Genome sequencing of four Aureobasidium pullulans varieties: biotechnological potential, stress tolerance, and description of new species

BMC Genomics

Nina Gunde-Cimerman¹  Igor V Grigoriev³  Kerrie Barry³  Anna Lipzen³  Chew Yee Ngan³  Jennifer Chiniquy³  Aditi Sharma³  James Han³  Hui Sun³  Martin Grube⁴  Polona Zalar²  Janja Zajc²  Martina Turk²  Silva Sonjak²  Tina Kogej²  Robin A Ohm³  Cene Gostinčar⁵ 

[1] Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins (CIPKeBiP), Jamova 39, Ljubljana SI-1000, Slovenia;Department of Biology, Biotechnical Faculty, University of Ljubljana, Večna pot 111, Ljubljana SI-1000, Slovenia;US Department of Energy Joint Genome Institute, 2800 Michell Drive, Walnut Creek, CA 94598, USA;Institute of Plant Sciences, Karl-Franzens-University Graz, Holteigasse 6, Graz A-8010, Austria;National Institute of Biology, Večna pot 111, Ljubljana SI-1000, Slovenia

关键词: Pullulan;    Opportunistic mycosis;    New species;    Polyextremotolerant;    Halotolerance;    Haloadaptation;    Stress;    Genome;    Dothideomycetes;    Aureobasidium pullulans;   

Others  :  1216541
DOI  :  10.1186/1471-2164-15-549

 received in 2014-03-05, accepted in 2014-06-20,  发布年份 2014

【 摘 要 】

Background

Aureobasidium pullulans is a black-yeast-like fungus used for production of the polysaccharide pullulan and the antimycotic aureobasidin A, and as a biocontrol agent in agriculture. It can cause opportunistic human infections, and it inhabits various extreme environments. To promote the understanding of these traits, we performed de-novo genome sequencing of the four varieties of A. pullulans.

Results

The 25.43-29.62 Mb genomes of these four varieties of A. pullulans encode between 10266 and 11866 predicted proteins. Their genomes encode most of the enzyme families involved in degradation of plant material and many sugar transporters, and they have genes possibly associated with degradation of plastic and aromatic compounds. Proteins believed to be involved in the synthesis of pullulan and siderophores, but not of aureobasidin A, are predicted. Putative stress-tolerance genes include several aquaporins and aquaglyceroporins, large numbers of alkali-metal cation transporters, genes for the synthesis of compatible solutes and melanin, all of the components of the high-osmolarity glycerol pathway, and bacteriorhodopsin-like proteins. All of these genomes contain a homothallic mating-type locus.

Conclusions

The differences between these four varieties of A. pullulans are large enough to justify their redefinition as separate species: A. pullulans, A. melanogenum, A. subglaciale and A. namibiae. The redundancy observed in several gene families can be linked to the nutritional versatility of these species and their particular stress tolerance. The availability of the genome sequences of the four Aureobasidium species should improve their biotechnological exploitation and promote our understanding of their stress-tolerance mechanisms, diverse lifestyles, and pathogenic potential.

【 授权许可】

   
2014 Gostinčar et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Gostinčar C, Grube M, Gunde-Cimerman N: Evolution of fungal pathogens in domestic environments? Fungal Biol 2011, 115:1008-1018.
• [2]Leathers TD: Biotechnological production and applications of pullulan. Appl Microbiol Biotechnol 2003, 62:468-473.
• [3]Cheng KC, Demirci A, Catchmark JM: Pullulan: biosynthesis, production, and applications. Appl Microbiol Biotechnol 2011, 92:29-44.
• [4]Tada R, Tanioka A, Ishibashi K, Adachi Y, Tsubaki K, Ohno N: Involvement of branched units at position 6 in the reactivity of a unique variety of beta-D-glucan from Aureobasidium pullulans to antibodies in human sera. Biosci Biotechnol Biochem 2009, 73:908-911.
• [5]Muramatsu D, Iwai A, Aoki S, Uchiyama H, Kawata K, Nakayama Y, Nikawa Y, Kusano K, Okabe M, Miyazaki T: β-glucan derived from Aureobasidium pullulans is effective for the prevention of influenza in mice. Plos One 2012., 7
• [6]Molnarova J, Vadkertiova R, Stratilova E: Extracellular enzymatic activities and physiological profiles of yeasts colonizing fruit trees. J Basic Microbiol 2013., 53
• [7]Buzzini P, Martini A: Extracellular enzymatic activity profiles in yeast and yeast-like strains isolated from tropical environments. J Appl Microbiol 2002, 93:1020-1025.
• [8]Chi Z, Wang F, Yue L, Liu G, Zhang T: Bioproducts from Aureobasidium pullulans, a biotechnologically important yeast. Appl Microbiol Biotechnol 2009, 82:793-804.
• [9]Rich JO, Leathers TD, Anderson AM, Bischoff KM, Manitchotpisit P: Laccases from Aureobasidium pullulans. Enzyme Microb Technol 2013, 53:33-37.
• [10]Takesako K, Ikai K, Haruna F, Endo M, Shimanaka K, Sono E, Nakamura T, Kato I, Yamaguchi H: Aureobasidins, new antifungal antibiotics taxonomy, fermentation, isolation, and properties. J Antibiot (Tokyo) 1991, 44:919-924.
• [11]Sharma RR, Singh D, Singh R: Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: A review. Biol Control 2009, 50:205-221.
• [12]Price NPJ, Manitchotpisit P, Vermillion KE, Bowman MJ, Leathers TD: Structural characterization of novel extracellular liamocins (mannitol oils) produced by Aureobasidium pullulans strain NRRL 50380. Carbohydr Res 2013, 370:24-32.
• [13]Andrews JH, Spear RN, Nordheim EV: Population biology of Aureobasidium pullulans on apple leaf surfaces. Can J Microbiol 2002, 48:500-513.
• [14]Grube M, Schmid F, Berg G: Black fungi and associated bacterial communities in the phyllosphere of grapevine. Fungal Biol 2011, 115:978-986.
• [15]Olstorpe M, Schnurer J, Passoth V: Microbial changes during storage of moist crimped cereal barley grain under Swedish farm conditions. Anim Feed Sci Technol 2010, 156:37-46.
• [16]Maciel NOP, Pilo FB, Freitas LFD, Gomes FCO, Johann S, Nardi RMD, Lachance MA, Rosa CA: The diversity and antifungal susceptibility of the yeasts isolated from coconut water and reconstituted fruit juices in Brazil. Int J Food Microbiol 2013, 160:201-205.
• [17]Gunde-Cimerman N, Zalar P, de Hoog S, Plemenitaš A: Hypersaline waters in salterns - natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 2000, 32:235-240.
• [18]Oren A, Gunde-Cimerman N: Fungal life in the Dead Sea. In Biology of Marine Fungi Edited by Raghukumar C. 2012.
• [19]Zalar P, Gostinčar C, de Hoog GS, Uršič V, Sudhadham M, Gunde-Cimerman N: Redefinition of Aureobasidium pullulans and its varieties. Stud Mycol 2008, 61:21-38.
• [20]Branda E, Turchetti B, Diolaiuti G, Pecci M, Smiraglia C, Buzzini P: Yeast and yeast-like diversity in the southernmost glacier of Europe (Calderone Glacier, Apennines, Italy). FEMS Microbiol Ecol 2010, 72:354-369.
• [21]Vaz ABM, Rosa LH, Vieira MLA, de Garcia V, Brandao LR, Teixeira LCRS, Moline M, Libkind D, van Broock M, Rosa CA: The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctica. Braz J Microbiol 2011, 42:937-947.
• [22]D'Elia T, Veerapaneni R, Theraisnathan V, Rogers SO: Isolation of fungi from Lake Vostok accretion ice. Mycologia 2009, 101:751-763.
• [23]Vadkertiova R, Slavikova E: Killer activity of yeasts isolated from the water environment. Can J Microbiol 1995, 41:759-766.
• [24]Pitt JI, Hocking AD: Fungi and food spoilage. 2nd edition. Gaithersburg, Maryland: Aspen Publishers, Inc.; 1999.
• [25]Nisiotou AA, Chorianopoulos N, Nychas GJE, Panagou EZ: Yeast heterogeneity during spontaneous fermentation of black Conservolea olives in different brine solutions. J Appl Microbiol 2010, 108:396-405.
• [26]Lotrakul P, Deenarn P, Prasongsuk S, Punnapayak H: Isolation of Aureobasidium pullulans from bathroom surfaces and their antifungal activity against some Aspergilli. Afr J Microbiol Res 2009, 3:253-257.
• [27]Kaarakainen P, Rintala H, Vepsalainen A, Hyvarinen A, Nevalainen A, Meklin T: Microbial content of house dust samples determined with qPCR. Sci Total Environ 2009, 407:4673-4680.
• [28]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.
• [29]Arvanitidou M, Kanellou K, Constantinides TC, Katsouyannopoulos V: The occurrence of fungi in hospital and community potable waters. Lett Apl Microbiol 1999, 29:81-84.
• [30]Zhang ES, Tanaka T, Tajima M, Tsuboi R, Nishikawa A, Sugita T: Characterization of the skin fungal microbiota in patients with atopic dermatitis and in healthy subjects. Microbiol Immunol 2011, 55:625-632.
• [31]Rauch ME, Graef HW, Rozenzhak SM, Jones SE, Bleckmann CA, Kruger RL, Naik RR, Stone MO: Characterization of microbial contamination in United States Air Force aviation fuel tanks. J Ind Microbiol Biotechnol 2006, 33:29-36.
• [32]Cappitelli F, Sorlini C: Microorganisms attack synthetic polymers in items representing our cultural heritage. Appl Environ Microbiol 2008, 74:564-569.
• [33]Shah AA, Hasan F, Hameed A, Ahmed S: Biological degradation of plastics: a comprehensive review. Biotechnol Adv 2008, 26:246-265.
• [34]Hawkes M, Rennie R, Sand C, Vaudry W: Aureobasidium pullulans infection: fungemia in an infant and a review of human cases. Diagn Microbiol Infect Dis 2005, 51:209-213.
• [35]Chan GF, Puad MSA, Chin CF, Rashid NAA: Emergence of Aureobasidium pullulans as human fungal pathogen and molecular assay for future medical diagnosis. Folia Microbiol (Praha) 2011, 56:459-467.
• [36]Chan GF, Bamadhaj HM, Gan HM, Rashid NAA: Genome sequence of Aureobasidium pullulans AY4, an emerging opportunistic fungal pathogen with diverse biotechnological potential. Eukaryot Cell 2012, 11:1419-1420.
• [37]Gostinčar C, Grube M, de Hoog GS, Zalar P, Gunde-Cimerman N: Extremotolerance in fungi: evolution on the edge. FEMS Microbiol Ecol 2010, 71:2-11.
• [38]Ranta HM: Effect of simulated acid rain on quantity of epiphytic microfungi on Scots pine (Pinus sylvestris L.) needles. Environ Pollut 1990, 67:349-359.
• [39]Shiomi N, Yasuda T, Inoue Y, Kusumoto N, Iwasaki S, Katsuda T, Katoh S: Characteristics of neutralization of acids by newly isolated fungal cells. J Biosci Bioeng 2004, 97:54-58.
• [40]Onofri S: Antarctic Microfungi. In Enigmatic microorganisms and life in extreme environments. Edited by Seckbach J. Dordrecht; London: Kluwer Academic; 1999:323-336. Cellular origin and life in extreme habitats; v.1
• [41]Kogej T, Ramos J, Plemenitas A, Gunde-Cimerman N: The halophilic fungus Hortaea werneckii and the halotolerant fungus Aureobasidium pullulans maintain low intracellular cation concentrations in hypersaline environments. Appl Environ Microbiol 2005, 71:6600-6605.
• [42]Managbanag JR, Torzilli AP: An analysis of trehalose, glycerol, and mannitol accumulation during heat and salt stress in a salt marsh isolate of Aureobasidium pullulans. Mycologia 2002, 94:384-391.
• [43]Kogej T, Gostinčar C, Volkmann M, Gorbushina AA, Gunde-Cimerman N: Mycosporines in extremophilic fungi — novel complementary osmolytes? Environ Chem 2006, 3:105-110.
• [44]Turk M, Mejanelle L, Šentjurc M, Grimalt JO, Gunde-Cimerman N, Plemenitaš A: Salt-induced changes in lipid composition and membrane fluidity of halophilic yeast-like melanized fungi. Extremophiles 2004, 8:53-61.
• [45]Gostinčar C, Turk M, Trbuha T, Vaupotič T, Plemenitaš A, Gunde-Cimerman N: Expression of fatty-acid-modifying enzymes in the halotolerant black yeast Aureobasidium pullulans (de Bary) G. Arnaud under salt stress. Stud Mycol 2008, 61:51-59.
• [46]Bermejo JM, Dominguez JB, Goni FM, Uruburu F: Influence of pH on the transition from yeast-like cells to chlamydospores in Aureobasidium pullulans. Antonie Van Leeuwenhoek 1981, 47:385-392.
• [47]Crous PW, Summerell BA, Swart L, Denman S, Taylor JE, Bezuidenhout CM, Palm ME, Marincowitz S, Groenewald JZ: Fungal pathogens of Proteaceae. Persoonia 2011, 27:20-45.
• [48]Peterson SW, Manitchotpisit P, Leathers TD: Aureobasidium thailandense sp. nov. isolated from leaves and wooden surfaces. Int J Syst Evol Microbiol 2013, 63:790-795.
• [49]Manitchotpisit P, Leathers TD, Peterson SW, Kurtzman CP, Li XL, Eveleigh DE, Lotrakul P, Prasongsuk S, Dunlap CA, Vermillion KE, Punnapayak H: Multilocus phylogenetic analyses, pullulan production and xylanase activity of tropical isolates of Aureobasidium pullulans. Mycol Res 2009, 113:1107-1120.
• [50]Slepecky RA, Starmer WT: Phenotypic plasticity in fungi: a review with observations on Aureobasidium pullulans. Mycologia 2009, 101:823-832.
• [51]Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA, Barry KW, Condon BJ, Copeland AC, Dhillon B, Glaser F, Hesse CN, Kosti I, Labutti K, Lindquist EA, Lucas S, Salamov AA, Bradshaw RE, Ciuffetti L, Hamelin RC, Kema GH, Lawrence C, Scott JA, Spatafora JW, Turgeon BG, de Wit PJ, Zhong S, Goodwin SB, Grigoriev IV: Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog 2012, 8:e1003037.
• [52]Gerstein AC, Chun HJE, Grant A, Otto SP: Genomic convergence toward diploidy in Saccharomyces cerevisiae. PLoS Genet 2006, 2:1396-1401.
• [53]Dhar R, Sagesser R, Weikert C, Yuan J, Wagner A: Adaptation of Saccharomyces cerevisiae to saline stress through laboratory evolution. J Evol Biol 2011, 24:1135-1153.
• [54]Lenassi M, Gostinčar C, Jackman S, Turk M, Sadowski I, Nislow C, Jones S, Birol I, Gunde-Cimerman N, Plemenitaš A: Whole genome duplication and enrichment of metal cation transporters revealed by de novo genome sequencing of extremely halotolerant black yeast Hortaea werneckii. PLoS ONE 2013, 8:e71328.
• [55]Duan XH, Chi ZM, Wang L, Wang XH: Influence of different sugars on pullulan production and activities of alpha-phosphoglucose mutase, UDPG-pyrophosphorylase and glucosyltransferase involved in pullulan synthesis in Aureobasidium pullulans Y68. Carbohydr Polym 2008, 73:587-593.
• [56]Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B: The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 2014, 42:D490-D495.
• [57]Kang BK, Yang HJ, Choi NS, Ahn KH, Park CS, Yoon BD, Kim MS: Production of pure beta-glucan by Aureobasidium pullulans after pullulan synthetase gene disruption. Biotechnol Lett 2010, 32:137-142.
• [58]Zhang DP, Spadaro D, Valente S, Garibaldi A, Gullino ML: Cloning, characterization, expression and antifungal activity of an alkaline serine protease of Aureobasidium pullulans PL5 involved in the biological control of postharvest pathogens. Int J Food Microbiol 2012, 153:453-464.
• [59]Chi Z, Wang XX, Ma ZC, Buzdar MA, Chi ZM: The unique role of siderophore in marine-derived Aureobasidium pullulans HN6.2. Biometals 2012, 25:219-230.
• [60]Takesako K, Kuroda H, Inoue T, Haruna F, Yoshikawa Y, Kato I, Uchida K, Hiratani T, Yamaguchi H: Biological properties of aureobasidin A, a cyclic depsipeptide antifungal antibiotic. J Antibiot (Tokyo) 1993, 46:1414-1420.
• [61]Slightom JL, Metzger BP, Luu HT, Elhammer AP: Cloning and molecular characterization of the gene encoding the aureobasidin A biosynthesis complex in Aureobasidium pullulans BP-1938. Gene 2009, 431:67-79.
• [62]Wang WL, Chi ZM, Chi Z, Li J, Wang XH: Siderophore production by the marine-derived Aureobasidium pullulans and its antimicrobial activity. Bioresour Technol 2009, 100:2639-2641.
• [63]Johnson L: Iron and siderophores in fungal-host interactions. Mycol Res 2008, 112:170-183.
• [64]Brakhage AA: Regulation of fungal secondary metabolism. Nat Rev Microbiol 2013, 11:21-32.
• [65]Scharf DH, Brakhage AA: Engineering fungal secondary metabolism: A roadmap to novel compounds. J Biotechnol 2013, 163:179-183.
• [66]Medema MH, Blin K, Cimermancic P, de Jager V, Zakrzewski P, Fischbach MA, Weber T, Takano E, Breitling R: antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 2011, 39:339-346.
• [67]Zhong XY, Tian YQ, Niu GQ, Tan HR: Assembly and features of secondary metabolite biosynthetic gene clusters in Streptomyces ansochromogenes. Sci China Life Sci 2013, 56:609-618.
• [68]Knerr PJ, van der Donk WA: Discovery, biosynthesis, and engineering of lantipeptides. Annu Rev Biochem 2012, 81:479-505.
• [69]Choi J, Park J, Kim D, Jung K, Kang S, Lee YH: Fungal Secretome Database: Integrated platform for annotation of fungal secretomes. BMC Genomics 2010., 11
• [70]Zhao ZT, Liu HQ, Wang CF, Xu JR: Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 2013., 14
• [71]Han MV, Thomas GWC, Lugo-Martinez J, Hahn MW: Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3. Mol Biol Evol 2013, 30:1987-1997.
• [72]Rawlings ND, Barrett AJ, Bateman A: MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 2012, 40:D343-D350.
• [73]Belmares R, Contreras-Esquivel JC, Rodriguez-Herrera R, Coronel AR, Aguilar CN: Microbial production of tannase: an enzyme with potential use in food industry. Lebensm Wiss Technol 2004, 37:857-864.
• [74]Isola D, Selbmann L, de Hoog GS, Fenice M, Onofri S, Prenafeta-Boldu FX, Zucconi L: Isolation and screening of black fungi as degraders of volatile aromatic hydrocarbons. Mycopathologia 2013, 175:369-379.
• [75]Prenafeta-Boldu FX, Guivernau M, Gallastegui G, Vinas M, de Hoog GS, Elias A: Fungal/bacterial interactions during the biodegradation of TEX hydrocarbons (toluene, ethylbenzene and p-xylene) in gas biofilters operated under xerophilic conditions. FEMS Microbiol Ecol 2012, 80:722-734.
• [76]Webb JS, Nixon M, Eastwood IM, Greenhalgh M, Robson GD, Handley PS: Fungal colonization and biodeterioration of plasticized polyvinyl chloride. Appl Environ Microbiol 2000, 66:3194-3200.
• [77]Howard GT: Biodegradation of polyurethane: a review. Int Biodeterior Biodegradation 2002, 49:245-252.
• [78]Shivakumar S: Poly-beta-hydroxybutyrate (PHB) Depolymerase from Fusarium solani Thom. J Chem 2013.
• [79]Reddy VS, Shlykov MA, Castillo R, Sun EI, Saier MH: The major facilitator superfamily (MFS) revisited. FEBS J 2012, 279:2022-2035.
• [80]Saier MH, Tran CV, Barabote RD: TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res 2006, 34:D181-D186.
• [81]Saier MH: Families of transmembrane sugar transport proteins. Mol Microbiol 2000, 35:699-710.
• [82]Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S, Rehman B, Elkins T, Engels R, Wang S, Nielsen CB, Butler J, Endrizzi M, Qui D, Ianakiev P, Bell-Pedersen D, Nelson MA, Werner-Washburne M, Selitrennikoff CP, Kinsey JA, Braun EL, Zelter A, Schulte U, Kothe GO, Jedd G, Mewes W, et al.: The genome sequence of the filamentous fungus Neurospora crassa. Nature 2003, 422:859-868.
• [83]Leandro MJ, Fonseca C, Goncalves P: Hexose and pentose transport in ascomycetous yeasts: an overview. FEMS Yeast Res 2009, 9:511-525.
• [84]Hohmann S: Control of high osmolarity signalling in the yeast Saccharomyces cerevisiae. FEBS Lett 2009, 583:4025-4029.
• [85]Bahn YS: Master and commander in fungal pathogens: the two-component system and the HOG signaling pathway. Eukaryot Cell 2008, 7:2017-2036.
• [86]Krantz M, Becit E, Hohmann S: Comparative genomics of the HOG-signalling system in fungi. Curr Genet 2006, 49:137-151.
• [87]Musacchio A, Gibson T, Rice P, Thompson J, Saraste M: The PH Domain - a common piece in the structural patchwork of signaling proteins. Trends Biochem Sci 1993, 18:343-348.
• [88]Gostinčar C, Muggia L, Grube M: Polyextremotolerant black fungi: oligotrophism, adaptive potential, and a link to lichen symbioses. Front Microbiol 2012, 3:390.
• [89]Robinson CH: Cold adaptation in Arctic and Antarctic fungi. New Phytol 2001, 151:341-353.
• [90]Ansell R, Granath K, Hohmann S, Thevelein JM, Adler L: The two isoenzymes for yeast NAD(+)-dependent glycerol-3-phosphate dehydrogenase encoded by GPD1 and GPD2 have distinct roles in osmoadaptation and redox regulation. EMBO J 1997, 16:2179-2187.
• [91]Zajc J, Liu Y, Dai W, Yang Z, Hu J, Gostinčar C, Gunde-Cimerman N: Genome and transcriptome sequencing of the halophilic fungus Wallemia ichthyophaga: haloadaptations present and absent. BMC Genomics 2013, 14:617.
• [92]Lenassi M, Zajc J, Gostinčar C, Gorjan A, Gunde-Cimerman N, Plemenitaš A: Adaptation of the glycerol-3-phosphate dehydrogenase Gpd1 to high salinities in the extremely halotolerant Hortaea werneckii and halophilic Wallemia ichthyophaga. Fungal Biol 2011, 115:959-970.
• [93]Jung S, Marelli M, Rachubinski RA, Goodlett DR, Aitchison JD: Dynamic changes in the subcellular distribution of Gpd1p in response to cell stress. J Biol Chem 2010, 285:6739-6749.
• [94]Francois J, Parrou JL: Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 2001, 25:125-145.
• [95]Ruijter GJG, Bax M, Patel H, Flitter SJ, van de Vondervoort PJI, de Vries RP, van Kuyk PA, Visser J: Mannitol is required for stress tolerance in Aspergillus niger conidiospores. Eukaryot Cell 2003, 2:690-698.
• [96]Silva SS, Felipe MGA, Mancilha IM: Factors that affect the biosynthesis of xylitol by xylose-fermenting yeasts - A review. Appl Biochem Biotechnol 1998, 70–72:331-339.
• [97]Granstrom TB, Izumori K, Leisola M: A rare sugar xylitol. Part I: the biochemistry and biosynthesis of xylitol. Appl Microbiol Biotechnol 2007, 74:277-281.
• [98]Sugai JK, Veiga LA: Purification and properties of the xylitol dehydrogenase from Pullularia pullulans. An Acad Bras Cienc 1981, 53:183-193.
• [99]Siehr DJ: Melanin biosynthesis in Aureobasidium pullulans. J Coating Tech 1981, 53:23-25.
• [100]Bell AA, Wheeler MH: Biosynthesis and functions of fungal melanins. Annu Rev Phytopathol 1986, 24:411-451.
• [101]Kogej T, Stein M, Volkmann M, Gorbushina AA, Galinski EA, Gunde-Cimerman N: Osmotic adaptation of the halophilic fungus Hortaea werneckii: role of osmolytes and melanization. Microbiol 2007, 153:4261-4273.
• [102]Butler MJ, Day AW: Fungal melanins: a review. Can J Microbiol 1998, 44:1115-1136.
• [103]Taborda CP, da Silva MB, Nosanchuk JD, Travassos LR: Melanin as a virulence factor of Paracoccidioides brasiliensis and other dimorphic pathogenic fungi: a minireview. Mycopathologia 2008, 165:331-339.
• [104]Yurlova NA, de Hoog GS, Fedorova LG: The influence of ortho- and para-diphenoloxidase substrates on pigment formation in black yeast-like fungi. Stud Mycol 2008, 39-49.
• [105]Kogej T, Wheeler MH, Lanisnik Rizner T, Gunde-Cimerman N: Evidence for 1,8-dihydroxynaphthalene melanin in three halophilic black yeasts grown under saline and non-saline conditions. FEMS Microbiol Lett 2004, 232:203-209.
• [106]Langfelder K, Streibel M, Jahn B, Haase G, Brakhage AA: Biosynthesis of fungal melanins and their importance for human pathogenic fungi. Fungal Genet Biol 2003, 38:143-158.
• [107]Takano Y, Kubo Y, Kawamura C, Tsuge T, Furusawa I: The Alternaria alternata melanin biosynthesis gene restores appressorial melanization and penetration of cellulose membranes in the melanin-deficient albino mutant of Colletotrichum lagenarium. Fungal Genet Biol 1997, 21:131-140.
• [108]Takano Y, Kubo Y, Shimizu K, Mise K, Okuno T, Furusawa I: Structural analysis of Pks1, a polyketide synthase gene involved in melanin biosynthesis in Colletotrichum lagenarium. Mol Gen Genet 1995, 249:162-167.
• [109]Zhang A, Lu P, Dahl-Roshak AM, Paress PS, Kennedy S, Tkacz JS, An Z: Efficient disruption of a polyketide synthase gene (pks1) required for melanin synthesis through Agrobacterium-mediated transformation of Glarea lozoyeasis. Mol Genet Genomics 2003, 268:645-655.
• [110]Tsai HF, Wheeler MH, Chang YC, Kwon-Chung KJ: A developmentally regulated gene cluster involved in conidial pigment biosynthesis in Aspergillus fumigatus. J Bacteriol 1999, 181:6469-6477.
• [111]Borgnia MJ, Agre P: Reconstitution and functional comparison of purified GlpF and AqpZ, the glycerol and water channels from Escherichia coli. Proc Natl Acad Sci USA 2001, 98:2888-2893.
• [112]Alleva K, Chara O, Amodeo G: Aquaporins: Another piece in the osmotic puzzle. FEBS Lett 2012, 586:2991-2999.
• [113]Borgnia M, Nielsen S, Engel A, Agre P: Cellular and molecular biology of the aquaporin water channels. Annu Rev Biochem 1999, 68:425-458.
• [114]Hohmann S, Bill RM, Kayingo G, Prior BA: Microbial MIP channels. Trends Microbiol 2000, 8:33-38.
• [115]Pettersson N, Filipsson C, Becit E, Brive L, Hohmann S: Aquaporins in yeasts and filamentous fungi. Biol Cell 2005, 97:487-500.
• [116]Xu H, Cooke JEK, Zwiazek JJ: Phylogenetic analysis of fungal aquaporins provides insight into their possible role in water transport of mycorrhizal associations. Botany-Botanique 2013, 91:495-504.
• [117]Arino J, Ramos J, Sychrova H: Alkali metal cation transport and homeostasis in yeasts. Microbiol Mol Biol Rev 2010, 74:95-120.
• [118]Shabala S, Cuin TA: Potassium transport and plant salt tolerance. Physiol Plant 2008, 133:651-669.
• [119]Ko CH, Gaber RF: Trk1 and Trk2 encode structurally related K+ transporters in Saccharomyces cerevisiae. Mol Cell Biol 1991, 11:4266-4273.
• [120]Ketchum KA, Joiner WJ, Sellers AJ, Kaczmarek LK, Goldstein SA: A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem. Nature 1995, 376:690-695.
• [121]Haro R, Garciadeblas B, Rodriguez-Navarro A: A novel P-type ATPase from yeast involved in sodium-transport. FEBS Lett 1991, 291:189-191.
• [122]Garciadeblas B, Rubio F, Quintero FJ, Banuelos MA, Haro R, Rodriguez-Navarro A: Differential expression of two genes encoding isoforms of the ATPase involved in sodium efflux in Saccharomyces cerevisiae. Mol Gen Genet 1993, 236:363-368.
• [123]Wieland J, Nitsche AM, Strayle J, Steiner H, Rudolph HK: The PMR2 gene-cluster encodes functionally distinct isoforms of a putative Na+ pump in the yeast plasma-membrane. EMBO J 1995, 14:3870-3882.
• [124]Ramos J, Arino J, Sychrova H: Alkali-metal-cation influx and efflux systems in nonconventional yeast species. FEMS Microbiol Lett 2011, 317:1-8.
• [125]Serrano R, Kiellandbrandt MC, Fink GR: Yeast plasma-membrane ATPase is essential for growth and has homology with (Na++K+), K+- and Ca2+-ATPases. Nature 1986, 319:689-693.
• [126]Ambesi A, Miranda M, Petrov VV, Slayman CW: Biogenesis and function of the yeast plasma-membrane H+-ATPase. J Exp Biol 2000, 203:155-160.
• [127]Waschuk SA, Bezerra AG, Shi L, Brown LS: Leptosphaeria rhodopsin: Bacteriorhodopsin-like proton pump from a eukaryote. Proc Natl Acad Sci USA 2005, 102:6879-6883.
• [128]Gostinčar C, Lenassi M, Gunde-Cimerman N, Plemenitaš A: Fungal adaptation to extremely high salt concentrations. Adv Appl Microbiol 2011, 77:71-96.
• [129]Wagner NL, Greco JA, Ranaghan MJ, Birge RR: Directed evolution of bacteriorhodopsin for applications in bioelectronics. J R Soc Interface 2013., 10
• [130]Zhang F, Vierock J, Yizhar O, Fenno LE, Tsunoda S, Kianianmomeni A, Prigge M, Berndt A, Cushman J, Polle J, Magnuson J, Hegemann P, Deisseroth K: The microbial opsin family of optogenetic tools. Cell 2011, 147:1446-1457.
• [131]Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Bolchacova E, Voigt K, Crous PW, Miller AN, Wingfield MJ, Aime MC, An KD, Bai FY, Barreto RW, Begerow D, Bergeron MJ, Blackwell M, Boekhout T, Bogale M, Boonyuen N, Burgaz AR, Buyck B, Cai L, Cai Q, Cardinali G, Chaverri P, Coppins BJ, Crespo A, et al.: Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA 2012, 109:6241-6246.
• [132]Manitchotpisit P, Skory CD, Peterson SW, Price NPJ, Vermillion KE, Leathers TD: Poly(beta-L-malic acid) production by diverse phylogenetic clades of Aureobasidium pullulans. J Ind Microbiol Biotechnol 2012, 39:125-132.
• [133]Spatafora JW, Sung GH, Johnson D, Hesse C, O'Rourke B, Serdani M, Spotts R, Lutzoni F, Hofstetter V, Miadlikowska J, Reeb V, Gueidan C, Fraker E, Lumbsch T, Lucking R, Schmitt I, Hosaka K, Aptroot A, Roux C, Miller AN, Geiser DM, Hafellner J, Hestmark G, Arnold AE, Budel B, Rauhut A, Hewitt D, Untereiner WA, Cole MS, Scheidegger C, et al.: A five-gene phylogeny of Pezizomycotina. Mycologia 2006, 98:1018-1028.
• [134]Liu YJ, Hall BD: Body plan evolution of ascomycetes, as inferred from an RNA polymerase II, phylogeny. Proc Natl Acad Sci USA 2004, 101:4507-4512.
• [135]Schmitt I, Crespo A, Divakar PK, Fankhauser JD, Herman-Sackett E, Kalb K, Nelsen MP, Nelson NA, Rivas-Plata E, Shimp AD, Widhelm T, Lumbsch HT: New primers for promising single-copy genes in fungal phylogenetics and systematics. Persoonia 2009, 23:35-40.
• [136]de Hoog GS, Guarro J, Gene J, Figueras MJ: Atlas of clinical fungi. 2nd edition. Utrecht: ASM Press; 2000.
• [137]Debuchy R, Turgeon BG: Mating-type structure, evolution, and function in Euascomycetes. In The Mycota: A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research: Growth, Differentiation and Sexuality, Volume 1. Edited by Kües U, Fischer R. Berlin, Heidelberg: Springer; 2006:293-323.
• [138]Ni M, Feretzaki M, Sun S, Wang XY, Heitman J: Sex in Fungi. Annu Rev Genet 2011, 45:405-430.
• [139]Butler G, Kenny C, Fagan A, Kurischko C, Gaillardin C, Wolfe KH: Evolution of the MAT locus and its Ho endonuclease in yeast species. Proc Natl Acad Sci USA 2004, 101:1632-1637.
• [140]Malik SB, Pightling AW, Stefaniak LM, Schurko AM, Logsdon JM: An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis. Plos One 2008., 3
• [141]Nakagawa T, Kolodner RD: Saccharomyces cerevisiae Mer3 is a DNA helicase involved in meiotic crossing over. Mol Cell Biol 2002, 22:3281-3291.
• [142]Gioti A, Nystedt B, Li WJ, Xu J, Andersson A, Averette AF, Munch K, Wang XY, Kappauf C, Kingsbury JM, Kraak B, Walker LA, Johansson HJ, Holm T, Lehtio J, Stajich JE, Mieczkowski P, Kahmann R, Kennell JC, Cardenas ME, Lundeberg J, Saunders CW, Boekhout T, Dawson TL, Munro CA, de Groot PWJ, Butler G, Heitman J, Scheynius A: Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis. Mbio 2013., 4
• [143]Srikantha T, Daniels KJ, Pujol C, Sahni N, Yi S, Soll DR: Nonsex genes in the mating type locus of Candida albicans play roles in a/alpha biofilm formation, including impermeability and fluconazole resistance. PLoS Pathog 2012., 8
• [144]Rozman D, Komel R: Isolation of genomic DNA from filamentous fungi with high glucan level. BioTechniques 1994, 16:382-383.
• [145]Gnerre S, MacCallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, Sharpe T, Hall G, Shea TP, Sykes S, Berlin AM, Aird D, Costello M, Daza R, Williams L, Nicol R, Gnirke A, Nusbaum C, Lander ES, Jaffe DB: High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci USA 2011, 108:1513-1518.
• [146]Zerbino DR, Birney E: Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008, 18:821-829.
• [147]Martin J, Bruno VM, Fang ZD, Meng XD, Blow M, Zhang T, Sherlock G, Snyder M, Wang Z: Rnnotator: an automated de novo transcriptome assembly pipeline from stranded RNA-Seq reads. BMC Genomics 2010., 11
• [148]Kent WJ: BLAT - The BLAST-like alignment tool. Genome Res 2002, 12:656-664.
• [149]Grigoriev I, Martines D, Salamov A: Fungal genomic annotation. In Applied mycology and biotechnology, Volume 6. Edited by Aurora D, Berka R, Singh G. Amsterdam London: Elsevier; 2006:123-142.
• [150]Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R, Otillar R, Riley R, Salamov A, Zhao X, Korzeniewski F, Smirnova T, Nordberg H, Dubchak I, Shabalov I: MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res 2014, 42:D699-D704.
• [151]RepeatMasker Open-3.0 http://www.repeatmasker.org webcite
• [152]Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J: Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 2005, 110:462-467.
• [153]Price AL, Jones NC, Pevzner PA: De novo identification of repeat families in large genomes. Bioinformatics 2005, 21:I351-I358.
• [154]Salamov AA, Solovyev VV: Ab initio gene finding in Drosophila genomic DNA. Genome Res 2000, 10:516-522.
• [155]Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M: Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res 2008, 18:1979-1990.
• [156]Birney E, Clamp M, Durbin R: GeneWise and Genomewise. Genome Res 2004, 14:988-995.
• [157]Altschul SF, Madden TL, Shaffer AA, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
• [158]Lowe TM, Eddy SR: tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25:955-964.
• [159]Nielsen H, Engelbrecht J, Brunak S, von Heijne G: Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 1997, 10:1-6.
• [160]Melen K, Krogh A, von Heijne G: Reliability measures for membrane protein topology prediction algorithms. J Mol Biol 2003, 327:735-744.
• [161]Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R: InterProScan: Protein domains identifier. Nucleic Acids Res 2005, 33:W116-W120.
• [162]Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y: KEGG for linking genomes to life and the environment. Nucleic Acids Res 2008, 36:D480-D484.
• [163]Koonin EV, Fedorova ND, Jackson JD, Jacobs AR, Krylov DM, Makarova KS, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Rogozin IB, Smirnov S, Sorokin AV, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA: A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes. Genome Biol 2004., 5
• [164]Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G, Consortium GO: Gene Ontology: tool for the unification of biology. Nat Genet 2000, 25:25-29.
• [165]Enright AJ, Van Dongen S, Ouzounis CA: An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002, 30:1575-1584.
• [166]Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, Kuo A, Minovitsky S, Nikitin R, Ohm RA, Otillar R, Poliakov A, Ratnere I, Riley R, Smirnova T, Rokhsar D, Dubchak I: The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 2012, 40:26-32.
• [167]Merlini L, Dudin O, Martin SG: Mate and fuse: how yeast cells do it. Open Biology 2013., 3
• [168]Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8:785-786.
• [169]Emanuelsson O, Nielsen H, Brunak S, von Heijne G: Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 2000, 300:1005-1016.
• [170]Krogh A, Larsson B, von Heijne G, Sonnhammer ELL: Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol 2001, 305:567-580.
• [171]Yu CS, Lin CJ, Hwang JK: Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci 2004, 13:1402-1406.
• [172]Chi SM, Nam D: WegoLoc: accurate prediction of protein subcellular localization using weighted Gene Ontology terms. Bioinformatics 2012, 28:1028-1030.
• [173]Park BH, Karpinets TV, Syed MH, MR L u, Uberbacher EC: CAZymes Analysis Toolkit (CAT): Web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. Glycobiology 2010, 20:1574-1584.
• [174]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [175]Robbertse B, Yoder RJ, Boyd A, Reeves J, Spatafora JW: Hal: an automated pipeline for phylogenetic analyses of genomic data. PLoS Currents 2011, 3:RRN1213.
• [176]de Wit PJGM, van der Burgt A, Okmen B, Stergiopoulos I, Abd-Elsalam KA, Aerts AL, Bahkali AH, Beenen HG, Chettri P, Cox MP, Datema E, de Vries RP, Dhillon B, Ganley AR, Griffiths SA, Guo YA, Hamelin RC, Henrissat B, Kabir MS, Jashni MK, Kema G, Klaubauf S, Lapidus A, Levasseur A, Lindquist E, Mehrabi R, Ohm RA, Owen TJ, Salamov A, Schwelm A: The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genet 2012., 8
• [177]Goodwin SB, Ben M'Barek S, Dhillon B, Wittenberg AHJ, Crane CF, Hane JK, Foster AJ, Van der Lee TAJ, Grimwood J, Aerts A, Antoniw J, Bailey A, Bluhm B, Bowler J, Bristow J, van der Burgt A, Canto-Canche B, Churchill ACL, Conde-Ferraez L, Cools HJ, Coutinho PM, Csukai M, Dehal P, De Wit P, Donzelli B, van de Geest HC, Van Ham RCHJ, Hammond-Kosack KE, Henrissat B, Kilian A, et al.: Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet 2011., 7
• [178]Amselem J, Cuomo CA, van Kan JAL, Viaud M, Benito EP, Couloux A, Coutinho PM, de Vries RP, Dyer PS, Fillinger S, Fournier E, Gout L, Hahn M, Kohn L, Lapalu N, Plummer KM, Pradier JM, Quevillon E, Sharon A, Simon A, ten Have A, Tudzynski B, Tudzynski P, Wincker P, Andrew M, Anthouard V, Beever RE, Beffa R, Benoit I, Bouzid O, et al.: Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 2011., 7
• [179]Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R, Porcel B, Rubini A, Amicucci A, Amselem J, Anthouard V, Arcioni S, Artiguenave F, Aury JM, Ballario P, Bolchi A, Brenna A, Brun A, Buee M, Cantarel B, Chevalier G, Couloux A, Da Silva C, Denoeud F, Duplessis S, Ghignone S, et al.: Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 2010, 464:1033-1038.
• [180]Arnaud MB, Chibucos MC, Costanzo MC, Crabtree J, Inglis DO, Lotia A, Orvis J, Shah P, Skrzypek MS, Binkley G, Miyasato SR, Wortman JR, Sherlock G: The Aspergillus Genome Database, a curated comparative genomics resource for gene, protein and sequence information for the Aspergillus research community. Nucleic Acids Res 2010, 38:420-427.
• [181]Talavera G, Castresana J: Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007, 56:564-577.
• [182]Darriba D, Taboada GL, Doallo R, Posada D: ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011, 27:1164-1165.
• [183]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol 2010, 59:307-321.
• [184]Sanderson MJ: r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 2003, 19:301-302.
• [185]Katoh K, Toh H: Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 2008, 9:286-298.
• [186]Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL: Versatile and open software for comparing large genomes. Genome Biol 2004., 5
• [187]Hane JK, Rouxel T, Howlett BJ, Kema GHJ, Goodwin SB, Oliver RP: A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol 2011., 12
• [188]Gremme G, Steinbiss S, Kurtz S: GenomeTools: A comprehensive software library for efficient processing of structured genome annotations. IEEE/ACM Trans Comput Biol Bioinform 2013, 10:645-656.
• [189]Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Finn RD: The Pfam protein families database. Nucleic Acids Res 2012, 40:290-301.
• [190]Blin K, Medema MH, Kazempour D, Fischbach MA, Breitling R, Takano E, Weber T: antiSMASH 2.0-a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res 2013, 41:204-212.