Skip to main content
SpringerLink
Log in

Wickerhamomyces anomalus in the sourdough microbial ecosystem

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

We previously found that Wickerhamomyces anomalus (formerly Hansenula anomala, Pichia anomala) was the second most frequently isolated yeast in Belgian artisan bakery sourdoughs and that the yeast dominated laboratory sourdough fermentations. Such findings are of interest in terms of the advantage of W. anomalus over other commonly encountered sourdough yeasts and its potential introduction into the sourdough ecosystem. Here, we provide a brief overview of current knowledge on yeast ecology and diversity in sourdough in the context of the potential natural habitat of W. anomalus. Insight into the population structure of W. anomalus was obtained by comparing internal transcribed spacer rDNA sequences of selected sourdough isolates with publicly available database sequences.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bjönberg A, Schnürer J (1993) Inhibition of the growth of grain-storage moulds in vitro by the yeast Pichia anomala (Hansen) Kurtzman. Can J Microbiol 39:623–628

    Article  Google Scholar 

  • Burmeister HR, Hartman PA (1966) Yeasts in ensiled high-moisture corn. Appl Microbiol 14:35–38

    CAS  PubMed  Google Scholar 

  • Castelli T (1933) Su alcune Hansenule della fermentazione panaria. Arch Microbiol 4:514–529

    Google Scholar 

  • Chakrabarti A, Singh K, Narang A, Singhi S, Batra R, Rao KLM, Ray P, Gopalan S, Das S, Gupta V, Gupta AK, Bose SM, McNeil MM (2001) Outbreak of Pichia anomala infection in the pediatric service of a tertiary-care center in Northern India. J Clin Microbiol 39:1702–1706

    Article  CAS  PubMed  Google Scholar 

  • Christensen JE, Dudley EG, Pederson JR, Steele JL (1999) Peptidases and amino acid catabolism in lactic acid bacteria. Antonie van Leeuwenhoek J Microbiol 76:217–246

    Article  CAS  PubMed  Google Scholar 

  • Coda R, Nionelli L, Rizzello CG, De Angelis M, Tossut P, Gobbetti M (2010) Spelt and emmer flours: characterization of the lactic acid bacteria microbiota and selection of mixed starters for bread making. J Appl Microbiol 108:925–935

    Article  CAS  PubMed  Google Scholar 

  • Corsetti A, Lavermicocca P, Morea M, Baruzzi F, Tosti N, Gobbetti M (2001) Phenotypic and molecular identification and clustering of lactic acid bacteria and yeasts from wheat (species Triticum durum and Triticum aestivum) sourdoughs of southern Italy. Int J Food Microbiol 64:95–104

    Article  CAS  PubMed  Google Scholar 

  • Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescence theory with applications to intraspecific phylogeny reconstruction. Genetics 134:959–969

    CAS  PubMed  Google Scholar 

  • da Matta VLR, de Souza Carvalho Melhem M, Colombo AL, Moretti ML, Rodero L, de Almeida GMD, dos Anjos Martins M, Costa SF, Souza Dias MBG, Nucci M, Levin AS (2001) Antifungal drug susceptibility profile of Pichia anomala isolates from patients presenting with nosocomial fungemia. Antimicrob Agents Chemother 51:1573–1576

    Article  Google Scholar 

  • De Vuyst L, Neysens P (2005) The sourdough microflora: biodiversity and metabolic interactions. Trends Food Sci Technol 16:43–56

    Article  Google Scholar 

  • De Vuyst L, Vancanneyt M (2007) Biodiversity and identification of sourdough lactic acid bacteria. Food Microbiol 24:120–127

    Article  PubMed  Google Scholar 

  • De Vuyst L, Vrancken G, Ravyts F, Rimaux T, Weckx S (2009) Biodiversity, ecological determinants, and metabolic exploitation of sourdough microbiota. Food Microbiol 26:666–675

    Article  PubMed  Google Scholar 

  • Falkow S (1997) What is a pathogen? ASM News 63:359–365

    Google Scholar 

  • Fernández M, Zúñiga M (2006) Amino acid catabolic pathways of lactic acid bacteria. Crit Rev Microbiol 32:155–183

    Article  PubMed  Google Scholar 

  • Foschino R, Galli A (1997) Italian style of life: pane, amore e… lievito naturale!. Tecnol Aliment 1:42–59

    Google Scholar 

  • Foschino R, Gallina S, Andrighetto C, Rossetti L, Galli A (2004) Comparison of cultural methods for the identification and molecular investigation of yeasts from sourdoughs for Italian sweet baked products. FEMS Yeast Res 4:609–618

    Article  CAS  PubMed  Google Scholar 

  • Fredlund E, Druvefors U, Boysen ME, Lingsten KH, Schnürer J (2002) Physiological characteristics of the biocontrol yeast Pichia anomala J121. FEMS Yeast Res 2:395–402

    CAS  PubMed  Google Scholar 

  • Gänzle MG, Vermeulen N, Vogel RF (2007) Carbohydrate, peptide and lipid metabolism of lactic acid bacteria in sourdough. Food Microbiol 24:128–138

    Article  PubMed  Google Scholar 

  • Gänzle MG, Zhang C, Monang B-S, Lee V, Schwab C (2009) Novel metabolites from cereal-associated lactobacilli—novel functionalities for cereal products? Food Microbiol 26:712–719

    Article  PubMed  Google Scholar 

  • Gobbetti M (1998) The sourdough microflora: interactions of lactic acid bacteria and yeasts. Trends Food Sci Technol 9:267–274

    Article  CAS  Google Scholar 

  • Gobbetti M, Corsetti A, Rossi J (1994) The sourdough microflora—interactions between lactic acid bacteria and yeasts—metabolism of carbohydrates. Appl Microbiol Biotechnol 41:456–460

    Article  CAS  Google Scholar 

  • Gullo M, Romano AD, Pulvirenti A, Giudici P (2003) Candida humilis—dominant species in sourdoughs for the production of durum wheat bran flour bread. Int J Food Microbiol 80:55–59

    Article  CAS  PubMed  Google Scholar 

  • Iacumin L, Cecchini F, Manzano M, Osualdini M, Boscolo D, Orlic S, Comi G (2009) Description of the microflora of sourdoughs by culture-dependent and culture-independent methods. Food Microbiol 26:128–135

    Article  CAS  PubMed  Google Scholar 

  • Infantes M, Schmidt JL (1992) Characterisation of the yeast flora of natural sourdough located in various French areas. Sci Aliment 12:271–287

    Google Scholar 

  • Infantes M, Tourneur C (1991) Survey on the lactic flora of natural sourdoughs located in various French areas. Sci Aliment 11:527–545

    Google Scholar 

  • Kalenic S, Jandrlic M, Vegar V, Zuech N, Sekulic A, Mlinaric-Missoni E (2001) Hansenula anomala outbreak at a surgical intensive care unit: a search for risk factors. Eur J Epidemiol 17:491–496

    Article  CAS  PubMed  Google Scholar 

  • Kurtzman CP (1998) Pichia E.C. Hansen emend. Kurtzman. In: Kurtzman CP, Fell JW (eds) The yeasts: a taxonomic study, 4th edn. Elsevier, Amsterdam, The Netherlands, pp 273–352

    Chapter  Google Scholar 

  • Kurtzman CP, Wickerham LJ, Hesseltine CW (1970) Yeasts from wheat and flour. Mycologia 62:542–547

    Article  CAS  PubMed  Google Scholar 

  • Kurtzman CP, Robnett CJ, Basehoar-Powers E (2008) Phylogenetic relationships among species of Pichia, Issatchenkia and Williopsis determined from multigene sequence analysis, and the proposal of Barnettozyma gen. nov., Lindnera gen. nov. and Wickerhamomyces gen. nov. FEMS Yeast Res 8:939–954

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Meroth CB, Hammes WP, Hertel C (2003a) Identification and population dynamics of yeasts in sourdough fermentation processes by PCR-denaturing gradient gel electrophoresis. Appl Environ Microbiol 69:7453–7461

    Article  CAS  PubMed  Google Scholar 

  • Meroth CB, Walter J, Hertel C, Brandt MJ, Hammes WP (2003b) Monitoring the bacterial population dynamics in sourdough fermentation processes by using PCR-denaturing gradient gel electrophoresis. Appl Environ Microbiol 69:475–482

    Article  CAS  PubMed  Google Scholar 

  • Murphy N, Damjanovic V, Hart CA, Buchanan CR, Whitaker R, Cooke RWI (1986) Infection and colonization of neonates by Hansenula anomala. Lancet 327:291–293

    Article  Google Scholar 

  • Osimani A, Zannini E, Aquilanti L, Mannazzu I, Comitini F, Clementi F (2009) Lactic acid bacteria and yeasts from wheat sourdoughs of the Marche region. Ital J Food Sci 21:269–286

    CAS  Google Scholar 

  • Piarroux R, Millon L, Bardonnet K, Vagner O, Koenig H (1999) Are live Saccharomyces yeasts harmful to patients? Lancet 353:1851–1852

    Article  CAS  PubMed  Google Scholar 

  • Polonelli L, Archibusacci C, Sestito M, Morace G (1983) Killer system: a simple method for differentiating Candida albicans strains. J Clin Microbiol 17:774–780

    CAS  PubMed  Google Scholar 

  • Pulvirenti A, Caggia C, Restuccia C, Gullo M, Giudici P (2001) DNA fingerprinting methods used for identification of yeasts isolated from Sicilian sourdoughs. Ann Microbiol 51:107–120

    CAS  Google Scholar 

  • Pulvirenti A, Solieri L, Gullo M, De Vero L, Giudici P (2004) Occurrence and dominance of yeast species in sourdough. Lett Appl Microbiol 38:113–117

    Article  CAS  PubMed  Google Scholar 

  • Reyes E, Barahona S, Fischman O, Niklitschek M, Baeza M, Cifuentes V (2004) Genetic polymorphism of clinical and environmental strains of Pichia anomala. Biol Res 37(Suppl A):747–757

    CAS  PubMed  Google Scholar 

  • Rocha JM, Malcata FX (1999) On the microbiological profile of traditional Portuguese sourdough. J Food Prot 62:1416–1429

    CAS  PubMed  Google Scholar 

  • Rossi J (1996) The yeasts in sourdough. Adv Food Sci 18:201–211

    CAS  Google Scholar 

  • Salovaara H, Savolainen J (1984) Yeast type isolated from Finnish sour rye dough starters. Acta Aliment Pol 10:241–246

    Google Scholar 

  • Scheirlinck I, Van der Meulen R, Van Schoor A, Vancanneyt M, De Vuyst L, Vandamme P, Huys G (2007) Influence of geographical origin and flour type on diversity of lactic acid bacteria in traditional Belgian sourdoughs. Appl Environ Microbiol 73:6262–6269

    Article  CAS  PubMed  Google Scholar 

  • Scheirlinck I, Van der Meulen R, Van Schoor A, Vancanneyt M, De Vuyst L, Vandamme P, Huys G (2008) Taxonomic structure and stability of the bacterial community in Belgian sourdough ecosystems as assessed by culture and population fingerprinting. Appl Environ Microbiol 74:2414–2423

    Article  CAS  PubMed  Google Scholar 

  • Sekhon AS, Kowalewska-Grochowska K, Garg AK, Vaudry W (1992) Hansenula anomala fungemia in an infant with gastric and cardiac complications with a review of the literature. Eur J Epidemiol 8:305–308

    CAS  PubMed  Google Scholar 

  • Sterr Y, Weiss A, Schmidt H (2009) Evaluation of lactic acid bacteria for sourdough fermentation of amaranth. Int J Food Microbiol 136:75–82

    Article  CAS  PubMed  Google Scholar 

  • Succi M, Reale A, Andrighetto C, Lombardi A, Sorrentino E, Coppola R (2003) Presence of yeasts in southern Italian sourdoughs from Triticum aestivum flour. FEMS Microbiol Lett 225:143–148

    Article  CAS  PubMed  Google Scholar 

  • Sugihara TF, Kline L, Miller MW (1971) Microorganisms of the San Francisco sour dough bread process. Appl Microbiol 21:456–458

    CAS  PubMed  Google Scholar 

  • Sutar R, David JK, Ganesan K, Ghosh AK, Singhi S, Chakrabarti A, Bachhawat AK (2004) Comparison of ITS and IGS1 regions for strain typing of clinical and non-clinical isolates of Pichia anomala. J Med Microbiol 53:1–5

    Article  Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III Cladogram estimation. Genetics 132:619–633

    CAS  PubMed  Google Scholar 

  • Teunisson DJ (1954) Yeasts from freshly combined rough rice stored in a sealed bin. Appl Microbiol 2:215–220

    CAS  PubMed  Google Scholar 

  • Valmorri S, Tofalo R, Settanni L, Corsetti A, Suzzi G (2010) Yeast microbiota associated with spontaneous sourdough fermentations in the production of traditional wheat sourdough breads of the Abruzzo region (Italy). Antonie van Leeuwenhoek J Microbiol 97:119–129

    Article  CAS  PubMed  Google Scholar 

  • Van der Meulen R, Scheirlinck I, Van Schoor A, Huys G, Vancanneyt M, Vandamme P, De Vuyst L (2007) Population dynamics and metabolite target analysis of lactic acid bacteria during laboratory fermentations of wheat and spelt sourdoughs. Appl Environ Microbiol 73:4741–4750

    Article  PubMed  Google Scholar 

  • Vernocchi P, Valmorri S, Gatto V, Torriani S, Gianotti A, Suzzi G, Guerzoni ME, Gardini F (2004) A survey on yeast microbiota associated with an Italian traditional wheat-leavened baked good fermentation. Food Res Int 37:469–476

    Article  CAS  Google Scholar 

  • Vrancken G, De Vuyst L, Van der Meulen R, Huys G, Vandamme P, Daniel HM (2010) Yeast species composition differs between artisan bakery and spontaneous laboratory sourdoughs. FEMS Yeast Res 10:471–481

    Article  CAS  PubMed  Google Scholar 

  • Zannini E, Garofalo C, Aquilanti L, Santarelli S, Silvestri G, Clementi F (2009) Microbiological and technological characterization of sourdoughs destined for bread-making with barley flour. Food Microbiol 26:744–753

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to acknowledge their financial support from the Research Council of the Vrije Universiteit Brussel (OZR, GOA, and IOF projects), the Fund for Scientific Research—Flanders, the Institute for the Promotion of Innovation through Science and Technology in Flanders, in particular the SBO project “New Strategy for the Development of Functional and Performance Starter Cultures for Foods in Function of ‘Food Qualitomics’ ”, and the Federal Research Policy (contract BCCM C3/10/003), in particular the project of the Action for the Promotion of and Cooperation with the Belgian Coordinated Collections of Microorganisms.

Author information

Authors and Affiliations

  1. Mycothèque de l’Université catholique de Louvain (MUCL), Member of the Belgian Coordinated Collection of Microorganisms (BCCM), Earth and Life Institute, Applied Microbiology, Mycology, Université Catholique de Louvain, Croix du Sud 3, bte 6, 1348, Louvain-la-Neuve, Belgium

    Heide-Marie Daniel, Marie-Chantal Moons & Stéphanie Huret

  2. Research Group of Industrial Microbiology and Food Biotechnology, Faculty of Sciences and Bioengineering Sciences, Vrije Universiteit Brussel, Pleinlaan 2, 1050, Brussels, Belgium

    Gino Vrancken & Luc De Vuyst

Authors
  1. Heide-Marie Daniel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie-Chantal Moons
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stéphanie Huret
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gino Vrancken
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luc De Vuyst
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Heide-Marie Daniel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Daniel, HM., Moons, MC., Huret, S. et al. Wickerhamomyces anomalus in the sourdough microbial ecosystem. Antonie van Leeuwenhoek 99, 63–73 (2011). https://doi.org/10.1007/s10482-010-9517-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-010-9517-2

Keywords

Search

Navigation