Abstract
Pichia anomala is a most interesting yeast species, from a number of environmental, industrial and medical aspects. This yeast has been isolated from very diverse natural habitats (e.g. in foods, insects, wastewaters etc.) and it also exhibits wide metabolic and physiological diversity. Some of the activities of P. anomala, particularly its antimicrobial action, make it a very attractive organism for biological control applications in the agri-food sectors of industry. Being a ‘robust’ organism, it additionally has potential to be exploited in bioremediation of environmental pollutants. This paper provides an overview of cell physiological characteristics (growth, metabolism, stress responses) and biotechnological potential (e.g. as a novel biocontrol agent) of P. anomala and compares such properties with other yeast species, notably Saccharomyces cerevisiae, which remains the most exploited industrial microorganism. We await further basic knowledge of P. anomala cell physiology and genetics prior to its fuller commercial exploitation, but the exciting biotechnological potential of this yeast is highlighted in this paper.
Similar content being viewed by others
Notes
Throughout this paper the species will be referred to as Pichia anomala, rather than Wickerhamomyces anomalus (see Kurtzman et al. 2008 and Kurtzman, 2010), mainly because it was the nomenclature used in the symposium from which this manuscript emanated (1st International Pichia anomala mini-Symposium).
References
Bellinger Y, Larher F (1988) A 13C comparative nuclear magnetic resonance study of organic solute production and excretion by the yeasts Hansenula anomala and Saccharomyces cerevisiae in saline media. Can J Microbiol 34:605–612
Björnberg A, Schnürer J (1993) Inhibition of grain-storage molds in vitro by the yeast Pichia anomala (Hansen) Kurtzman. Can J Microbiol 39:623–628
Buzzini P, Martini A (2001) Large-scale screening of selected Candida maltosa, Debaryomyces hansenii and Pichia anomala killer toxin activity against pathogenic yeasts. Med Mycol 39:479–482
Buzzini P, Martini A, Cappelli F, Pagnoni UM, Davoli P (2003) A study on volatile organic compounds (VOCs) produced by tropical ascomycetous yeasts. Antonie van Leeuwenhoek 84:301–311
Charkrabarti A, Singh K, Narang A, Singhi S, Batra R, Rao KLN, Ray P, Gopalan S, Das S, Gupta V, Guota 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
Conti S, Magliani W, Arseni S, Frazzi R, Salati A, Ravanetti L, Polonelli L (2002) Inhibition by yeast killer toxin-like antibodies of oral Streptococci adhesion to tooth surfaces in an ex vivo model. Mol Med 8:313–317
Conti G, Magliani W, Conti S, Nencioni L, Sgarbanti R, Palamara AT, Polonelli L (2008) Therapeutic activity of an anti-idiotypic antibody-derived killer peptide against influenza a virus experimental infection. Antimicro Agents Chemother 52(12):4331–4337
Daniel H-M, Moons MC, Huret S, Van der Meulen R, Vrancken G, Vuyst L (2010) The sourdough ecosystem and Wickerhamomyces anomalus (= Pichia anomala). Antonie van Leeuwenhoek (in press)
De Hoog GS (1996) Risk assessment of fungi reported from humans and animals. Mycoses 39:407–417
De Ingeniis J, Raffaelli N, Ciani M, Mannazzu I (2009) Pichia anomala DBVPG 3003 secretes a ubiquitin-like protein that has antimicrobial activity. Appl Environ Microbiol 75:1129–1134
Deak T (2008) Handbook of food spoilage yeasts, 2nd edn. CRC Press/Taylor & Francis Group, Boca Raton
Druvefors UÄ, Passoth V, Schnürer J (2005) Nutrient effects on biocontrol of Pencillium roquefortii by Pichia anomala J121 during airtight storage of wheat. Appl Environ Microbiol 71:1865–1869
El-Latif Hesham A, Wang Z, Zhang Y, Zhang J, Wenzhou LV, Yang M (2006) Isolation and identification of a yeast strain capable of degrading four and five ring aromatic hydrocarbons. Ann Microbiol 56:109–112
Ertin H, Campbell I (2001) The production of low-alcohol wines by aerobic yeasts. J Inst Brew 107:207–215
Eun-Kyoung M, Kang H-J, Lee C-T, Xu B-J, Kim J-H, Wang Q-J, Kim J-C, Sung C-K (2003) Identification of phenylethyl alcohol and other volatile flavor compounds from yeasts, Pichia farinosa SKM-l, Pichia anomala SKM-T, and Galactomyces geotrichum SJM-59. J Microbiol Biotechnol 13:800–808
Fiori PL, Mattana A, Dessì D, Conti S, Magliani W, Polonelli L (2006) In vitro acanthamoebicidal activity of a killer monoclonal antibody and a synthetic peptide. J Antimicrob Chemother 57:891–898
Fredlund E (2004) Central carbon metabolism of the biocontrol yeast Pichia anomala—influence of oxygen limitation. PhD thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden
Fredlund E, Druvefors U, Boysen ME, Lingsten K-J, Schnürer J (2002) Physiological charachteristics of the biocontrol yeast Pichia anomala J121. FEMS Yeast Res 2:395–402
Fredlund E, Blank LM, Schnǘrer J, Sauer U, Passoth V (2004a) Oxygen- and glucose-dependent regulation of central carbon metabolism in Pichia anomala. Appl Environ Microbiol 70:5905–5911
Fredlund E, Druvefors UÄ, Olstorpe M, Passoth V, Schnürer J (2004b) Influence of ethyl acetate production and ploidy on the anti-mould activity of Pichia anomala. FEMS Microbiol Lett 238:475–478
Fredlund E, Beerlage C, Melin P, Schnürer J, Passoth V (2006) Oxygen and carbon source-regulated expression of PDC and ADH genes in the respiratory yeast Pichia anomala. Yeast 23:1137–1149
Hodgson VJ, Button D, Walker GM (1995) Anti-Candida activity of a killer toxin from the yeast Williopsis mrakii. Microbiology 141:2003–2012
Izgü F, Altinbay D (2004) Isolation and characterisation of the K5-type yeast killer protein and its homology with an exo-β-1, 3-glucanase. Biosci Biotechnol Biochem 68:685–693
Izgü F, Altinbay D, Türeli AE (2006) In vitro activity of panomycin, a novel exo-β-1, 3-glucanase isolated from Pichia anomala NCYC 434, against dermatophytes. Mycoses 50:31–34
Jijakli MH (2010) Pichia anomala in biocontrol for fruits: 20 years of fundamental and practical research. Antonie van Leeuwenhoek in press
Jijakli MH, Lepoivre P (1998) Characterisation of an exo-β-1, 3-glucanase produced by Pichia anomala strain K, antagonist of Botrytis cinerea on apples. Phytopathology 88:335–343
Jonsson A, Pahlow G (1984) Systematic classification and biochemical characterization of yeasts growing in grass silage inoculated with Lactobacillus cultures. Anim Res Develop 20:7–22
Kajikazawa T, Sugita T, Takashima M, Nishikawa A (2007) Detection of pathogenic yeasts from processes fresh edible sea urchins sold in a fish market. Japan J Med mycol 48:169–172
Kaku G, Hagiwara T (2008) Method for producing γ-aminobutyric-acid-containing food and yeast having high ability to produce γ -aminobutric acid. US Patent 20080138467
Kalathenos P, Sutherland JP, Roberts TA (1995) Resistance of some wine spoilage yeasts to combinations of ethanol and acids present in wine. J Appl Microbiol 78:245–250
Kurita O (2008) Increase of acetate ester-hydrolysing esterase activity in mixed cultures of S. cerevisiae and P. anomala. J Appl Microbiol 104:1051–1058
Kurtzman CP (1998) Pichia E.C. Hansen emend. Kurtzman. In: Kurtzman CP, Fell JW (eds) The yeasts a taxonomic study. Elsevier Science BV, Amsterdam, pp 273–352
Kurtzman CP (2001) Four new Candida species from geographically diverse locations. Antonie Van Leeuwenhoek 79:353–361
Kurtzman CP, Robnett CJ, Basehoar-Powers E (2008) Relationships among species of Pichia, Issatchenkia and Williopsis determined from multigene phylogenetic analysis and the proposal of Barnettozyma gen. nov., Lindnera gen. nov. and Wickerhamomyces gen. nov. FEMS Yeast Res 8:939–954
Lahlali R, Bajji M, Serrhini MN, Jijakli MH (2008) Modelling the effect of temperature, water activity and solute on the in vitro growth of the biocontrol yeast Pichia anomala strain K. Biotechnologie, Agronomie, Société et Environnement 12:353–359
Laitila A, Sarlin Y, Kotaviita E, Huttunen T, Home S, Williamson A (2007) Yeasts isolated from industrial maltings can suppress Fusarium growth and formation of gushing factors. J Ind Microbiol Biotechnol 34:701–713
Laitila A, Juvonen R, Sarlin T, Kotaviita E, Huttenen T, Wilhelmson A (2010) Pichia anomala in malting. Antonie van Leeuwenhoek (in press)
Lanciotti R, Sinigaglia M, Gardini F, Guerzoni ME (1998) Hansenula anomala as spoilage agent of cream-filled cakes. Microbiol Res 153:145–148
Lee J-S, Hyun K-W, Jeong S-C, Kim J-H, Choi YJ, Miguez CB (2003) Production of ribonucleotides by autolysis of Pichia anomala mutant and some physiological activities. Can J Microbiol 50:489–492
Liti G, Wardrop FR, Cardinali G, Martini A, Walker GM (2001) Differential responses to antimycin A and expressions of the Crabtree effect in selected Kluyveromyces spp. Annals of Microbiology 51:235–243
Lodder J, Kreger-van Rij NJW (1952) The yeasts a taxonomic study. North Holland Publishing Company, Amsterdam
Magliani W, Conti S, de Bernardis F, Gerloni M, Bertolotti D, Mozzoni P, Cassone A, Polonelli L (1997) Therapeutic potential of antiidiotypic single chain antibodies with yeast killer toxin activity. Nat Biotechnol 15:155–158
Martini A (1993) Origin and domestication of the wine yeast, Saccharomyces cerevisiae. J Wine Res 4:165–176
Masih EI, Alie I, Paul B (2000) Can the grey mould disease of the grape-vine be controlled by yeast? FEMS Microbiol Lett 189:233–237
Melin P, Håkansson S, Eberhard TH, Schnürer J (2005) Survival of the biocontrol yeast Pichia anomala afterlong-term storage in liquid formulations at different temperatures, assessed by flow cytometry. J Appl Microbiol 100:264–271
Melin P, Håkansson S, Schnürer J (2007) Optimisation and comparison of liquid and dry formulations of the biocontrol yeast Pichia anomala J121. Appl Microbiol Biotechnol 73:1008–1016
Mo EK, Lee JH, Xu BJ, Sung CK (2004) Identification of yeasts from Korean faeces and prerequisite characterisation for preparation of probiotics. Food Sci Biotechnol 13:63–70
Mohamed H, Saad A (2009) The biocontrol of postharvest disease (Botryodiplodia threobromae) of guava (Psidum guajava L) by the application of yeast strains. Postharvest Biol Technol 53:123–130
Mokiou S, Magan N (2008) Physiological manipulation and formulation of the biocontrol yeast Pichia anomala for control of Penicillium verrucosum and ochratoxin A contamination of moist grain. Biocontrol Sci Tech 18:1063–1073
Murphy N, Buchannan CR, Berenguer J, Bernaldo JL, Bouza EB (1986) Infective colonization of neonates by Hansenula anomala. Lancet 1:291–293
Nagatsuka Y, Kawasaki H, Seki T (2005) Pichia myanmarensis sp. nov., a novel cation-resistant yeast isolated from palm sugar in Mayanmar. Int J Syst Evol Microbiol 55:1379–1382
Naumov GI, Naumova ES, Schnürer J (2000) Genetic characterisation of the non-conventional yeast Hansenula anomala. Res Microbiol 152:551–562
Olstorpe M (2008) Feed grain improvement through biopreservation and bioprocessing. Microbial diversity, energy conservation and animal nutrition aspects. PhD thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden
Olstorpe, M (2010) P. anomala in grain biopreservation. Antonie van Leeuwenhoek (in press)
Olstorpe M, Schnürer J, Passoth V (2009) Screening of yeast strains for phytase activity. FEMS Yeast Res 9:478–488
Passoth V, Fredlund E, Druvefors UÄ, Schnürer J (2006) Biotechnology, physiology and genetics of the yeast Pichia anomala. FEMS Yeast Res 6:3–13
Passoth V, Eriksson A, Sandgren M, Ståhlberg J, Piens K, Schnürer J (2009) Airtight storage of moist wheat grain improves bioethanol yields. Biotechnol Biofuels 20:16. doi:10.1186/1754-6834-2-16
US Patent (2009) Patent #20090226991 Yeast organism producing isobutanol at a high yield
Petersson S, Schnürer J (1995) Biocontrol of mold growth in high moisture wheat stored under airtight conditions by Pichia anomala, Pichia guillermondii and Saccharomyces cerevisiae. Appl Environ Microbiol 61:1027–1032
Polonelli L, Morace G (1986) Re-evaluation of the yeast killer phenomenon. J Clin Microbiol 24:866–869
Polonelli L, Archbusacci C, Sestito M, Morace G (1983) Killer system: a simple method for differentiating Candida albicans strains. J Clin Microbiol 17:774–780
Polonelli L, Conti S, Gerloni M, Campani, Mantovanni MP, Morace G (1990) Production of yeast killer toxin in experimentally infected animals. Mycopathologia 110:169–175
Polonelli L, Magliani W, Conti S (2010) From Pichia anomala killer toxin through killer antibodies to killer peptides for a comprehensive anti-infective strategy. Antonie van Leeuwenhoek (in press)
Recek M, Cadez N, Raspor P (2002) Identification and characterisation of yeast isolates from pharmaceutical waste water. Food Technol Biotechnol 40:79–84
Reyes E (2004) Genetic polymorphism of clinical and environmental strains of Pichia anomala. Biol Res 37:747–757
Ricci I, Mosca M, Damiani C, Scuppa P, Rossi P, Capone A, Esposito F, Alma A, Sacchi L, Bandi C, Daffonchio D, Favia G (2010) Wickerhamomyces anomalus inhabits the midgut and reproductive organs of the Asian malaria vector Anopheles stephensi. Antonie van Leeuwenhoek (in press)
Rojas V, Gil JV, Pinaga F, Manzanares P (2001) Studies on acetate ester production by non-Saccharomyces wine yeasts. Int J Food Microbiol 86:181–188
Satyanarayana, T (2010) Production, characteristics and applications of the cell-bound phytase of Pichia anomala. Antonie van Leeuwenhoek (in press)
Sawant AD, Abdelal AT, Ahearn DG (1988) Anti-Candida albicans activity of Pichia anomala as determined by a growth rate reduction assay. Appl Environ Microbiol 54:1099–1103
Olstorpe M, Borling J, Schnürer, J and Passoth V (2009b) The biocontrol yeast Pichia anomala improves feed hygiene during moist storage of crimped cereal grain under Swedish farm conditions. Animal Feed Science and Technology doi;10.1016/j.anifeedsci.2009.12.008
Seguy N, Cailliez J-C, Polonelli L, Dei-Cas E, Camus D (1996) Inhibitory effect of a Pichia anomala killer toxin on Pneumocystis carnii infectivity to the SCID mouse. Parasitol Res 82:114–116
Stratford M (2006) Food and beverage spoilage yeasts. In: Querol A, Fleet GH (eds) The yeast handbook yeasts in food, beverages. Springer-Verlag, Berlin, pp 335–379
Sundh, I and Melin, P (2010) Safety and regulation of yeasts intentionally added to the food or feed chains. Antonie van Leeuwenhoek (in press)
Swangkeaw J, Vichitphan S, Butzke CE, Vichitphan K (2009) The characteristics of a novel Pichia anomala β-glucosidase with potentially aroma-enhancing capabilities in wine. Ann Microbiol 59:335–343
Thaniyavarn J, Chianguthai T, Sangvanich P, Roongsawang N, Washio K, Morikawa M, Thianiyavarn S (2008) Production of sophorolipid biosurfactant by Pichia anomala. Biosci Biotechnol Biochem 72:2061–2068
Thuler LC, Faviichenco S, Velasco E, Martins CA, Nascimiento CR, ans Castolho IA (1997) Fungemia caused by Hansenula anomala—an outbreak in a cancer hospital. Mycoses 40:193–196
Walker GM (1998) Yeast Physiology and Biotechnology. Wiley, Chichester
Walker GM, Van Dijck P (2006) Physiological and molecular responses of yeasts to the environment. In: Querol A, Fleet GH (eds) The yeast handbook. yeasts in food, beverages. Springer-Verlag, Berlin, pp 111–152
Walker GM, MacLeod AM, Hodgson VJ (1995) Interactions between killer yeasts and pathogenic fungi. FEMS Microbiol Lett 127:213–222
Wang X, Chi Z, Yue L, Li J, Li M, Wu L (2007) A marine killer yeast against the pathogenic yeast strain in crab (Portunus trituberculatus) and an optimisation of the toxin production. Microbiol Res 62:77–85
Ray RR, Nanda G (1996) Microbial β-amylases: biosynthesis, characteristics, and industrial applications. Crit Rev Microbiol 22(3):181–199
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Walker, G.M. Pichia anomala: cell physiology and biotechnology relative to other yeasts. Antonie van Leeuwenhoek 99, 25–34 (2011). https://doi.org/10.1007/s10482-010-9491-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-010-9491-8