Abstract
This study aimed to isolate and identify yeasts from peat in To Daeng peat swamp forest in southern of Thailand, and to investigate their ability to produce ethanol from glucose and xylose and to produce indole-3-acetic acid (IAA) and extracellular enzymes. A total of 65 yeast strains were obtained from 15 peat samples using an enrichment technique, and 61 strains were identified to be five species belonging to the phylum Ascomycota, namely Cyberlindnera subsufficiens, Debaryomyces fabryi, Meyerozyma guilliermondii, Saturnispora diversa and Schwanniomyces polymorphus var. africanus, and five species of the phylum Basidiomycota, namely Cryptococcus taiwanensis pro tem, Cutaneotrichosporon mucoides, Papiliotrema flavescens, Papiliotrema laurentii and Rhodotorula mucilaginosa. Four strains were unidentified and require further analysis. They differed from the type strain of P. flavescens by two nucleotide substitutions in the D1/D2 region of the LSU rRNA gene and nine nucleotide substitutions in the ITS region. R. mucilaginosa was the most prevalent yeast species, followed by S. polymorphus var. africanus, Cy. subsufficiens and D. fabryi. None of the yeast strains obtained in this study were able to ferment xylose to ethanol, but all ascomycetous yeast strains produced ethanol from glucose in a range of 9.0–58.0 g/L, with Cy. subsufficiens DMKU-YNB42-1 producing the highest ethanol concentration. A total of 62 strains produced IAA in a range of 9.0 to 66.9 mg/L, with the highest IAA produced by R. mucilaginosa DMKU-Y33-A. Investigation of the production of cellulases, xylanase, pectinase, amylase, protease and lipase revealed that all 65 yeast strains produced at least one extracellular enzyme, a lipase.
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Altschul SF, Madden TL, Schaffer 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 25:3389–3402
Anagnostakis SL, Hankin L (1975) Use of selective media to detect enzyme production by microorganisms in food products. J Milk Food Technol 38:570–572
Boonmak C, Jindamorakot S, Kawasaki H, Yongmanitchai W, Suwanarit P, Nakase T, Limtong S (2009) Candida siamensis sp. nov., an anamorphic yeast species in the Saturnispora clade isolated in Thailand. FEMS Yeast Res 9:668–672
Boonyuen N, Sri-Indrasutdhi V, Suetrong S, Sivichai S, Jones EG (2012) Annulatascus aquatorba sp. nov., a lignicolous freshwater ascomycete from Sirindhorn Peat Swamp Forest, Narathiwat, Thailand. Mycologia 104:746–757
Botha A (2006) Yeasts in soil. In: Rosa C, Gabor P (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 221–240
Bunterngsook B, Kanokratana P, Thongaram T, Tanapongpipat S, Uengwetwanit T, Rachdawong S, Vichitsoonthonkul T, Eurwilaichitr L (2010) Identification and characterization of lipolytic enzymes from a peat-swamp forest soil metagenome. Biosci Biotechnol Biochem 74:1848–1854
Buzzini P, Martini A (2002) Extracellular enzymatic activity profiles in yeast and yeast‐like strains isolated from tropical environments. J Appl Microbiol 93:1020–1025
Carrasco M, Rozas JM, Barahona S, Alcaíno J, Cifuentes V, Baeza M (2012) Diversity and extracellular enzymatic activities of yeasts isolated from King George Island, the sub-Antarctic region. BMC Microbiol 12:251
Carvalho FP, Cristina de Souza A, Magalhães-Guedes KT, Dias DR, Silva CF, Schwan RF (2013) Yeasts diversity in Brazilian Cerrado soils: study of the enzymatic activities. Afr J Microbiol Res 7:4176–4190
Charoenchai C, Fleet GH, Henschke PA, Todd BENT (1997) Screening of non-Saccharomyces wine yeasts for the presence of extracellular hydrolytic enzymes. Aust J Grape Wine Res 3:2–8
Chimner RA, Ewel KC (2005) A tropical freshwater wetland: II. Production, decomposition, and peat formation. Wetl Ecol Manag 13:671–684
Cleland RE (1990) Auxin and cell elongation. In: Davies PJ (ed) Plant hormones. Springer, pp 132–148
Dedysh SN, Pankratov TA, Belova SE, Kulichevskaya IS, Liesack W (2006) Phylogenetic analysis and in situ identification of bacteria community composition in an acidic Sphagnum peat bog. Appl Environ Microbiol 72:2110–2117
Fell JW, Blatt GM, Statzell-Tallman A (1998) Validation of the basidiomycetous yeast, Sporidiobolus microsporus sp. nov., based on phenotypic and molecular analyses. Antonie Van Leeuwenhoek 74:265–270
Fell JW, Roeijmans H, Boekhout T (1999) Cystofilobasidiales, a new order of basidiomycetous yeasts. Int J Syst Evol Microbiol 49:907–913
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 50:1351–1371
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Fonseca Á, Boekhout T, Fell JW (2011) Cryptococcus Vuillemin (1901). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, London, pp 1661–1737
Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 6:793–796
Goldbeck R, Maugeri Filho F (2013) Screening, characterization, and biocatalytic capacity of lipases producing wild yeasts from Brazil biomes. Food Sci Biotechnol 22:79–87
Gomes FC, Safar SV, Marques AR, Medeiros AO, Santos AR, Carvalho C, Lachance MA, Sampaio JP, Rosa CA (2015) The diversity and extracellular enzymatic activities of yeasts isolated from water tanks of Vriesea minarum, an endangered bromeliad species in Brazil, and the description of Occultifur brasiliensis f.a., sp. nov. Antonie Van Leeuwenhoek 107:597–611
Grum-Grzhimaylo OA, Debets AJM, Bilanenko EN (2016) The diversity of microfungi in peatlands originated from the White Sea. Mycologia 108:233–254
Hadi A, Fatah L, Affandi DN, Bakar RA, Inubushi K (2012) Population and genetic diversities of bacteria related to nitrous oxide and methane in peat soils of South Kalimantan, Indonesia. Malays J Soil Sci 16:121–135
Hooijer A, Page S, Jauhiainen J, Lee WA, Lu XX, Idris A, Anshari G (2012) Subsidence and carbon loss in drained tropical peatlands. Biogeosciences 9:1053–1071
Huang C, Lee F, Tien C (2011) Cryptococcus taiwanensis sp. nov., a novel yeast in Taiwan. Fungal Sci 26:57–64
Ignatova LV, Brazhnikova YV, Berzhanova RZ, Mukasheva TD (2015) Plant growth-promoting and antifungal activity of yeasts from dark chestnut soil. Microbiol Res 175:78–83
Jackson CR, Liew KC, Yule CM (2009) Structural and functional changes with depth in microbial communities in a tropical Malaysian peat swamp forest. Microb Ecol 57:402–12
Johnson EA, Echavarri-Erasun C (2011) Yeast biotechnology. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, London, pp 21–44
Kachalkin AV, Yurkov AM (2012) Yeast communities in Sphagnum phyllosphere along the temperature-moisture ecocline in the boreal forest-swamp ecosystem and description of Candida sphagnicola sp. nov. Antonie Van Leeuwenhoek 102:29–43
Kachalkin AV, Glushakova AM, Yurkov AM, Chernov IY (2008) Characterization of yeast groupings in the phyllosphere of Sphagnum mosses. Microbiology 77:474–481
Kasana RC, Salwan R, Dhar H, Dutt S, Gulati A (2008) A rapid and easy method for the detection of microbial cellulases on agar plates using Gram’s iodine. Curr Microbiol 57:503–507
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kurtzman CP (2011a) Lindnera Kurtzman, Robnett & Basehoar-Powers (2008). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, London, pp 521–543
Kurtzman CP (2011b) Meyerozyma Kurtzman & M. Suzuki (2010). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, London, pp 621–624
Kurtzman CP (2015) Description of Martiniozyma gen. nov. and transfer of seven Candida species to Saturnispora as new combinations. Antonie Van Leeuwenhoek 108:803–809
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 35:1216–1223
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 73:331–371
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
Kurtzman CP, Robnett CJ, Basehoar-Powers E (2008) Phylogenetic relationships among species of Pichia, Issatchenkia and Williopsis determined from multigene sequence analysis, and the proposal of Barnettozyma gen. nov., Lindnera gen. nov. and Wickerhamomyces gen. nov. FEMS Yeast Res 8:939–954
Lachance M-A, Boekhout T, Scorzetti G, Fell JW, Kurtzman CP (2011) Candida Berkhout (1923). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, London, pp 987–1278
Lee J-S, Park E-H, Kim J-W, Yeo S-H, Kim M-D (2013) Growth and fermentation characteristics of Saccharomyces cerevisiae NK28 isolated from kiwi fruit. J Microbiol Biotechnol 23:1253–1259
Limtong S, Koowadjanakul N (2012) Yeasts from phylloplane and their capability to produce indole-3-acetic acid. World J Microbiol Biotechnol 28:3323–3335
Limtong S, Yongmanitchai W (2010) Candida chanthaburiensis sp. nov., Candida kungkrabaensis sp. nov. and Candida suratensis sp. nov., three novel yeast species from decaying plant materials submerged in water of mangrove forest. Antonie Van Leeuwenhoek 98:379–388
Limtong S, Sringiew C, Yongmanitchai W (2007) Production of fuel ethanol at high temperature from sugar cane juice by a newly isolated Kluyveromyces marxianus. Bioresou Technol 98:367–3374
Limtong S, Yongmanitchai W, Kawasaki H, Seki T (2008) Candida phangngensis sp. nov., an anamorphic yeast species in the Yarrowia clade, isolated from water in mangrove forests in Phang-Nga Province, Thailand. Int J Syst Evol Microbiol 58:515–519
Limtong S, Yongmanitchai W, Kawasaki H, Fujiyama K (2009) Wickerhamomyces edaphicus sp. nov. and Pichia jaroonii sp. nov., two ascomycetous yeast species isolated from forest soil in Thailand. FEMS Yeast Res 9:504–510
Limtong S, Nitiyon S, Kaewwichian R, Jindamorakot S, Am-In S, Yongmanitchai W (2012) Wickerhamomyces xylosica sp. nov. and Candida phayaonensis sp. nov., two xylose-assimilating yeast species from soil. Int J Syst Evol Microbiol 62:2786–2792
Limtong S, Kaewwichian R, Yongmanitchai W, Kawasaki H (2014) Diversity of culturable yeasts in phylloplane of sugarcane in Thailand and their capability to produce indole-3-acetic acid. World J Microbiol Biotechnol 30:1785–1796
Liu XZ, Wang QM, Göker M, Groenewald M, Kachalkin AV, Lumbsch HT, Millanes AM, Wedin M, Yurkov AM, Boekhout T, Bai FY (2016) Towards an integrated phylogenetic classification of the Tremellomycetes. Stud Mycol 81:85–147
Molnarova J, Vadkertiova R, Stratilova E (2014) Extracellular enzymatic activities and physiological profiles of yeasts colonizing fruit trees. J Basic Microbiol 54(Suppl 1):S74–84
Mukherjee S, Sen SK (2015) Exploration of novel rhizospheric yeast isolate as fertilizing soil inoculant for improvement of maize cultivation. J Sci Food Agric 95:1491–1499
Nasanit R, Tangwong-o-thai A, Tantirungkij M, Limtong S (2015) The assessment of epiphytic yeast diversity in sugarcane phyllosphere in Thailand by culture‐independent method. Fungal Biol 119:1145–1157
Pinnoi A, Lumyong S, Hyde KD, Jones EG (2006) Biodiversity of fungi on the palm Eleiodoxa conferta in Sirindhorn peat swamp forest, Narathiwat, Thailand. Fungal Divers 22:205–218
Posa MRC, Wijedasa LS, Corlett RT (2011) Biodiversity and conservation of tropical peat swamp forests. Bioscience 61:49–57
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sampaio JP (2011) Rhodotorula Harrison (1928). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, London, pp 1873–1927
Sarawan S, Mahakhan P, Jindamorakot S, Vichitphan K, Vichitphan S, Sawaengkaew J (2013) Candida konsanensis sp. nov., a new yeast species isolated from Jasminum adenophyllum in Thailand with potentially carboxymethyl cellulase-producing capability. World J Microbiol Biotechnol 29:1481–1486
Silva-Bedoya LM, Ramirez-Castrillon M, Osorio-Cadavid E (2014) Yeast diversity associated to sediments and water from two Colombian artificial lakes. Braz J Microbiol 45:135–142
Sugita T (2011) Trichosporon Behrend (1890). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, London, pp 2015–2061
Sugita T, Takashima M, Ikeda R, Nakase T, Shinoda T (2000) Intraspecies diversity of Cryptococcus laurentii as revealed by sequences of internal transcribed spacer regions and 28S rRNA gene and taxonomic position of C. laurentii clinical isolates. J Clin Microbiol 38:1468–1471
Sun P-F, Fang W-T, Shin L-Y, Wei J-Y, Fu S-F, Chou J-Y (2014) Indole-3-acetic acid-producing yeasts in the phyllosphere of the carnivorous plant Drosera indica L. PLoS One 9:e114196
Suzuki M, Kurtzman CP (2011) Schwanniomyces Klöcker emend., M. Suzuki & Kurtzman (2010). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, London, pp 785–794
Suzuki M, Prasad GS, Kurtzman CP (2011) Debaryomyces Lodder & Kreger-van Rij (1952). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, London, pp 361–372
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Thormann MN, Rice AV, Beilman DW (2007) Yeasts in peatlands: a review of richness and roles in peat decomposition. Wetlands 27:761–773
Vaughan-Martini A, Martini A (2011) Saccharomyces Meyen ex Reess (1870). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, London, pp 733–746
Wang L, Chi Z, Wang X, Liu Z, Li J (2007) Diversity of lipase-producing yeasts from marine environments and oil hydrolysis by their crude enzymes. Ann Microbiol 57:495–501
Wang QM, Groenewald M, Takashima M, Theelen B, Han PJ, Liu XZ, Boekhout T, Bai FY (2016) Phylogeny of yeasts and related filamentous fungi within Pucciniomycotina determined from multigene sequence analyses. Stud Mycol 81:27–53
Weintraub SR, Wieder WR, Cleveland CC, Townsend AR (2013) Organic matter inputs shift soil enzyme activity and allocation patterns in a wet tropical forest. Biogeochemistry 114:313–326
Yalcin HT, Corbaci C, Ucar FB (2014) Molecular characterization and lipase profiling of the yeasts isolated from environments contaminated with petroleum. J Basic Microbiol 54(Suppl 1):S85–92
Yang Q, Zhang H, Li X, Wang Z, Xu Y, Ren S, Chen X, Xu Y, Hao H, Wang H (2013) Extracellular enzyme production and phylogenetic distribution of yeasts in wastewater treatment systems. Bioresour Technol 129:264–273
Yurkov A, Guerreiro MA, Sharma L, Carvalho C, Fonseca Á (2015) Multigene assessment of the species boundaries and sexual status of the basidiomycetous yeasts Cryptococcus flavescens and C. terrestris (Tremellales). PLoS One 10(3):e0120400. doi:10.1371/journal.pone.0120400
Acknowledgments
This work was supported by the Office of The Royal Development Projects Board, Thailand, The Pikunthong Royal Development Study Centre, Land Development Department, Thailand, and the Higher Education Research Promotion and National Research University Project of Thailand. The authors would like to thank Dr. Pisoot Vijarnsorn, Ms. Saiyud Petsik and Mr. Anurak Buakleeklay, Land Development Department, for their valuable comments, peat sample collection and peat analysis.
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Jaiboon, K., Lertwattanasakul, N., Limtong, P. et al. Yeasts from peat in a tropical peat swamp forest in Thailand and their ability to produce ethanol, indole-3-acetic acid and extracellular enzymes. Mycol Progress 15, 755–770 (2016). https://doi.org/10.1007/s11557-016-1205-9
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DOI: https://doi.org/10.1007/s11557-016-1205-9