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Yarrowia porcina sp. nov. and Yarrowia bubula f.a. sp. nov., two yeast species from meat and river sediment

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Abstract

Eleven yeast strains representing two hitherto undescribed species were isolated from different kinds of meat samples in Hungary and one from the sediment of a tropical freshwater river in Southeastern Brazil. The analysis of the sequences of their large subunit rRNA gene D1/D2 domain and the internal transcribed spacer (ITS) regions placed the two new species in the Yarrowia clade. Some of the seven strains representing the first new species can mate and give rise to asci and form ascospores embedded in capsular material, which qualifies it as the third teleomorph species of the Yarrowia clade. The name Yarrowia porcina sp. nov. (type strain: NCAIM Y.02100T = CBS 12935T = NRRL Y-63669T, allotype strain UFMG-RD131A = CBS 12932A) is proposed for this new yeast species, which, based on physiological characters, is indistinguishable from Yarrowia lipolytica and some other species of the genus. Considerable intraspecific variability was detected among the sequences of the large subunit rRNA gene D1/D2 domains of the seven strains. The variability among the D1/D2 sequences exceeded the divergence observed among the ITS sequences and in some cases more than 1 % substitution among the D1/D2 sequences was detected. The conspecificity of these strains was supported by the low (0–3 substitutions) sequence divergence among their ITS sequences, the result of a parsimony network analysis utilizing the concatenated ITS and D1/D2 sequences and also by the fingerprint patterns generated by microsatellite primed PCR. No ascospore formation was observed in the group of the other five strains representing the second new species. These strains shared identical D1/D2 and ITS sequences. Yarrowia bubula f.a., sp. nov. (type strain: NCAIM Y.01998T = CBS 12934T = NRRL Y-63668T) is proposed to accommodate these strains.

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References

  • Atlas RM (1993) In: Parks LC (ed) Handbook of microbiological media. CRC Press, Boca Raton, p 968

    Google Scholar 

  • Chang C-F, Chen C-C, Lee C-F, Liu S-M (2013) Identifying and characterizing Yarrowia keelungensis sp. nov., an oil-degrading yeast isolated from the sea surface microlayer. Antonie van Leeuwenhoek. doi:10.1007/s10482-013-0033-z

    Google Scholar 

  • Chen Y-C, Eisner JD, Kattar MM, Rassoulian-Barrett SL, LaFe K, Yarfitz SL, Limaye AP, Cookson BT (2000) Identification of medically important yeasts using PCR-based detection of DNA sequence polymorphisms in the internal transcribed spacer 2 region of the rRNA genes. J Clin Microbiol 38:2302–2310

    CAS  PubMed Central  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Coelho MAZ, Amaral PFF, Belo I (2010) Yarrowia lipolytica: an industrial workhorse. In: Méndes-Vilas A (ed) Current research, technology and education topics in applied microbiology and microbial biotechnology. Formatex Research Center, Badajoz, pp 930–944

    Google Scholar 

  • Daniel H-M, Vrancken G, Takrama JF, Camu N, De Vos P, De Vuyst L (2009) Yeast diversity of Ghanaian cocoa bean heap fermentations. FEMS Yeast Res 9:774–783

    Article  CAS  PubMed  Google Scholar 

  • de Barros Lopes M, Soden A, Martens AL, Henschke PA, Langridge P (1998) Differentiation and species identification on yeasts using PCR. Int J Syst Bacteriol 48:279–286

    Article  PubMed  Google Scholar 

  • Deák T (2008) Detection and enumeration. Handbook of food spoilage yeasts, 2nd edn. CRC Press, Boca Raton, pp 203–220

    Google Scholar 

  • Encinas JP, López-Díaz TM, García-López ML, Otero A, Moreno B (2000) Yeast populations on Spanish fermented sausages. Meat Sci 54:203–208

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Ferreira AD, Viljoen BC (2003) Yeasts as adjunct starters in matured cheddar cheese. Int J Food Microbiol 86:131–140

    Article  CAS  PubMed  Google Scholar 

  • Fonseca Á, Scorzetti G, Fell JW (2000) Diversity in the yeast Cryptococcus albidus and related species as revealed by ribosomal DNA sequence analysis. Can J Microbiol 46:7–27

    Article  CAS  PubMed  Google Scholar 

  • Groenewald M, Smith MTh (2013) The teleomorph state of Candida deformans Langeron and Guerra and description of Yarrowia yakushimensis comb. nov. Antonie Van Leeuwenhoek 103:1023–1028

    Article  CAS  PubMed  Google Scholar 

  • Groenewald M, Boekhout T, Neuvéglise C, Gaillardin C, van Dijck PWM, Wyss M (2013) Yarrowia lipolytica: safety assessment of an oleaginous yeast with a great industrial potential. Crit Rev Microbiol. doi:10.3109/1040841X.2013.770386

    PubMed  Google Scholar 

  • Hart MW, Sunday J (2007) Things fall apart: biological species form unconnected parsimony networks. Biol Lett 3:509–512

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ismail SAS, Deák T, Abd El-Rahman HA, Yassien MA, Beuchat LR (2000) Presence and changes in populations of yeasts on raw and processed poultry products stored at refrigeration temperature. Int J Food Microbiol 62:113–121

    Article  CAS  PubMed  Google Scholar 

  • Knutsen AK, Robert V, Poot GA, Epping W, Figge M, Holst-Jensen A, Skaar I, Smith MTh (2007) Polyphasic re-examination of Yarrowia lipolytica strains and the description of three novel Candida species: Candida oslonensis sp. nov., Candida alimentaria sp. nov. and Candida hollandica sp. nov. Int J Syst Evol Microbiol 57:2426–2435

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kurtzman CP, Fell JW, Boekhout T, Robert V (2011) Methods for isolation, phenotypic characterization and maintenance of yeasts. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, Amsterdam, pp 97–107

    Google Scholar 

  • Lachance MA (2012) In defense of yeast sexual life cycles: the forma asexualis: An informal proposal. Yeast Newsl 61:24–25

    Google Scholar 

  • Lachance MA, Bowles JM, Starmer WT, Barker JSF (1999) Kodamaea kakaduensis and Candida tolerans, two new ascomycetous yeast species from Australian Hibiscus flowers. Can J Microbiol 45:172–177

    Article  CAS  PubMed  Google Scholar 

  • Lachance MA, Daniel HM, Meyer W, Prasad GS, Gautam SP, Boundy-Mills K (2003) The D1/D2 domain of the large-subunit rDNA of the yeast species Clavispora lusitaniae is unusually polymorphic. FEMS Yeast Res 4:253–258

    Article  CAS  PubMed  Google Scholar 

  • Lachance MA, Dobson J, Wijayanayaka DN, Smith AM (2010) The use of parsimony network analysis for the formal delineation of phylogenetic species of yeasts: Candida apicola, Candida azyma, and Candida parazyma sp. nov., cosmopolitan yeasts associated with floricolous insects. Antonie Van Leeuwenhoek 97:155–170

    Article  CAS  PubMed  Google Scholar 

  • Lachance MA, Wijayanayaka TM, Bundus JD, Wijayanayaka DN (2011) Ribosomal DNA sequence polymorphism and the delineation of two ascosporic yeast species: Metschnikowia agaves and Starmerella bombicola. FEMS Yeast Res 11:324–333

    Article  CAS  PubMed  Google Scholar 

  • Mayoral MB, Martin R, Sanz A, Hernández PE, González I, Garcia T (2005) Detection of Kluyveromyces marxianus and other spoilage yeasts in yoghurt using a PCR-culture technique. Int J Food Microbiol 105:27–34

    Article  CAS  PubMed  Google Scholar 

  • McIlvaine TC (1921) A buffer solution for colorimetric comparison. J Biol Chem 49:183–186

    CAS  Google Scholar 

  • Mcneill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J, Prud’homme Van Reine WF, Smith GF, Wiersema JH, Turland NJ (2012) International code of nomenclature for algae, fungi, and plants (Melbourne Code). Koeltz scientific books. http://www.iapt-taxon.org/nomen/main.php. Accessed 15 Sept 2013

  • Medeiros AO, Kohler LM, Hamdan JS, Missagia BS, Barbosa FAR, Rosa CA (2008) Diversity and antifungal susceptibility of yeasts from tropical freshwater environments in Southeastern Brazil. Water Res 42:3921–3929

    Article  CAS  PubMed  Google Scholar 

  • Mirbagheri M, Nahvi I, Emtiazi G, Mafakher L, Darvishi F (2012) Taxonomic characterization and potential biotechnological applications of Yarrowia lipolytica isolated from meat and its products. Jundishapur J Microbiol 5:346–351

    Google Scholar 

  • Nagy E, Niss M, Dlauchy D, Arneborg N, Nielsen DS, Péter G (2013) Yarrowia divulgata f.a., sp. nov., a yeast species from animal related and marine sources. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.057208-0

    PubMed  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Patrignani F, Iucci L, Vallicelli M, Guerzoni ME, Gardini F, Lanciotti R (2007) Role of surfaceinoculated Debaryomyces hansenii and Yarrowia lipolytica strains in dried fermented sausage manufacture. Part 1: evaluation of their effects on microbial evolution, lipolytic and proteolytic patterns. Meat Sci 75:676–686

    Article  CAS  PubMed  Google Scholar 

  • Péter G, Tornai-Lehoczki J, Dlauchy D (2009) Candida ogatae sp. nov., an anamorphic member of the Kuraishia clade. FEMS Yeast Res 9:328–333

    Article  PubMed  Google Scholar 

  • Pincus DH, Salkin IF, Hurd NJ, Levy IL, Kemna MA (1988) Modification of potassium nitrate assimilation test for identification of clinically important yeasts. J Clin Microbiol 26:366–368

    CAS  PubMed Central  PubMed  Google Scholar 

  • Samson RA, Hoekstra ES, Frisvad JC (eds) (2004) Introduction to food- and airborne fungi, 7th edn. Centraalbureau voor Schimmelcultures, Utrecht

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vasdinyei R, Deák T (2003) Characterization of yeast isolates originating from Hungarian dairy products using traditional and molecular identification techniques. Int J Food Microbiol 86:123–130

    Article  CAS  PubMed  Google Scholar 

  • Wickerham LJ, Kurtzman CP, Herman AI (1970) Sexuality in Candida lipolytica. In: Ahearn DG (ed) Recent trends in yeast research, vol 1. Georgia State University, Atlanta, pp 81–92

    Google Scholar 

  • Wyder MT, Bachmann HP, Puhan Z (1999) Role of selected yeasts in cheese ripening: an evaluation in foil wrapped raclette cheese. Lebensm Wiss Technol 32:333–343

    Article  CAS  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was partly supported by the State Secretariat for Higher Education, Hungarian Ministry of Human Resources and the Doctoral School of Food Sciences, Corvinus University of Budapest. This work was also funded by the Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq – Brazil), Fundação do Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG), the Financiadora de Estudos e Projetos (FINEP, Brazil, process number 2084/07).

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Authors and Affiliations

  1. National Collection of Agricultural and Industrial Microorganisms, Faculty of Food Science, Corvinus University of Budapest, Somlói út 14-16, Budapest, 1118, Hungary

    Edina Nagy, Dénes Dlauchy & Gábor Péter

  2. Departamento de Botânica, Instituto de Biologia, Campus Universitário de Ondina, Universidade Federal da Bahia, Salvador, Bahia, 40170-115, Brazil

    Adriana O. Medeiros

  3. Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Avenida Antônio Carlos 6627, Belo Horizonte, Minas Gerais, 31270-901, Brazil

    Carlos A. Rosa

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  1. Edina Nagy
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  2. Dénes Dlauchy
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  3. Adriana O. Medeiros
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  4. Gábor Péter
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Correspondence to Gábor Péter.

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Nagy, E., Dlauchy, D., Medeiros, A.O. et al. Yarrowia porcina sp. nov. and Yarrowia bubula f.a. sp. nov., two yeast species from meat and river sediment. Antonie van Leeuwenhoek 105, 697–707 (2014). https://doi.org/10.1007/s10482-014-0125-4

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