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Candida guilliermondii: biotechnological applications, perspectives for biological control, emerging clinical importance and recent advances in genetics

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Abstract

Candida guilliermondii (teleomorph Meyerozyma guilliermondii) is an ascomycetous species belonging to the Saccharomycotina CTG clade which has been studied over the last 40 years due to its biotechnological interest, biological control potential and clinical importance. Such a wide range of applications in various areas of fundamental and applied scientific research has progressively made C. guilliermondii an attractive model for exploring the potential of yeast metabolic engineering as well as for elucidating new molecular events supporting pathogenicity and antifungal resistance. All these research fields now take advantage of the establishment of a useful molecular toolbox specifically dedicated to C. guilliermondii genetics including the construction of recipient strains, the development of selectable markers and reporter genes and optimization of transformation protocols. This area of study is further supported by the availability of the complete genome sequence of the reference strain ATCC 6260 and the creation of numerous databases dedicated to gene ontology annotation (metabolic pathways, virulence, and morphogenesis). These genetic tools and genomic resources represent essential prerequisites for further successful development of C. guilliermondii research in medical mycology and in biological control by facilitating the identification of the multiple factors that contribute to its pathogenic potential. These genetic and genomic advances should also expedite future practical uses of C. guilliermondii strains of biotechnological interest by opening a window into a better understanding of the biosynthetic pathways of valuable metabolites.

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References

  • Abbas CA, Sibirny AA (2011) Genetic control of biosynthesis and transport of riboflavin and flavin nucleotides and construction of robust biotechnological producers. Microbiol Mol Biol Rev 75:321–360

    Article  PubMed  CAS  Google Scholar 

  • Acourene S, Ammouche A (2012) Optimization of ethanol, citric acid, and alpha-amylase production from date wastes by strains of Saccharomyces cerevisiae, Aspergillus niger, and Candida guilliermondii. J Ind Microbiol Biotechnol 39:759–766

    Article  PubMed  CAS  Google Scholar 

  • Arnaud MB, Costanzo MC, Skrzypek MS, Shah P, Binkley G, Lane C, Miyasato SR, Sherlock G (2007) Sequence resources at the Candida Genome Database. Nucl Acids Res 35:D452–D456

    Article  PubMed  CAS  Google Scholar 

  • Arras G, De Cicco V, Arru S, Lima G (1998) Biocontrol by yeasts of blue mould of citrus fruits and the mode of action of an isolate of Pichia guilliermondii. J Hortic Sci Biotechnol 73:413–418

    Google Scholar 

  • Bai FY (1996) Separation of Candida fermentati comb nov from Candida guilliermondii by DNA base composition and electrophoretic karyotyping. Syst Appl Microbiol 19:178–181

    Article  CAS  Google Scholar 

  • Boeke JD, LaCroute F, Fink GR (1984) A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet 197:345–346

    Article  PubMed  CAS  Google Scholar 

  • Boretsky Y, Voronovsky A, Liuta-Tehlivets O, Hasslacher M, Kohlwein SD, Shavlovsky GM (1999) Identification of an ARS element and development of a high efficiency transformation system for Pichia guilliermondii. Curr Genet 36:215–221

    Article  PubMed  CAS  Google Scholar 

  • Boretsky YR, Kapustyak KY, Fayura LR, Stasyk OV, Stenchuk MM, Bobak YP, Drobot LB, Sibirny AA (2005) Positive selection of mutants defective in transcriptional repression of riboflavin synthesis by iron in the flavinogenic yeast Pichia guilliermondii. FEMS Yeast Res 5:829–837

    Article  PubMed  CAS  Google Scholar 

  • Boretsky YR, Pynyaha YV, Boretsky VY, Kutsyaba VI, Protchenko OV, Philpott CC, Sibirny AA (2007) Development of a transformation system for gene knock-out in the flavinogenic yeast Pichia guilliermondii. J Microbiol Methods 70:13–19

    Google Scholar 

  • Boretsky YR, Pynyaha YV, Boretsky VY, Fedorovych DV, Fayura LR, Protchenko O, Philpott CC, Sibirny AA (2011) Identification of the genes affecting the regulation of riboflavin synthesis in the flavinogenic yeast Pichia guilliermondii using insertion mutagenesis. FEMS Yeast Res 11:307–314

    Article  PubMed  CAS  Google Scholar 

  • Butler G, Rasmussen MD, Lin MF, Santos MA, Sakthikumar S, Munro CA, Rheinbay E, Grabherr M, Forche A, Reedy JL, Agrafioti I, Arnaud MB, Bates S, Brown AJ, Brunke S, Costanzo MC, Fitzpatrick DA, de Groot PW, Harris D, Hoyer LL, Hube B, Klis FM, Kodira C, Lennard N, Logue ME, Martin R, Neiman AM, Nikolaou E, Quail MA, Quinn J, Santos MC, Schmitzberger FF, Sherlock G, Shah P, Silverstein KA, Skrzypek MS, Soll D, Staggs R, Stansfield I, Stumpf MP, Sudbery PE, Srikantha T, Zeng Q, Berman J, Berriman M, Heitman J, Gow NA, Lorenz MC, Birren BW, Kellis M, Cuomo CA (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459:657–662

    Article  PubMed  CAS  Google Scholar 

  • Canettieri EV, Almeida e Silva JB, Felipe MG (2001) Application of factorial design to the study of xylitol production from eucalyptus hemicellulosic hydrolysate. Appl Biochem Biotechnol 94:159–168

    Article  PubMed  CAS  Google Scholar 

  • Carvalho W, Silva SS, Converti A, Vitolo M (2002) Metabolic behavior of immobilized Candida guilliermondii cells during batch xylitol production from sugarcane bagasse acid hydrolyzate. Biotechnol Bioeng 79:165–169

    Article  PubMed  CAS  Google Scholar 

  • Castanheira M, Woosley LN, Diekema DJ, Jones RN, Pfaller MA (2013) Candida guilliermondii and other species of Candida misidentified as Candida famata: assessment by vitek 2, DNA sequencing analysis, and matrix-assisted laser desorption ionization-time of flight mass spectrometry in two global antifungal surveillance programs. J Clin Microbiol 51:117–124

    Article  PubMed  CAS  Google Scholar 

  • Castellani A (1912) Observations on the fungi found in tropical bronchomycosis. Lancet 1:13–15

    Article  Google Scholar 

  • Chanchaichaovivat A, Panijpan B, Ruenwongsa P (2008) Putative modes of action of Pichia guilliermondii strain R13 in controlling chilli anthracnose after harvest. Biol Control 47:207–215

    Article  Google Scholar 

  • Cormack BP, Bertram G, Egerton M, Gow NA, Falkow S, Brown AJ (1997) Yeast-enhanced green fluorescent protein (yEGFP): a reporter of gene expression in Candida albicans. Microbiology 143(Pt 2):303–311

    Article  PubMed  CAS  Google Scholar 

  • Courdavault V, Millerioux Y, Clastre M, Simkin AJ, Marais E, Creche J, Giglioli-Guivarc’h N, Papon N (2011) Fluorescent protein fusions in Candida guilliermondii. Fungal Genet Biol 48:1004–1011

    Article  PubMed  CAS  Google Scholar 

  • Desnos-Ollivier M, Ragon M, Robert V, Raoux D, Gantier JC, Dromer F (2008) Debaryomyces hansenii (Candida famata), a rare human fungal pathogen often misidentified as Pichia guilliermondii (Candida guilliermondii). J Clin Microbiol 46:3237–3242

    Article  PubMed  CAS  Google Scholar 

  • Dias JC, Rezende RP, Rosa CA, Lachance MA, Linardi VR (2000) Enzymatic degradation of nitriles by a Candida guilliermondii UFMG-Y65. Can J Microbiol 46:525–531

    PubMed  CAS  Google Scholar 

  • Diba K, Namaki A, Ayatolahi H, Hanifian H (2012) Rapid identification of drug resistant Candida species causing recurrent vulvovaginal candidiasis. Med Mycol J 53:193–198

    Article  PubMed  CAS  Google Scholar 

  • Diekema D, Arbefeville S, Boyken L, Kroeger J, Pfaller M (2012) The changing epidemiology of healthcare-associated candidemia over three decades. Diagn Microbiol Infect Dis 73:45–48

    Article  PubMed  Google Scholar 

  • Droby S, Hofstein R, Wilson CL, Wisniewski M, Fridlender B, Cohen L, Weiss B, Daus A, Timar D, Chalutz E (1993) Pilot testing of Pichia guilliermondii—a biocontrol agent of postharvest diseases of citrus fruit. Biol Control 3:47–52

    Article  Google Scholar 

  • Droby S, Wisniewski ME, Cohen L, Weiss B, Touitou D, Eilam Y, Chalutz E (1997) Influence of CaCl2 on Penicillium digitatum, grapefruit peel tissue, and biocontrol activity of Pichia guilliermondii. Phytopathology 87:310–315

    Article  PubMed  CAS  Google Scholar 

  • Enary TM (1955) Effect of cobalt and iron on riboflavin by Candida guilliermondii. Acta Chem Scand 9:19–23

    Google Scholar 

  • Enjalbert B, Rachini A, Vediyappan G, Pietrella D, Spaccapelo R, Vecchiarelli A, Brown AJ, d’Enfert C (2009) A multifunctional, synthetic Gaussia princeps luciferase reporter for live imaging of Candida albicans infections. Infect Immun 77:4847–4858

    Article  PubMed  CAS  Google Scholar 

  • Espinel-Ingroff A, Canton E (2011) In vitro activity of echinocandins against non-Candida albicans: is echinocandin antifungal activity the same? Enfermedades Infecciosas y Microbiología Clínica 29(Suppl 2):3–9

    Article  PubMed  Google Scholar 

  • Fan Q, Tian SP, Xu Y, Wang Y, Jiang AL (2000) Biological control of Rhizopus rot of peach fruits by Candida guilliermondii. Acta Botanica Sin 42:1033–1038

    Google Scholar 

  • Fedorovich D, Protchenko O, Lesuisse E (1999) Iron uptake by the yeast Pichia guilliermondii. Flavinogenesis and reductive iron assimilation are co-regulated processes. Biometals 12:295–300

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick DA, Logue ME, Stajich JE, Butler G (2006) A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol 6:26

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick DA, O’Gaora P, Byrne KP, Butler G (2010) Analysis of gene evolution and metabolic pathways using the Candida Gene Order Browser. BMC Genomics 11:290

    Article  PubMed  CAS  Google Scholar 

  • Foureau E, Clastre M, Millerioux Y, Simkin AJ, Cornet L, Dutilleul C, Besseau S, Marais E, Melin C, Guillard J, Creche J, Giglioli-Guivarc’h N, Courdavault V, Papon N (2012a) A TRP5/5-fluoroanthranilic acid counter-selection system for gene disruption in Candida guilliermondii. Curr Genet 58:245–254

    Article  PubMed  CAS  Google Scholar 

  • Foureau E, Courdavault V, Simkin AJ, Pichon O, Creche J, Giglioli-Guivarc’h N, Clastre M, Papon N (2012b) Optimization of the URA-blaster disruption system in Candida guilliermondii: efficient gene targeting using the URA3 marker. J Microbiol Methods 91:117–120

    Article  PubMed  CAS  Google Scholar 

  • Foureau E, Courdavault V, Rojas LF, Dutilleul C, Simkin AJ, Crèche J, Atehortùa L, Giglioli-Guivarc’h N, Clastre M, Papon N (2013a) Efficient gene targeting in a Candida guilliermondii nonhomologous end-joining pathway-deficient strain. Biotechnol Lett. doi:10.1007/s10529-013-1169-7

  • Foureau E, Courdavault V, Simkin AJ, Sibirny AA, Crèche J, Giglioli-Guivarc’h N, Clastre M, Papon N (2013b) Transformation of Candida guilliermondii wild-type strains using the Staphylococcus aureus MRSA 252 ble gene as a phleomycin-resistant marker. FEMS Yeast Res. doi:10.1111/1567-1364.12034

  • Gerami-Nejad M, Berman J, Gale CA (2001) Cassettes for PCR-mediated construction of green, yellow, and cyan fluorescent protein fusions in Candida albicans. Yeast 18:859–864

    Article  PubMed  CAS  Google Scholar 

  • Gerami-Nejad M, Dulmage K, Berman J (2009) Additional cassettes for epitope and fluorescent fusion proteins in Candida albicans. Yeast 26:399–406

    Article  PubMed  CAS  Google Scholar 

  • Gong F, Sheng J, Chi ZM, Li J (2007) Inulinase production by a marine yeast Pichia guilliermondii and inulin hydrolysis by the crude inulinase. J Ind Microbiol Biotechnol 34:179–185

    Article  PubMed  CAS  Google Scholar 

  • Govinden R, Pillay B, van Zyl WH, Pillay D (2001) Xylitol production by recombinant Saccharomyces cerevisiae expressing the Pichia stipitis and Candida shehatae XYL1 genes. Appl Microbiol Biotechnol 55:76–80

    Article  PubMed  CAS  Google Scholar 

  • Guetsky R, Shtienberg D, Elad Y, Fischer E, Dinoor A (2002) Improving biological control by combining biocontrol agents each with several mechanisms of disease suppression. Phytopathology 92:976–985

    Article  PubMed  Google Scholar 

  • Guo C, Zhao C, He P, Lu D, Shen A, Jiang N (2006) Screening and characterization of yeasts for xylitol production. J Appl Microbiol 101:1096–1104

    Article  PubMed  CAS  Google Scholar 

  • Guo N, Gong F, Chi Z, Sheng J, Li J (2009) Enhanced inulinase production in solid state fermentation by a mutant of the marine yeast Pichia guilliermondii using surface response methodology and inulin hydrolysis. J Ind Microbiol Biotechnol 36:499–507

    Article  PubMed  CAS  Google Scholar 

  • Hara A, Ueda M, Misawa S, Matsui T, Furuhashi K, Tanaka A (2000) A mutated hygromycin resistance gene is functional in the n-alkane-assimilating yeast Candida tropicalis. Arch Microbiol 173:187–192

    Article  PubMed  CAS  Google Scholar 

  • Hara A, Arie M, Kanai T, Matsui T, Matsuda H, Furuhashi K, Ueda M, Tanaka A (2001) Novel and convenient methods for Candida tropicalis gene disruption using a mutated hygromycin B resistance gene. Arch Microbiol 176:364–369

    Article  PubMed  CAS  Google Scholar 

  • Hashem M, Alamri S (2009) The biocontrol of postharvest disease (Botryodiplodia theobromae) of guava (Psidium guajava L.) by the application of yeast strains. Postharvest Biol Technol 53:123–130

    Google Scholar 

  • Hashem M, Abo-Elyousr KA (2011) Management of the root-knot nematode Meloidogyne incognita on tomato with combinations of different biocontrol organisms. Crop Prot 30:285–292

    Article  Google Scholar 

  • Hellstrom AM, Vazques-Juarez R, Svanberg U, Andlid TA (2010) Biodiversity and phytase capacity of yeasts isolated from Tanzanian togwa. Int J Food Microbiol 136:352–358

    Article  PubMed  CAS  Google Scholar 

  • Inglis DO, Skrzypek MS, Arnaud MB, Binkley J, Shah P, Wymore F, Sherlock G (2013) Improved gene ontology annotation for biofilm formation, filamentous growth, and phenotypic switching in Candida albicans. Eukaryot Cell 12:101–108

    Article  PubMed  CAS  Google Scholar 

  • Ishchuk OP, Dmytruk KV, Rohulya OV, Voronovsky AY, Abbas CA, Sibirny AA (2008) Development of a promoter assay system for the flavinogenic yeast Candida famata based on the Kluyveromyces lactis β-galactosidase LAC4 reporter gene. Enzym Microb Technol 42:208–215

    Article  CAS  Google Scholar 

  • Ismailov NM (1985) Biodegradation of petroleum hydrocarbons in soil inoculated with yeasts. Mikrobiologiia 54:835–841

    PubMed  CAS  Google Scholar 

  • Jones EW, Berget PB, Burnette JM 3rd, Anderson C, Asafu-Adjei D, Avetisian S, Barrie F, Chen R, Chu B, Conroy S, Conroy S, Dill A, Eimer W, Garrity D, Greenwood A, Hamilton T, Hucko S, Jackson C, Livesey K, Monaco T, Onorato C, Otsuka M, Pai S, Schaeffer G, Shung S, Spath S, Stahlman J, Sweeney B, Wiltrout E, Yurovsky D, Zonneveld A (2008) The spectrum of Trp-mutants isolated as 5-fluoroanthranilate-resistant clones in Saccharomyces bayanus, S. mikatae and S. paradoxus. Yeast 25:41–46

    Article  PubMed  CAS  Google Scholar 

  • Kashchenko VE, Preobrazenskaya EN, Sibirny AA (1991) The method for determination of riboflavin kinase, Soviet Patent

  • Kaszycki P, Fedorovych D, Ksheminska H, Babyak L, Wójcik D, Koloczek H (2004) Chromium accumulation by living yeast at various environmental conditions. Microbiol Res 159:11–17

    Article  PubMed  CAS  Google Scholar 

  • Kawaguchi Y, Honda H, Taniguchi-Morimura J, Iwasaki S (1989) The codon CUG is read as serine in an asporogenic yeast Candida cylindracea. Nature 341:164–166

    Article  PubMed  CAS  Google Scholar 

  • Kegel A, Martinez P, Carter SD, Astrom SU (2006) Genome wide distribution of illegitimate recombination events in Kluyveromyces lactis. Nucl Acids Res 34:1633–1645

    Article  PubMed  CAS  Google Scholar 

  • Keppler-Ross S, Noffz C, Dean N (2008) A new purple fluorescent color marker for genetic studies in Saccharomyces cerevisiae and Candida albicans. Genetics 179:705–710

    Article  PubMed  CAS  Google Scholar 

  • Klinner U, Böttcher F (1984) Hybridization of yeasts by protoplast fusion: ploidy level of hybrids resulting from fusions in haploid strains of Pichia guilliermondii. Zeitschrift für allgemeine Mikrobiologie 24:533–537

    Article  Google Scholar 

  • Knight SA, Lesuisse E, Stearman R, Klausner RD, Dancis A (2002) Reductive iron uptake by Candida albicans: role of copper, iron and the TUP1 regulator. Microbiology 148:29–40

    PubMed  CAS  Google Scholar 

  • Koehler AP, Chu KC, Houang ET, Cheng AF (1999) Simple, reliable, and cost-effective yeast identification scheme for the clinical laboratory. J Clin Microbiol 37:422–426

    PubMed  CAS  Google Scholar 

  • Kooistra R, Hooykaas PJ, Steensma HY (2004) Efficient gene targeting in Kluyveromyces lactis. Yeast 21:781–792

    Article  PubMed  CAS  Google Scholar 

  • Kosa P, Gavenciakova B, Nosek J (2007) Development of a set of plasmid vectors for genetic manipulations of the pathogenic yeast Candida parapsilosis. Gene 396:338–345

    Article  PubMed  CAS  Google Scholar 

  • Kreger-van Rij NJW (1970) Genus 15. Pichia Hansen. In: Lodder J (ed) The yeasts, 2nd edn. North Holland Publishing Co., Amsterdam, pp 455–554

    Google Scholar 

  • Ksheminska H, Jaglarz A, Fedorovych D, Babyak L, Yanovych D, Kaszycki P, Koloczek H (2003) Bioremediation of chromium by the yeast Pichia guilliermondii: toxicity and accumulation of Cr(III) and Cr(VI) and the influence of riboflavin on Cr tolerance. Microbiol Res 158:59–67

    Article  PubMed  CAS  Google Scholar 

  • Kunze G, Petzoldt C, Bode R, Samsonova I, Hecker M, Birnbaum D (1985a) Transformation of Candida maltosa and Pichia guilliermondii by a plasmid containing Saccharomyces cerevisiae ARG4 DNA. Curr Genet 9:205–209

    Article  PubMed  CAS  Google Scholar 

  • Kunze G, Petzoldt C, Bode R, Samsonova IA, Bottcher F, Birnbaum D (1985b) Transformation of the industrially important yeasts Candida maltosa and Pichia guilliermondii. J Basic Microbiol 25:141–144

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kutsiaba VI, Stenchuk NN, Fedorovich DV (2002) Riboflavin overproduction in 4-aminopyrazole[3,4-d]pyrimidine-treated yeast Pichia guilliermondii. Prikl Biokhim Mikrobiol 38:268–272

    PubMed  CAS  Google Scholar 

  • Lahlali R, Hamadi Y, El Guilli M, Jijakli MH (2011) Efficacy assessment of Pichia guilliermondii strain Z1, a new biocontrol agent, against citrus blue mould in Morocco under the influence of temperature and relative humidity. Biol Control 56:217–224

    Article  Google Scholar 

  • Leathers TD (2003) Bioconversions of maize residues to value-added coproducts using yeast-like fungi. FEMS Yeast Res 3:133–140

    Article  PubMed  CAS  Google Scholar 

  • Lee GW, Kim TH, Son JH (2012) Primary Candida guilliermondii Infection of the knee in a patient without predisposing factors. Case Report Med 2012:375682

    Google Scholar 

  • Leuker CE, Hahn AM, Ernst JF (1992) Beta-galactosidase of Kluyveromyces lactis (Lac4p) as reporter of gene expression in Candida albicans and C. tropicalis. Mol Gen Genet 235:235–241

    Article  PubMed  CAS  Google Scholar 

  • Liauta-Teglivets O, Hasslacher M, Boretskii IuR, Kohlwein SD, Shavlovskii GM (1995) Molecular cloning of the GTP-cyclohydrolase structural gene RIB1 of Pichia guilliermondii involved in riboflavin biosynthesis. Yeast 11:945–952

    Article  PubMed  CAS  Google Scholar 

  • Liu FJ, Tu K, Shao XF, Zhao Y, Tu SC, Su J, Hou YP, Zou XR (2010) Effect of hot air treatment in combination with Pichia guilliermondii on postharvest anthracnose rot of loquat fruit. Postharvest Biol Technol 58:65–71

    Article  CAS  Google Scholar 

  • Logvinenko EM, Stasiv IuZ, Zlochevskii ML, Voronovskii A, Beburov M, Shavlovskii GM (1993) Cloning of the RIB7 gene encoding the riboflavin synthase of the yeast Pichia guilliermondii. Genetika 29:922–927

    PubMed  CAS  Google Scholar 

  • Masuda Y, Park SM, Ohkuma M, Ohta A, Takagi M (1994) Expression of an endogenous and a heterologous gene in Candida maltosa by using a promoter of a newly-isolated phosphoglycerate kinase (PGK) gene. Curr Genet 25:412–417

    Article  PubMed  CAS  Google Scholar 

  • McGuire RG (1994) Application of Candida guilliermondii in commercial citrus coatings for biocontrol of Penicillium digitatum on grapefruits. Biol Control 4:1–7

    Article  Google Scholar 

  • Medeiros EA, Lott TJ, Colombo AL, Godoy P, Coutinho AP, Braga MS, Nucci M, Brandt ME (2007) Evidence for a pseudo-outbreak of Candida guilliermondii fungemia in a university hospital in Brazil. J Clin Microbiol 45:942–947

    Article  PubMed  CAS  Google Scholar 

  • Millerioux Y, Clastre M, Simkin AJ, Courdavault V, Marais E, Sibirny AA, Noel T, Creche J, Giglioli-Guivarc’h N, Papon N (2011a) Drug-resistant cassettes for the efficient transformation of Candida guilliermondii wild-type strains. FEMS Yeast Res 11:457–463

    Article  PubMed  CAS  Google Scholar 

  • Millerioux Y, Clastre M, Simkin AJ, Marais E, Sibirny AA, Noel T, Creche J, Giglioli-Guivarc’h N, Papon N (2011b) Development of a URA5 integrative cassette for gene disruption in the Candida guilliermondii ATCC 6260 strain. J Microbiol Methods 84:355–358

    Article  PubMed  CAS  Google Scholar 

  • Morschhauser J, Michel S, Hacker J (1998) Expression of a chromosomally integrated, single-copy GFP gene in Candida albicans, and its use as a reporter of gene regulation. Mol Gen Genet 257:412–420

    Article  PubMed  CAS  Google Scholar 

  • Nantawanit N, Chanchaichaovivat A, Panijpan B, Ruenwongsa P (2010) Induction of defense response against Colletotrichum capsici in chili fruit by the yeast Pichia guilliermondii strain R13. Biol Control 52:145–152

    Article  CAS  Google Scholar 

  • Neistat MA, Alenin VV, Tolstorukov II (1986) Transformation of Hansenula polymorpha, Pichia guilliermondii, Williopsis saturnus yeasts by a plasmid carrying the ADE2 gene of Saccharomyces cerevisiae. Molekuliarnaia Genetika, Mikrobiologiia i Virusologiia:19–23

  • Nguyen HV, Gaillardin C, Neuveglise C (2009) Differentiation of Debaryomyces hansenii and Candida famata by rRNA gene intergenic spacer fingerprinting and reassessment of phylogenetic relationships among D. hansenii, C. famata, D. fabryi, C. flareri (=D. subglobosus) and D. prosopidis: description of D. vietnamensis sp. nov. closely related to D. nepalensis. FEMS Yeast Res 9:641–662

    Article  PubMed  CAS  Google Scholar 

  • Nosek J, Holesova Z, Kosa P, Gacser A, Tomaska L (2009) Biology and genetics of the pathogenic yeast Candida parapsilosis. Curr Genet 55:497–509

    Article  PubMed  CAS  Google Scholar 

  • Ohama T, Suzuki T, Mori M, Osawa S, Ueda T, Watanabe K, Nakase T (1993) Non-universal decoding of the leucine codon CUG in several Candida species. Nucl Acids Res 21:4039–4045

    Article  PubMed  CAS  Google Scholar 

  • Papon N, Courdavault V, Clastre M, Simkin AJ, Creche J, Giglioli-Guivarc’h N (2012) Deus ex Candida genetics: overcoming the hurdles for the development of a molecular toolbox in the CTG clade. Microbiology 158:585–600

    Article  PubMed  CAS  Google Scholar 

  • Paster N, Droby S, Chalutz E, Menasherov M, Nitzan R, Wilson CL (1993) Evaluation of the potential of the yeast Pichia guilliermondii as a biocontrol agent against Aspergillus flavus and fungi of stored soya beans. Mycol Res 97:1201–1206

    Article  Google Scholar 

  • Pepper T, Olinger PM (1988) Xylitol in sugar-free confections. Food Technol 42:98–105

    Google Scholar 

  • Petersson S, Schnurer J (1995) Biocontrol of mold growth in high-moisture wheat stored under airtight conditions by Pichia anomala, Pichia guilliermondii and Saccharomyces cerevisiae. Appl Environ Microbiol 61:1027–1032

    PubMed  CAS  Google Scholar 

  • Pfaller MA, Diekema DJ, Messer SA, Boyken L, Hollis RJ, Jones RN, International Fungal Surveillance Participant G (2003) In vitro activities of voriconazole, posaconazole, and four licensed systemic antifungal agents against Candida species infrequently isolated from blood. J Clin Microbiol 41:78–83

    Article  PubMed  CAS  Google Scholar 

  • Pfaller MA, Diekema DJ, Mendez M, Kibbler C, Erzsebet P, Chang SC, Gibbs DL, Newell VA (2006) Candida guilliermondii, an opportunistic fungal pathogen with decreased susceptibility to fluconazole: geographic and temporal trends from the ARTEMIS DISK antifungal surveillance program. J Clin Microbiol 44:3551–3556

    Article  PubMed  CAS  Google Scholar 

  • Protchenko OV, Boretsky YuR, Romanyuk TM, Fedorovych DV (2000) Oversynthesis of riboflavin by yeast Pichia guilliermondii in response to oxidative stress. Ukrainskiĭ Biokhimicheskiĭ Zhurnal 72:19–23

    PubMed  CAS  Google Scholar 

  • Pynyaha YV, Boretsky YR, Fedorovych DV, Fayura LR, Levkiv AI, Ubiyvovk VM, Protchenko OV, Philpott CC, Sibirny AA (2009) Deficiency in frataxin homologue YFH1 in the yeast Pichia guilliermondii leads to missregulation of iron acquisition and riboflavin biosynthesis and affects sulfate assimilation. Biometals 22:1051–1061

    Article  PubMed  CAS  Google Scholar 

  • Reedy JL, Floyd AM, Heitman J (2009) Mechanistic plasticity of sexual reproduction and meiosis in the Candida pathogenic species complex. Curr Biol 19:891–899

    Article  PubMed  CAS  Google Scholar 

  • Reijnst P, Walther A, Wendland J (2011) Dual-colour fluorescence microscopy using yEmCherry-/GFP-tagging of eisosome components Pil1 and Lsp1 in Candida albicans. Yeast 28:331–338

    Article  PubMed  CAS  Google Scholar 

  • Reuss O, Vik A, Kolter R, Morschhauser J (2004) The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341:119–127

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues RC, Sene L, Matos GS, Roberto IC, Pessoa A Jr, Felipe MG (2006) Enhanced xylitol production by precultivation of Candida guilliermondii cells in sugarcane bagasse hemicellulosic hydrolysate. Curr Microbiol 53:53–59

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez ME, Lopes CA, van Broock M, Valles S, Ramon D, Caballero AC (2004) Screening and typing of Patagonian wine yeasts for glycosidase activities. J Appl Microbiol 96:84–95

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez ME, Lopes CA, Valles S, Caballero AC (2010) Characterization of alpha-rhamnosidase activity from a Patagonian Pichia guilliermondii wine strain. J Appl Microbiol 109:2206–2213

    Article  PubMed  CAS  Google Scholar 

  • Rossignol T, Lechat P, Cuomo C, Zeng Q, Moszer I, d’Enfert C (2008) CandidaDB: a multi-genome database for Candida species and related Saccharomycotina. Nucl Acids Res 36:D557–D561

    Article  PubMed  CAS  Google Scholar 

  • Saligkarias ID, Gravanis FT, Epton HAS (2002) Biological control of Botrytis cinerea on tomato plants by the use of epiphytic yeasts Candida guilliermondii strains 101 and US 7 and Candida oleophila strain I-182: II. A study on mode of action. Biol Control 25:151–161

    Article  CAS  Google Scholar 

  • San Millàn RM, Wu LC, Salkin IF, Lehmann PF (1997) Clinical isolates of Candida guilliermondii include Candida fermentati. Int J Syst Bacteriol 47:385–393

    Article  PubMed  Google Scholar 

  • Savini V, Catavitello C, Di Marzio I, Masciarelli G, Astolfi D, Balbinot A, Bianco A, Pompilio A, Di Bonaventura G, D’Amario C, D’Antonio D (2010) Pan-azole-resistant Candida guilliermondii from a leukemia patient’s silent funguria. Mycopathologia 169:457–459

    Article  PubMed  Google Scholar 

  • Savini V, Catavitello C, Onofrillo D, Masciarelli G, Astolfi D, Balbinot A, Febbo F, D’Amario C, D’Antonio D (2011) What do we know about Candida guilliermondii? A voyage throughout past and current literature about this emerging yeast. Mycoses 54:434–441

    Article  PubMed  Google Scholar 

  • Scherm B, Ortu G, Muzzu A, Budroni M, Arras G, Migheli Q (2003) Biocontrol activity of antagonistic yeasts against Penicillium expansum on apple. J Plant Pathol 85:205–213

    Google Scholar 

  • Schirmer-Michel AC, Flores SH, Hertz PF, Matos GS, Ayub MA (2008) Production of ethanol from soybean hull hydrolysate by osmotolerant Candida guilliermondii NRRL Y-2075. Bioresour Technol 99:2898–2904

    Article  PubMed  CAS  Google Scholar 

  • Schneider J, Blom J, Jaenicke S, Linke B, Brinkrolf K, Neuweger H, Tauch A, Goesmann A (2011) RAPYD—rapid annotation platform for yeast data. J Biotechnol 155:118–126

    Article  PubMed  CAS  Google Scholar 

  • Shavlovskii GM, Fedorovich DV (1977) Investigation of the activity of enzymes participating in the synthesis and hydrolysis of flavin adenine dinucleotide in the yeast Pichia guilliermondii at various levels of flavinogenesis. Microbiology 46:734–740

    Google Scholar 

  • Shavlovskii GM, Kashchenko VE (1975) Determination of riboflavin kinase activity in yeast. Ukrainskiĭ Biokhimicheskiĭ Zhurnal 47:536–541

    CAS  Google Scholar 

  • Shavlovskii GM, Logvinenko EM (1988) Supersynthesis of flavins in microorganisms and its molecular mechanism. Prikl Biokhim Mikrobiol 24:435–447

    PubMed  CAS  Google Scholar 

  • Shavlovskii GM, Logvinenko EM, Sibirnyi AA, Fedorovich DV, Zakalskii AE (1981) Activity of the second step flavinogenesis enzyme 2,5-diamino-6-hydroxy-4-ribosylaminopyrimidine-5′-phosphate reductase in the yeast Pichia guilliermondii. Microbiology 50:752–755

    Google Scholar 

  • Shavlovskii GM, Fedorovich DV, Babyak LY (1993) The effect rib81 mutation on riboflavin biosynthesis and iron transport in Pichia guilliermondii yeast. Microbiology 62:537–540

    Google Scholar 

  • Shavlovsky GM, Sibirny AA (1985) Riboflavin transport in yeasts and its regulation. In: Dawes EA, Tempest DW, Kulaev IS (eds) Environmental regulation of microbial metabolism. Academic Press, London, pp 385–392

    Google Scholar 

  • Shavlovsky GΜ, Zharova VP, Shchelokova IF, Trach VΜ, Sibirny AA, Ksheminskaya GP (1978) Flavinogenic activity of natural strains of the yeast Pichia guilliermondii. Prikl Biokhim Mikrobiol 14:184–189

    Google Scholar 

  • Shavlovsky GM, Babyak LY, Sibirny AA, Logvinenko EM (1985a) Genetic control of riboflavin biosynthesis in Pichia guilliermondii yeasts. The detection of a new regulator gene RIB81. Genetika 21:368–374

    Google Scholar 

  • Shavlovsky GΜ, Fedorovich DV, Logvinenko EΜ, Koltun LV (1985b) The isolation and characteristics of Pichia guilliermondii strains over producing riboflavin and having the regulator mutation rib80 (ribR). Mikrobiologiia 54:919–926

    Google Scholar 

  • Shavlovsky GM, Fedorovich DV, Kutsyaba VI, Babyak LY, Stentchuk NN (1992) Participation of the RIB80 gene in regulation of riboflavin biosynthesis and iron transport in Pichia guilliermondii. Genetika 28:25–32

    Google Scholar 

  • Shchelokova IP, Zharova VP, Kvasnikov EI (1974) Obtaining hybrids of haploid strains of Pichia guilliermondii Wickerham that assimilate petroleum hydrocarbons. Mikrobiologicheskiĭ Zhurnal 36:275–278

    CAS  Google Scholar 

  • Sibirny AA (1986) Genetic control of biosynthesis and transport of riboflavin in the yeast Pichia guilliermondii. PhD report, Leningrad State University

  • Sibirny AA, Boretsky YR (2009) Pichia guilliermondii. In: T. Satyanarayana, Kunze G (ed) Yeast biotechnology: diversity and applications. Springer Science + Business Media B.V., pp 113–134

  • Sibirny AA, Shavlovsky GΜ (1984) Strain Pichia guilliermondii ss16-8 accumulating large amounts of riboflavin inside the cells. Soviet Patent

  • Sibirny AA, Shavlovsky GM, Kshanovskaya BV, Naumov GI (1977) Hybridization and meiotic segregation in the paraffin-utilizing yeast Pichia guilliermondii Wickerham. Genetika 13:314–321

    Google Scholar 

  • Sibirny AA, Shavlovsky GΜ, Kshanovskaya BV, Kutsiaba VI (1982) Intraspecific and interspecific hybridization of yeasts by protoplast fusion. In: Dumka N (ed) Molekularnaya Biologiya. Naukova Dumka, Kiev, pp 16–24

    Google Scholar 

  • Sibirny AA, Trach VΜ, Shavlovsky GΜ (1984) The method for riboflavin sorption from solutions. USSR author’s certificate

  • Sibirnyi AA, Zharova VP, Kshanovskaya BV, Shavlovsky GM (1977a) Selection of genetic line of the yeast Pichia guilliermondii capable of producing a large amount of spores. Tsitologiya i Genetika 11:330–333

    CAS  Google Scholar 

  • Sibirnyi AA, Shavlovskii GM, Ksheminskaya GP, Orlovskaya AG (1977b) Active transport of riboflavin in the yeast Pichia guilliermondii. Detection and some properties of the cryptic riboflavin permease. Biochemistry-Moscow 42:1851–1860

    Google Scholar 

  • Sibirnyi AA, Shavlovskii GM, Ksheminskaya GP, Orlovskaya AG (1977c) Riboflavin transport in cells of riboflavin-dependent yeast mutants. Microbiology 46:313–315

    Google Scholar 

  • Sibirnyi AA, Shavlovskii GM, Ksheminskaya GP, Orlovskaya AG (1978) Effect of glucose and its derivatives on systems of riboflavin uptake and excretion in the yeast Pichia guilliermondii. Biochemistry-Moscow 43:1414–1422

    CAS  Google Scholar 

  • Sibirnyi AA, Shavlovskii GM, Ksheminskaya GP, Orlovskaya AG (1979) Coordinate regulation of riboflavin permease and alpha-glucosidase synthesis in the yeast Pichia guilliermondii. Biochemistry-Moscow 44:1226–1234

    Google Scholar 

  • Skrzypek MS, Arnaud MB, Costanzo MC, Inglis DO, Shah P, Binkley G, Miyasato SR, Sherlock G (2010) New tools at the Candida Genome Database: biochemical pathways and full-text literature search. Nucl Acids Res 38:D428–D432

    Article  PubMed  CAS  Google Scholar 

  • Spadaro D, Gullino ML (2004) State of the art and future prospects of the biological control of postharvest fruit diseases. Int J Food Microbiol 91:185–194

    Article  PubMed  Google Scholar 

  • Stenchuk NN, Kapustiak KE (2003) The red mutations impair the regulation of flavinogenesis and metal homeostas in yeast Pichia guilliermondii. Genetika 39:1026–1032

    PubMed  CAS  Google Scholar 

  • Stenchuk NN, Protchenko OV, Fedorovich DV, Shavlovsky GM (1991) Mutants of Pichia guilliermondii with high reducing activity for riboflavin and iron ions. Genetika 27:561–564

    CAS  Google Scholar 

  • Stenchuk NN, Kutsiaba VI, Kshanovskaia BV, Fedorovich DV (2001) Effect of rib83 mutation on riboflavin biosynthesis and iron assimilation in Pichia guilliermondii. Mikrobiologiia 70:753–758

    PubMed  CAS  Google Scholar 

  • Sugita T, Nakase T (1999) Non-universal usage of the leucine CUG codon and the molecular phylogeny of the genus Candida. Syst Appl Microbiol 22:79–86

    Article  PubMed  CAS  Google Scholar 

  • Sundh I, Melin P (2011) Safety and regulation of yeasts used for biocontrol or biopreservation in the food or feed chain. Antonie Van Leeuwenhoek 99:113–119

    Article  PubMed  Google Scholar 

  • Tanner FW, Vojnovich C, Vanlanen JM (1945) Riboflavin production by Candida species. Science 101:180–181

    Article  PubMed  CAS  Google Scholar 

  • Tian SP, Fan Q, Xu Y, Jiang AL (2002) Effects of calcium on biocontrol activity of yeast antagonists against the postharvest fungal pathogen Rhizopus stolonifer. Plant Pathol 51:352–358

    Article  Google Scholar 

  • Toyn JH, Gunyuzlu PL, White WH, Thompson LA, Hollis GF (2000) A counterselection for the tryptophan pathway in yeast: 5-fluoroanthranilic acid resistance. Yeast 16:553–560

    Article  PubMed  CAS  Google Scholar 

  • Uhl MA, Johnson AD (2001) Development of Streptococcus thermophilus lacZ as a reporter gene for Candida albicans. Microbiology 147:1189–1195

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Vijayaraghavan K, Yamini D, Ambika V, Sowdamini NS (2009) Trends in inulinase production—a review. Crit Rev Biotechnol 29:67–77

    Article  PubMed  CAS  Google Scholar 

  • Wah TT, Walaisri S, Assavanig A, Niamsiri N, Lertsiri S (2013) Co-culturing of Pichia guilliermondii enhanced volatile flavor compound formation by Zygosaccharomyces rouxii in the model system of Thai soy sauce fermentation. Int J Food Microbiol 160:282–289

    Article  PubMed  CAS  Google Scholar 

  • Walker LA, Gow NA, Munro CA (2013) Elevated chitin content reduces the susceptibility of Candida species to caspofungin. Antimicrob Agents Chemother 57:146–154

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Song L, Zhou Y (1992) Selection of strains capable of utilizing d-xylose and cellobiose to produce ethanol by electric field-induced protoplast fusion. Chin J Biotechnol 8:51–56

    PubMed  CAS  Google Scholar 

  • Wang GY, Chi Z, Song B, Wang ZP, Chi ZM (2012) High level lipid production by a novel inulinase-producing yeast Pichia guilliermondii Pcla22. Bioresour Technol 124:77–82

    Article  PubMed  CAS  Google Scholar 

  • Weld RJ, Plummer KM, Carpenter MA, Ridgway HJ (2006) Approaches to functional genomics in filamentous fungi. Cell Res 16:31–44

    Article  PubMed  CAS  Google Scholar 

  • Wickerham LJ (1966) Validation of the species Pichia guilliermondii. J Bacteriol 92:1269

    PubMed  CAS  Google Scholar 

  • Wickerham LJ, Burton KA (1954) A clarification of the relationship of Candida guilliermondii to other yeasts by a study of their mating types. J Bacteriol 68:594–597

    PubMed  CAS  Google Scholar 

  • Wisniewski M, Biles C, Droby S, McLaughlin R, Wilson C, Chalutz E (1991) Mode of action of the postharvest biocontrol yeast, Pichia guilliermondii.1. Characterization of attachment to Botrytis cinerea. Physiol Mol Plant Pathol 39:245–258

    Article  CAS  Google Scholar 

  • Yamamura M, Makimura K, Fujisaki R, Satoh K, Kawakami S, Nishiya H, Ota Y (2009) Polymerase chain reaction assay for specific identification of Candida guilliermondii (Pichia guilliermondii). J Infect Chemother 15:214–218

    Article  PubMed  CAS  Google Scholar 

  • Zahavi T, Cohen L, Weiss B, Schena L, Daus A, Kaplunov T, Zutkhi J, Ben-Arie R, Droby S (2000) Biological control of Botrytis, Aspergillus and Rhizopus rots on table and wine grapes in Israel. Postharvest Biol Technol 20:115–124

    Article  Google Scholar 

  • Zakalsky AE, Zlochevsky ML, Stasiv YZ, Logvinenko EM, Beburov MY, Shavlovsky GM (1990) Cloning of the RIB1 gene coding for the enzyme of the first stage of flavinogenesis in the yeast Pichia guilliermondi, GTP cyclohydrolase, in Escherichia coli cells. Genetika 26:614–620

    CAS  Google Scholar 

  • Zhang DP, Spadaro D, Valente S, Garibaldi A, Gullino ML (2011) Cloning, characterization and expression of an exo-1,3-beta-glucanase gene from the antagonistic yeast, Pichia guilliermondii strain M8 against grey mold on apples. Biol Control 59:284–293

    Article  CAS  Google Scholar 

  • Zhao Y, Tu K, Shao XF, Jing W, Su ZP (2008) Effects of the yeast Pichia guilliermondii against Rhizopus nigricans on tomato fruit. Postharvest Biol Technol 49:113–120

    Article  Google Scholar 

  • Zharova VP, Schelokova IF, Kvasnikov EI (1977) Genetic study of alkane utilization in yeast Pichia guilliermondii Wickerham. 1. Identification of haploid cultures by mating type and obtaining their hybrids. Genetika 13:309–313

    Google Scholar 

  • Zharova VP, Kvasnikov EI, Naumov GI (1980) Production and genetic analysis of Pichia guilliermondii Wicherham mutants that do not assimilate hexadecane. Mikrobiologicheskiĭ Zhurnal 42:167–171

    PubMed  CAS  Google Scholar 

  • Zinjarde SS, Pant AA (2002) Hydrocarbon degraders from tropical marine environments. Mar Pollut Bull 44:118–121

    Article  PubMed  CAS  Google Scholar 

  • Zou YZ, Qi K, Chen X, Miao XL, Zhong JJ (2010) Favorable effect of very low initial K(L)a value on xylitol production from xylose by a self-isolated strain of Pichia guilliermondii. J Biosci Bioeng 109:149–152

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Christophe d’Enfert (Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, Paris, France) and Alexander D. Johnson (University of California, Department of Microbiology & Immunology, San Francisco, USA) for providing gLUC59 and S. thermophiles LacZ, respectively. We acknowledge Françoise Dromer and Marie Desnos-Ollivier (National Reference Center for Mycoses and Antifungals, Institut Pasteur, Paris, France) for providing various C. guilliermondii isolates. We acknowledge the Broad Institute Fungal Genome Initiative for making the complete genome sequence of C. guilliermondii available.

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Authors and Affiliations

  1. EA2106, Biomolécules et Biotechnologies Végétales, Faculté de Pharmacie, Université François-Rabelais de Tours, Tours, France

    Nicolas Papon, Arnaud Lanoue, Joël Crèche & Marc Clastre

  2. Microbiology and Virology, Spirito Santo Hospital, Pescara (PE), Italy

    Vincenzo Savini

  3. School of Biological Sciences, University of Essex, Wivenhoe Park, Colchester, CO34SQ, UK

    Andrew J. Simkin

  4. EA2106, Biomolécules et Biotechnologies Végétales, Faculté des Sciences et Techniques, Université François-Rabelais de Tours, Tours, France

    Nathalie Giglioli-Guivarc’h & Vincent Courdavault

  5. Institute of Cell Biology, NAS of Ukraine, Lviv, Ukraine

    Andriy A. Sibirny

  6. Department of Biotechnology and Microbiology, University of Rzeszow, Rzeszow, Poland

    Andriy A. Sibirny

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  1. Nicolas Papon
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  2. Vincenzo Savini
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Correspondence to Nicolas Papon or Andriy A. Sibirny.

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Communicated by C. Gaillardin.

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Papon, N., Savini, V., Lanoue, A. et al. Candida guilliermondii: biotechnological applications, perspectives for biological control, emerging clinical importance and recent advances in genetics. Curr Genet 59, 73–90 (2013). https://doi.org/10.1007/s00294-013-0391-0

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