
  18. Daniel HM, Vrancken G, Takrama JF, Camu N, de Vos P, de Vuyst L (2009) Yeast diversity of Ghanaian cocoa bean heap fermentations. FEMS Yeast Res 9:774–783. doi: 10.1111/j.1567-1364.2009.00520.x PubMedGoogle Scholar
  19. Duarte FL, Pais C, Spencer-Martins I, Leão C (2004) Isoenzyme patterns: a valuable molecular tool for the differentiation of Zygosaccharomyces species and detection of misidentified isolates. System Appl Microbiol 27:436–442Google Scholar
  20. Egli CM, Henick-Kling T (2001) Identification of Brettanomyces/Dekkera species based on polymorphism in the rRNA internal transcribed spacer region. Am J Enol Vitic 52:241–247Google Scholar
  21. El-Latif Hesham A, Khan S, Liu X, Zhang Y, Wang Z, Min Yang M (2006) Application of PCR–DGGE to analyse the yeast population dynamics in slurry reactors during degradation of polycyclic aromatic hydrocarbons in weathered oil. Yeast 23:879–887. doi: 10.1002/yea.1401 PubMedGoogle Scholar
  22. Engel MS (1999) The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae; Apis). J Hym Res 8:165–196Google Scholar
  23. Enger L, Joly S, Pujol C, Simonson P, Pfaller M, Soll DR (2001) Cloning and characterization of a complex DNA fingerprinting probe for Candida parapsilosis. J Clin Microbiol 39:658–669. doi: 10.1128/JCM.39.2.658-669.2001 PubMedGoogle Scholar
  24. Etchells JL, Bell TA (1950) Film yeasts on commercial cucumber brines. Food Technol 4:77–83Google Scholar
  25. Fell JW, Boekhout T, Fonseca A, Scorzetti G, Statzell-Tallman A (2000) Biodiversity and systematics of basidiomycetous yeasts as determined by large-subunit rDNA D1/D2 domain sequence analysis. Int J Syst Evol Microbiol 50:1351–1371PubMedGoogle Scholar
  26. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791Google Scholar
  27. Fröhlich-Wyder MT (2003) Yeasts in dairy products. In: Boekhout T, Robert V (eds) Yeasts in food: beneficial and detrimental aspects. Behr’s Verlag, Hamburg, pp 209–237Google Scholar
  28. Gilliam M (1979) Microbiology of pollen and bee bread: the yeasts. Apidologie 10:43–53Google Scholar
  29. Gilliam M (1997) Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiol Lett 155:1–10Google Scholar
  30. Gilliam M, Wickerham LJ, Morton HL, Martin RD (1974) Yeasts isolated from honey bees, Apis mellifera, fed 2,4-D and antibiotics. J Invert Pathol 24:349–356Google Scholar
  31. Golonka AM (2002) Nectar-inhabiting yeasts in Silene latifolia and co-flowering plants. Dissertation, Duke UniversityGoogle Scholar
  32. Gomez-Lopez A, Alastruey-Izquierdo A, Rodriguez D, Almirante B, Pahissa A, Rodriguez-Tudela JL, Cuenca-Estrella M, the Barcelona Candidemia Project Study Group (2008) Prevalence and susceptibility profile of Candida metapsilosis and Candida orthopsilosis: results from population-based surveillance of candidemia in Spain. Antimicrob Agents Chemother 52:1506–1509. doi: 10.1128/AAC.01595-07 Google Scholar
  33. Gonçalves SS, Amorim CS, Nucci M, Padovan ACB, Briones MRS, Melo ASA, Colombo AL (2010) Prevalence rates and antifungal susceptibility profiles of the Candida parapsilosis species complex: results from a nationwide surveillance of candidaemia in Brazil. Clin Microbiol Infect 16:885–887. doi: 10.1016/j.ijfoodmicro.2009.10.011 PubMedGoogle Scholar
  34. Guo C, Zhao C, He P, Lu D, Shen A, Jiang N (2006) Screening and characterization of yeasts for xylitol production. J Appl Microbiol 101:1096–1104PubMedGoogle Scholar
  35. Heard TA (1999) The role of stingless bees in crop pollination. Annu Rev Entomol 44:183–206PubMedGoogle Scholar
  36. Hellström AM, Vázques-Juárez R, Svanberg U, Andlid TA (2010) Biodiversity and phytase capacity of yeasts isolated from Tanzanian togwa. Int J Food Microbiol 136:352–358. doi: 10.1111/j.1469-0691.2009.03020.x PubMedGoogle Scholar
  37. Hensgens LAM, Tavanti A, Mogavero S, Ghelardi E, Senesi S (2009) AFLP genotyping of Candida metapsilosis clinical isolates: evidence for recombination. Fungal Genet Biol 46:750–758. doi: 10.1016/j.fgb.2009.06.006 PubMedGoogle Scholar
  38. Hepburn HR, Radloff SE, Otis GW, Fuchs S, Verma LR, Ken T, Chaiyawong T, Tahmasebi G, Ebadi R, Wongsiri S (2005) Apis florea: morphometrics, classification and biogeography. Apidologie 36:359–376. doi: 10.1051/apido:2005023 Google Scholar
  39. Iida S, Imai T, Oguri T, Okuzumi K, Yamanaka A, Moretti-Branchini ML, Nishimura K, Mikami Y (2005) Genetic diversity of the internal transcribed spacers (ITS) and 5.8S rRNA genes among the clinical isolates of Candida parapsilosis in Brazil and Japan. Jpn J Med Mycol 46:133–137Google Scholar
  40. Inglis GD, Sigler L, Goettel MS (1993) Aerobic microorganisms associated with alfalfa leafcutter bees (Megachile rotundata). Microb Ecol 26:125–143Google Scholar
  41. Insuan S, Deowanish S, Klinbunga S, Sittipraneed S, Sylvester HA, Wongsiri S (2007) Genetic differentiation of the giant honey bee (Apis dorsata) in Thailand analyzed by mitochondrial genes and microsatellites. Biochem Genet 45:345–361. doi: 10.1007/s10528-007-9079-9 PubMedGoogle Scholar
  42. James SA, Stratford M (2003) Spoilage yeasts with emphasis on the genus Zygosaccharomyces. In: Boekhout T, Robert V (eds) Yeasts in food, beneficial and detrimental aspects. Behr’s Verlag, Hamburg, pp 171–191Google Scholar
  43. James SA, Bond CJ, Roberts IN (2001) Candida sorbosivorans sp. nov., a new member of the genus Candida Berkhout. Int J Syst Evol Microbiol 51:1215–1219PubMedGoogle Scholar
  44. Jongjitvimol T, Wattanachaiyingcharoen W (2006) Pollen food sources of the stingless bees Trigona apicalis Smith, 1857, Trigona collina Smith, 1857 and Trigona fimbriata Smith, 1857 (Apidae, Meliponinae) in Thailand. Nat Hist J Chulalongkorn Univ 6:75–82Google Scholar
  45. Jongjitvimol T, Wattanachaiyingcharoen W (2007) Distribution, nesting sites and nest structures of the stingless bee species, Trigona collina Smith, 1857 (Apidae, Meliponinae) in Thailand. Nat Hist J Chulalongkorn Univ 7:25–34Google Scholar
  46. Jongjitvimol T, Boontawon K, Wattanachaiyingcharoen W, Deowanish S (2005) Nest dispersion of a stingless bee species, Trigona collina Smith, 1857 (Apidae, Meliponinae) in a mixed deciduous forest in Thailand. Nat Hist J Chulalongkorn Univ 5:69–71Google Scholar
  47. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedGoogle Scholar
  48. Kirchner WH, Dreller C, Grasser A, Baidya D (1996) The silent dances of the Himalayan honeybee, Apis laboriosa. Apidologie 27:331–339Google Scholar
  49. Klakasikorn A, Wongsiri S, Deowanish S, Orawan Duangphakdee O (2005) New Record of Stingless Bees (Meliponini: Trigona) in Thailand. Nat Hist J Chulalongkorn Univ 5:1–7Google Scholar
  50. Kocsubé S, Tóth M, Vágvölgyi C, Dóczi I, Pesti M, Pócsi I, Szabó J, Varga J (2007) Occurrence and genetic variability of Candida parapsilosis sensu lato in Hungary. J Med Microbiol 56:190–195. doi: 10.1099/jmm.0.46838-0 PubMedGoogle Scholar
  51. Koeniger G, Koeniger N, Mardan M, Otis G, Wongsiri S (1991) Comparative anatomy of male genital organs in the genus Apis. Apidologie 22:539–552Google Scholar
  52. Kosa P, Valach M, Tomaska L, Wolfe KH, Nosek J (2006) Complete DNA sequences of the mitochondrial genomes of the pathogenic yeasts Candida orthopsilosis and Candida metapsilosis: insight into the evolution of linear DNA genomes from mitochondrial telomere mutants. Nucleic Acids Res 34:2472–2481. doi: 10.1093/nar/gkl327 PubMedGoogle Scholar
  53. Kreger-van Rij NJW (1964) A taxonomic study of the yeast genera Endomycopsis, Pichia, and Debaryomyces. Dissertation, University of LeidenGoogle Scholar
  54. Kurtzman CP (1990) DNA relatedness among species of the genus Zygosacharomyces. Yeast 6:213–219Google Scholar
  55. Kurtzman CP (1998) Issatchenkia Kudryavtsev emend. Kurtzman, Smiley & Johnson. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study, 4th edn. Elsevier, Amsterdam, pp 221–226Google Scholar
  56. Kurtzman CP (2003) Phylogenetic circumscription of Saccharomyces, Kluyveromyces and other members of the Saccharomycetaceae, and the proposal of the new genera Lachancea, Nakaseomyces, Naumovia, Vanderwaltozyma and Zygotorulaspora. FEMS Yeast Res 4:233–245. doi: 10.1016/S1567-1356(03)00175-2 PubMedGoogle Scholar
  57. Kurtzman CP, Fell JW (1998) Summary of species characteristics. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study, 4th edn. Elsevier, Amsterdam, pp 915–947Google Scholar
  58. Kurtzman CP, Robnett CJ (1997) Identification of clinically important ascomycetous yeasts based on nucleotide divergence in the 5’ end of the large-subunit (26S) ribosomal DNA gene. J Clin Microbiol 35:1216–1223PubMedGoogle Scholar
  59. Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie van Leeuwenhoek 73:331–371PubMedGoogle Scholar
  60. Kurtzman CP, Suzuki M (2010) Phylogenetic analysis of ascomycete yeasts that form coenzyme Q-9 and the proposal of the new genera Babjeviella, Meyerozyma, Millerozyma, Priceomyces, and Scheffersomyces. Mycoscience 51:2–14. doi: 10.1007/s10267-009-0011-5 Google Scholar
  61. Kurtzman CP, Robnett CJ, Basehoar-Powers E (2001) Zygosaccharomyces kombuchaensis, a new ascosporogenous yeast from `Kombucha tea'. FEMS Yeast Res 1:133–138PubMedGoogle Scholar
  62. Lachance MA, Bowles JM, Díaz MMC, Janzen DH (2001a) Candida cleridarum, Candida tilneyi and Candida powellii, three new yeast species isolated from insects associated with flowers. Int J Syst Evol Microbiol 51:1201–1207PubMedGoogle Scholar
  63. Lachance MA, Starmer WT, Rosa CA, Bowles JM, Barker JSF, Janzen DH (2001b) Biogeography of the yeasts of ephemeral flowers and their insects. FEMS Yeast Res 1:1–8PubMedGoogle Scholar
  64. Lachance MA, Dobson J, Wijayanayaka DN, Smith AME (2010) The use of parsimony network analysis for the formal delineation of phylogenetic species of yeasts: Candida apicola, Candida azyma, and Candida parazyma sp. nov., cosmopolitan yeasts associated with floricolous insects. Antonie van Leeuwenhoek 97:155–170. doi: 10.1007/s10482-009-9399-3 PubMedGoogle Scholar
  65. Laitila A, Wilhelmson A, Kotaviita E, Olkku J, Home S, Juvonen R (2006) Yeasts in an industrial malting ecosystem. J Ind Microbiol Biotechnol 33:953–966. doi: 10.1007/s10295-006-0150-z PubMedGoogle Scholar
  66. Lehmann PF, Lin D, Lasker BA (1992) Genotypic identification and characterization of species and strains within the genus Candida by using random amplified polymorphic DNA. J Clin Microbiol 30:3249–3254PubMedGoogle Scholar
  67. Lin D, Wu LC, Rinaldi MG, Lehmann PF (1995) Three distinct genotypes within Candida parapsilosis from clinical sources. J Clin Microbiol 33:1815–1821PubMedGoogle Scholar
  68. Lockhart SR, Messer SA, Pfaller MA, Daniel J, Diekema DJ (2008) Geographic distribution and antifungal susceptibility of the newly described species Candida orthopsilosis and Candida metapsilosis in comparison to the closely related species Candida parapsilosis. J Clin Microbiol 46:2659–2664. doi: 10.1128/JCM.00803-08 PubMedGoogle Scholar
  69. Lott TJ, Kuykendall RJ, Welbel SF, Pramanik A, Lasker BA (1993) Genomic heterogeneity in the yeast Candida parapsilosis. Curr Genet 23:463–467PubMedGoogle Scholar
  70. Messer SA, Jones RN, Fritsche TR (2006) International surveillance of Candida spp. and Aspergillus spp.: report from the SENTRY antimicrobial surveillance program (2003). J Clin Microbiol 44:1782–1787. doi: 10.1128/JCM.44.5.1782-1787.2006 PubMedGoogle Scholar
  71. Meyer SA, Payne RW, Yarrow D (1998) Candida Berkhout. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study, 4th edn. Elsevier, Amsterdam, pp 454–573Google Scholar
  72. Michener CD (1974) The social behavior of the bees. Harvard University Press, CambridgeGoogle Scholar
  73. Michener CD (2007) The bees of the world, 2nd edn. Johns Hopkins University Press, BaltimoreGoogle Scholar
  74. Mirhendi H, Bruun B, Schønheyder HC, Christensen JJ, Fuursted K, Gahrn-Hansen B, Johansen HK, Nielsen L, Knudsen JD, Arendrup MC (2010) Molecular screening for Candida orthopsilosis and Candida metapsilosis among Danish Candida parapsilosis group blood culture isolates: proposal of a new RFLP profile for differentiation. J Med Microbiol 59:414–420. doi: 10.1099/jmm.0.017293-0 PubMedGoogle Scholar
  75. Morais PB, Rosa CA, Hagler AN, Mendonca-Hagler LC (1994) Yeast communities of the cactus Pilosocereus arrabidae as resources for larval and adult stages of Drosophila serido. Antonie van Leeuwenhoek 66:313–317PubMedGoogle Scholar
  76. Nagahama T, Hamamoto M, Nakase T, Horikoshi K (2001a) Rhodotorula lamellibrachii sp. nov., a new yeast species from a tubeworm collected at the deep-sea floor in Sagami Bay and its phylogenetic analysis. Antonie van Leeuwenhoek 80:317–323PubMedGoogle Scholar
  77. Nagahama T, Hamamoto M, Nakase T, Takami H, Horikoshi K (2001b) Distribution and identification of red yeasts in deep-sea environments around the northwest Pacific Ocean. Antonie van Leeuwenhoek 80:101–110PubMedGoogle Scholar
  78. Nagahama T, Hamamoto M, Nakase T, Horikoshi K (2003) Rhodotorula benthica sp. nov. and Rhodotorula calyptogenae sp. nov., novel yeast species from animals collected from the deep-sea floor, and Rhodotorula lysiniphila sp. nov., which is related phylogenetically. Int J Syst Evol Microbiol 53:897–903. doi: 10.1099/ijs.0.02395-0 x PubMedGoogle Scholar
  79. Nguyen NH, Suh SO, Blackwell M (2007) Five novel Candida species in insect-associated yeast clades isolated from Neuroptera and other insects. Mycologia 99:842–858PubMedGoogle Scholar
  80. Nisiotou AA, Chorianopoulos N, Nychas GJE, Panagou EZ (2010) Yeast heterogeneity during spontaneous fermentation of black Conservolea olives in different brine solutions. J Appl Microbiol 108:396–405. doi: 10.1111/j.1365-2672.2009.04424.x PubMedGoogle Scholar
  81. Nosek J, Tomáška L, Ryčovská A, Fukuhara H (2002) Mitochondrial telomeres as molecular markers for identification of the opportunistic yeast pathogen Candida parapsilosis. J Clin Microbiol 40:1283–1289. doi: 10.1128/JCM.40.4.1283-1289.2002 PubMedGoogle Scholar
  82. Oldroyd BP, Wongsiri S (2006) Asian honey bees: biology, conservation, and human interactions. Harvard University Press, CambridgeGoogle Scholar
  83. Péter G, Tornai-Lehoczki J, Dlauchy D (2009) Trichomonascus apis sp. nov., a heterothallic yeast species from honeycomb. Int J Syst Evol Microbiol 59:1550–1554PubMedGoogle Scholar
  84. Pimentel MRC, Antonini Y, Martins RP, Lachance MA, Rosa CA (2005) Candida riodocensis and Candida cellae, two new yeast species from the Starmerella clade associated with solitary bees in the Atlantic rain forest of Brazil. FEMS Yeast Res 5:875–879. doi: 10.1016/j.femsyr.2005.03.006 PubMedGoogle Scholar
  85. Prista C, Loureiro-Dias MC (2007) Debaryomyces hansenii, a salt loving spoilage yeast. In: Pereira MS (ed) A portrait of state-of-the-art research at the Technical University of Lisbon, part 7. Springer, Dordrecht, pp 457–464. doi: 10.1007/978-1-4020-5690-1_28 Google Scholar
  86. Pryce TM, Palladino S, Price DM, Gardam DJ, Campbell PB, Christiansen KJ, Murray RJ (2006) Rapid identification of fungal pathogens in BacT/ALERT, BACTEC, and BBL MGIT media using polymerase chain reaction and DNA sequencing of the internal transcribed spacer regions. Diagn Microbiol Infect Dis 54:289–297. doi: 10.1016/j.diagmicrobio.2005.11.002 PubMedGoogle Scholar
  87. Raffiudin R, Crozier RH (2007) Phylogenetic analysis of honey bee behavioral evolution. Mol Phylogenet Evol 43:543–552. doi: 10.1016/j.ympev.2006.10.013 PubMedGoogle Scholar
  88. Rao RS, Bhadra B, Kumar NN, Shivaji S (2007a) Candida hyderabadensis sp. nov., a novel ascomycetous yeast isolated from wine grapes. Yeast Res 7:489–493. doi: 10.1111/j.1567-1364.2006.00206.x Google Scholar
  89. Rao RS, Bhadra B, Shivaji S (2007b) Isolation and characterization of xylitol-producing yeasts from the gut of colleopteran insects. Curr Microbiol 55:441–446. doi: 10.1007/s00284-007-9005-8 PubMedGoogle Scholar
  90. Rinderer TE, Oldroyd BP, Wongsiri S, Sylvester HA, de Guzman LI, Stelzer JA, Riggio RM (1995) A morphological comparison of the dwarf honey bees of southeastern Thailand and Palawan, Philippines. Apidologie 26:387–394Google Scholar
  91. Rosa CA, Lachance MA (1998) The yeast genus Starmerella gen. nov. and Starmerella bombicola sp. nov., the teleomorph of Candida bombicola (Spencer, Gorin & Tullock) Meyer & Yarrow. Int J Syst Bacteriol 48:1413–1417PubMedGoogle Scholar
  92. Rosa CA, Lachance MA (2005) Zygosaccharomyces machadoi sp. n., a yeast species isolated from a nest of the stingless bee Tetragonisca angustula. Lundiana 6:27–29Google Scholar
  93. Rosa CA, Viana EM, Martins RP, Antonini Y, Lachance MA (1999) Candida batistae, a new yeast species associated with solitary digger nesting bees in Brazil. Mycologia 91:428–433Google Scholar
  94. Rosa CA, Lachance MA, Silva JOC, Teixeira ACP, Marini MM, Antonini Y, Martins RP (2003) Yeast communities associated with stingless bees. FEMS Yeast Res 4:271–275. doi: 10.1016/S1567-1356(03)00173-9 PubMedGoogle Scholar
  95. Rosa CA, Pagnocca FC, Lachance MA, Ruivo CCC, Medeiros AO, Pimentel MRC, Fontenelle JCR, Martins RP (2007) Candida flosculorum sp. nov. and Candida floris sp. nov., two yeast species associated with tropical flowers. Int J Syst Evol Microbiol 57:2970–2974. doi: 10.1099/ijs.0.65230-0 PubMedGoogle Scholar
  96. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, CambridgeGoogle Scholar
  97. Roubik DW (2006) Stingless bee nesting biology. Apidologie 37:124–143Google Scholar
  98. Roy B, Meyer SA (1998) Confirmation of the distinct genotype groups within the form species Candida parapsilosis. J Clin Microbiol 36:216–218PubMedGoogle Scholar
  99. Safdar A, Perlin DS, Armstrong D (2002) Hematogenous infections due to Candida parapsilosis: changing trends in fungemic patients at a comprehensive cancer center during the last four decades. Diagn Microbiol Infect Dis 44:11–16PubMedGoogle Scholar
  100. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  101. Samelis J, Sofos JN (2003) Yeasts in meat and meat products. In: Boekhout T, Robert V (eds) Yeasts in food: beneficial and detrimental aspects. Behr’s Verlag, Hamburg, pp 239–265Google Scholar
  102. Schwarz HF (1939) The Indo-Malayan species of Trigona. Bull Amer Mus Nat Hist 76:83–141Google Scholar
  103. Sette LD, Passarini MRZ, Rodrigues A, Leal RR, Simioni KCM, Nobre FS, de Brito BR, da Rocha AJ, Pagnocca FC (2010) Fungal diversity associated with Brazilian energy transmission towers. Fungal Divers 44:53–63. doi: 10.1007/s13225-010-0048-y Google Scholar
  104. Silva AP, Miranda IM, Lisboa C, Pina-Vaz C, Rodrigues AG (2009) Prevalence, distribution, and antifungal susceptibility profiles of Candida parapsilosis, C. orthopsilosis, and C. metapsilosis in a tertiary care hospital. J Clin Microbiol 47:2392–2397. doi: 10.1128/JCM.02379-08 PubMedGoogle Scholar
  105. Sipiczki M, Ciani M, Csoma H (2005) Taxonomic reclassification of Candida stellata DBVPG 3827. Folia Microbiol 50:494–498Google Scholar
  106. Smith DR, Villafuerte L, Otis G, Palmer MR (2000) Biogeography of Apis cerana F. and A. nigrocincta Smith: insights from mtDNA studies. Apidologie 31:265–279Google Scholar
  107. Snowdon JA, Cliver DO (1996) Microorganisms in honey. Int J Food Microbiol 31:1–26Google Scholar
  108. Spencer JFT, Spencer DM (1997) Ecology: where yeasts live. In: Spencer JFT, Spencer DM (eds) Yeasts in natural and artificial habitats. Springer, Berlin, pp 33–58Google Scholar
  109. Steels H, Bond CJ, Collins MD, Roberts IN, Stratford M, James SA (1999) Zygosaccharomyces lentus sp. nov., a new member of the yeast genus Zygosaccharomyces Barker. Int J Syst Bacteriol 49:319–327PubMedGoogle Scholar
  110. Steels H, James SA, Bond CJ, Roberts IN, Stratford M (2002) Zygosaccharomyces kombuchaensis: the physiology of a new species related to the spoilage yeasts Zygosaccharomyces lentus and Zygosaccharomyces bailii. FEMS Yeast Res 2:113–121PubMedGoogle Scholar
  111. Stratford M, Bond CJ, James SA, Roberts IN, Steels H (2002) Candida davenportii sp. nov., a potential soft-drinks spoilage yeast isolated from a wasp. Int J Syst Evol Microbiol 52:1369–1375. doi: 10.1099/ijs.0.02088-0 Google Scholar
  112. Suezawa Y, Suzuki M (2007) Bioconversion of ferulic acid to 4-vinylguaiacol and 4-ethylguaiacol and of 4-vunylguaiacol to 4-ethylguaiacol by halotolerant yeasts belonging to the genus Candida. Biosci Biotechnol Biochem 71:1058–1062PubMedGoogle Scholar
  113. Suezawa Y, Kimura I, Inoue M, Gohda N, Suzuki M (2006) Identification and typing of miso and soy sauce fermentation yeasts, Candida etchellsii and C. versatilis, based on sequence analyses of the D1D2 domain of the 26S ribosomal RNA gene, and the region of internal transcribed spacer 1, 5.8S ribosomal RNA gene and internal transcribed spacer 2. Biosci Biotechnol Biochem 70:348–354PubMedGoogle Scholar
  114. Suezawa Y, Suzuki M, Mori H (2008) Genotyping of a miso and soy sauce fermentation yeast, Zygosaccharomyces rouxii, based on sequence analysis of the partial 26S ribosomal RNA gene and two internal transcribed spacers. Biosci Biotechnol Biochem 79:2452–2455. doi: 10.1271/bbb.80211 Google Scholar
  115. Suh SO, Blackwell M (2004) Three new beetle-associated yeast species in the Pichia guilliermondii clade. FEMS Yeast Res 5:87–95. doi: 10.1016/j.femsyr.2004.06.001 PubMedGoogle Scholar
  116. Suh SO, McHugh JV, Pollock DD, Blackwell M (2005) The beetle gut: a hyperdiverse source of novel yeasts. Mycol Res 109:261–265. doi: 10.1017/S0953756205002388 PubMedGoogle Scholar
  117. Suh SO, Nguyen NH, Blackwell M (2008) Yeasts isolated from plant-associated beetles and other insects: seven novel Candida species near Candida albicans. FEMS Yeast Res 8:88–102. doi: 10.1111/j.1567-1364.2007.00320.x PubMedGoogle Scholar
  118. Tapia-Tussell R, Lappe P, Ulloa M, Quijano-Ramayo A, Cáceres-Farfán M, Larqué-Saavedra A, Perez-Brito D (2006) A rapid and simple method for DNA extraction from yeasts and fungi isolated from Agave fourcroydes. Mol Biotechnol 33:67–70PubMedGoogle Scholar
  119. Tavanti A, Davidson AD, Gow NAR, Maiden MCJ, Odds FC (2005) Candida orthopsilosis and Candida metapsilosis spp. nov. to replace Candida parapsilosis groups II and III. J Clin Microbiol 43:284–292. doi: 10.1128/JCM.43.1.284-292.2005 PubMedGoogle Scholar
  120. Tavanti A, Hensgens LAM, Ghelardi E, Campa M, Senesi S (2007) Genotyping of Candida orthopsilosis clinical isolates by amplification fragment length polymorphism reveals genetic diversity among independent isolates and strain maintenance within patients. J Clin Microbiol 45:1455–1467. doi: 10.1128/JCM.00243-07 PubMedGoogle Scholar
  121. Tay ST, Na SL, Chong J (2009) Molecular differentiation and antifungal susceptibilities of Candida parapsilosis isolated from patients with bloodstream infections. J Med Microbiol 58:185–191. doi: 10.1099/jmm.0.004242-0 PubMedGoogle Scholar
  122. Teixeira ACP, Marini MM, Nicoli JR, Antonini Y, Martins RP, Lachance MA, Rosa CA (2003) Starmerella meliponinorum sp. nov., a novel ascomycetous yeast species associated with stingless bees. Int J Syst Evol Microbiol 53:339–343. doi: 10.1099/ijs.0.02262-0 PubMedGoogle Scholar
  123. Thanh VN, van Dyk MS, Wingfeld MJ (2002) Debaryomyces mycophilus sp. nov., a siderophore-dependent yeast isolated from woodlice. FEMS Yeast Res 2:415–427PubMedGoogle Scholar
  124. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedGoogle Scholar
  125. Tofalo R, Chaves-López C, di Fabio F, Schirone M, Felis GE, Torriani S, Paparella A, Suzzi G (2009) Molecular identification and osmotolerant profile of wine yeasts that ferment a high sugar grape must. Int J Food Microbiol 130:179–187. doi: 10.1016/j.ijfoodmicro.2009.01.024 PubMedGoogle Scholar
  126. Tokuoka K (1993) Sugar- and salt-tolerant yeasts. J Appl Bacteriol 74:101–110Google Scholar
  127. Torriani S, Lorenzini M, Salvetti E, Felis GE (2011) Zygosaccharomyces gambellarensis sp. nov., a new ascosporogenous yeast isolated from an Italian “passito” style wine. Int J Syst Evol Microbiol (in press). doi: 10.1099/ijs.0.031146-0
  128. Torto B, Boucias DG, Arbogast RT, Tumlinson JH, Teal PEA (2007) Multitrophic interaction facilitates parasite-host relationship between an invasive beetle and the honey bee. Proc Natl Acad Sci 104:8374–8378PubMedGoogle Scholar
  129. Trindade RC, Resende MA, Silva CM, Rosa CA (2002) Yeasts associated with fresh and frozen pulps of Brazilian tropical fruits. System Appl Microbiol 25:294–300Google Scholar
  130. Underwood BA (1990) Time of drone flight of Apis laboriosa Smith in Nepal. Apidologie 21:501–504Google Scholar
  131. Urubschurov V, Janczyk P, Pieper R, Souffrant WB (2008) Biological diversity of yeasts in the gastrointestinal tract of weaned piglets kept under different farm conditions. FEMS Yeast Res 8:1349–1356. doi: 10.1111/j.1567-1364.2008.00444.x PubMedGoogle Scholar
  132. Vaughan-Martini A, Kurtzman CP, Meyer SA, O’Neill EB (2005) Two new species in the Pichia guilliermondii clade: Pichia caribbica sp. nov., the ascosporic state of Candida fermentati, and Candida carpophila comb. nov. FEMS Yeast Res 5:463–469. doi: 10.1016lj.femsyr.2004.10.008 PubMedGoogle Scholar
  133. Vega FE, Blackburn MB, Kurtzman CP, Dowd PF (2003) Identification of a coffee berry borer-associated yeast: does it break down caffeine? Entomol Exp Appl 107:19–24Google Scholar
  134. Westall S, Filtenborg O (1998) Spoilage yeasts of decorated soft cheese packed in modified atmosphere. Food Microbiol 15:243–249Google Scholar
  135. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, Taylor TJ (eds) PCR protocols: a guide for methods and applications. Academic, New York, pp 315–322Google Scholar
  136. Wongsiri S, Limbipichai K, Tangkanasing P, Mardan M, Rinderer TE, Sylvester HA, Koeniger G, Otis G (1990) Evidence of reproductive isolation confirms that Apis andreniformis (Smith, 1858) is a separate species from sympatric Apis florea (Fabricius, 1787). Apidologie 21:47–52Google Scholar
  137. Wongsiri S, Lekprayoon C, Thapa R, Thirakupt K, Rinderer TE, Sylvester HA, Oldroyd BP, Booncham U (1996) Comparative biology of Apis andreniformis and Apis florea in Thailand. Bee World 77:23–35Google Scholar
  138. Yamada Y, Suzuki T, Matsuda M, Mikata K (1995a) The phylogenetic relationships of the Q9-equipped, hat-shaped ascospore-forming species of the genus Yamadazyma Billion-Grand (Saccharomycetaceae) based on the partial sequences of 18S and 26S ribosomal RNAs. Biosci Biotechol Biochem 59:445–450Google Scholar
  139. Yamada Y, Suzuki T, Matsuda M, Mikata K (1995b) The phylogeny of Yamadazyma ohmeri (Etchells et Bell) Billon-Grand based on the partial sequences of 18S and 26S ribosomal RNAs: the proposal of Kodamaea gen. nov. (Saccharomycetaceae). Biosci Biotechol Biochem 59:1172–1174Google Scholar
  140. Yarrow D (1998) Methods for the isolation, maintenance and identification of yeasts. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study, 4th edn. Elsevier, Amsterdam, pp 77–100Google Scholar
  141. Yukawa M, Maki T (1931) Schizosaccharomyces japonicas nov. spec. La. Bul. Sci. Fakultato Terkultura, Kjusu Imp. Univ., Fukuoka, Japan 4:218–226. In Japanese; English summaryGoogle Scholar
  142. Zacchi L, Vaughan-Martini A (2002) Yeasts associated with insects in agricultural areas of Perugia, Italy. Ann Microbiol 52:237–244Google Scholar

Copyright information

© Kevin D. Hyde 2011

Authors and Affiliations

  • Sujinan Saksinchai
    • 1
    • 2
  • Motofumi Suzuki
    • 3
  • Panuwan Chantawannakul
    • 4
  • Moriya Ohkuma
    • 3
  • Saisamorn Lumyong
    • 4
    Email author
  1. 1.The Graduate SchoolChiang Mai UniversityChiang MaiThailand
  2. 2.Department of Biology, Faculty of ScienceChiang Mai UniversityChiang MaiThailand
  3. 3.Microbe Division/Japan Collection of Microorganisms (JCM)RIKEN BioResource CenterWakoJapan
  4. 4.Department of Biology, Faculty of ScienceChiang Mai UniversityChiang MaiThailand

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