Biotechnological exploitation of Tetrapisispora phaffii killer toxin: heterologous production in Komagataella phaffii (Pichia pastoris)

Applied Microbiology and Biotechnology

Volumn 101, Issue 7, 2017, Pages 2931-2942

  Chessa, Rossella ^a   Landolfo, Sara ^a   Ciani, Maurizio ^b   Budroni, Marilena ^a   Zara, Severino ^a   Ustun, Murat ^a,c   Cakar, Zeynep Petek ^c   Mannazzu, Ilaria ^a  

^a UNIVERSITY OF SASSARI   (Italy)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^c ISTANBUL TECHNICAL UNIVERSITY   (Turkey)

Author keywords

Dekkera bruxellensis; Kpkt; Natural antimicrobial; Pichia pastoris; Spoilage yeast; Glucanase

Indexed keywords

ANTIMICROBIAL AGENTS; BEVERAGES; BIOTECHNOLOGY; MICROORGANISMS; YEAST;

DEKKERA BRUXELLENSIS; GLUCANASE; KPKT; NATURAL-ANTIMICROBIALS; PICHIA PASTORIS;

SPOILAGE;

BETA GLUCAN HYDROLASE; GENOMIC DNA; HISTIDINE; LAMINARAN; METHANOL; RECOMBINANT PROTEIN; YEAST KILLER FACTOR; CYTOTOXIN;

ANTIMALARIAL AGENT; ANTIMICROBIAL ACTIVITY; BEVERAGE; BIOFUEL; BIOTECHNOLOGY; EXPLOITATION; FUNGUS; GROWTH; INDUSTRIAL TECHNOLOGY; RECOMBINATION; TOXIN; ULTRASTRUCTURE; WINE; YEAST;

ARTICLE; BIOTECHNOLOGICAL EXPLOITATION; BIOTECHNOLOGICAL PRODUCTION; CODON; CONTROLLED STUDY; ELECTROPORATION; ENZYME ACTIVITY; GENE INSERTION; GENE SEQUENCE; GENETIC TRANSCRIPTION; KOMAGATAELLA; KOMAGATAELLA PASTORIS; KOMAGATAELLA PHAFFII; MOLECULAR CLONING; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN STABILITY; RECOMBINANT PLASMID; RNA EXTRACTION; TETRAPISISPORA PHAFFII; WESTERN BLOTTING; YEAST; BIOTECHNOLOGY; BUDDING YEAST; CELL WALL; CHEMISTRY; DRUG EFFECTS; GENETICS; ISOLATION AND PURIFICATION; KLUYVEROMYCES; METABOLISM; MICROBIOLOGY; PICHIA; PROCEDURES; SACCHAROMYCES CEREVISIAE; WINE; ZYGOSACCHAROMYCES;

ANIMALIA; DEKKERA BRUXELLENSIS; PICHIA PASTORIS; TETRAPISISPORA PHAFFII; VITACEAE; ZYGOSACCHAROMYCES;

BIOTECHNOLOGY; CELL WALL; CYTOTOXINS; KILLER FACTORS, YEAST; KLUYVEROMYCES; PICHIA; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; WINE; YEASTS; ZYGOSACCHAROMYCES;

EID: 85007444079     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-016-8050-2     Document Type: Article

References (55)

1. Ashida S, Shimazaki T, Kitano K, Hara S (1983) New killer toxin of Hansenula mrakii. Agric Biol Chem 47:2953–2955
2. Bai J, Swartz DJ, Protasevich II, Brouillette CG, Harrel PM, Hildebrandt E, Gasser B, Mattanovich D, Ward A, Chang G, Urbatsch IL (2011) A gene optimization strategy that enhances production of fully functional P-glycoprotein in Pichia pastoris. PLoS One 6(8):e22577. doi:10.1371/journal.pone.0022577
3. Bevan EA, Somers JM (1969) Somatic segregation of the killer (k) and neutral (n) cytoplasmic genetic determinants in yeast. Genet Res 14:71–77
4. Borneman AR, Zeppel R, Chambers PJ, Curtin CD (2014) Insights into the Dekkera bruxellensis genomic landscape: comparative genomics reveals variations in ploidy and nutrient utilisation potential amongst wine isolates. PLoS Genet 10(2):e1004161. doi:10.1371/journal.pgen.1004161
5. Burke DA, Dawson D, Stearns T (2000) Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. Cold Spring Harbor Laboratory Press, Plainview, NY
6. Bussey H, Skipper N (1975) Membrane-mediated killing of Saccharomyces cerevisiae by glycoproteins from Torulopsis glabrata. J Bacteriol 124:476–483
7. Butler AR, White JH, Stark M Jr (1991) Analysis of the response of Saccharomyces cerevisiae cells to Kluyveromyces lactis toxin. J Gen Microbiol 137:1749–1757
8. Cereghino GPL, Stark CM, Kim D, Chang J, Shaheen N, Poerwanto H, Agari K, Moua P, Low LK, Tran N, Huang HD, Nattestad M, Oshiro KT, Chang JW, Chavan A, Tsai JW, Cereghino JL (2013) The effect of α-mating factor secretion signal mutations on recombinant protein expression in Pichia pastoris. Gene 519:311–317
9. Cereghino JL, Cregg J (2000) Heterologous protein expression in the methylotrophic yeast Pichia pastoris. FEMS Microbiol Rev 24:45–66
10. Chang S-W, Lee G-C, Shaw J-F (2006) Codon optimization of Candida rugosa lip1 gene for improving expression in Pichia pastoris and biochemical characterization of the purified recombinant LIP1 lipase. J Agric Food Chem 54:815–822
11. Chen WB, Han YF, Jong SC, Chang SC (2000) Isolation, purification, and characterization of a killer protein from Schwanniomyces occidentalis. Appl Environ Microbiol 66:5348–5352
12. Ciani M, Fatichenti F (2001) Killer toxin of Kluyveromyces phaffii DBVPG 6076 as a biopreservative agent to control apiculate wine yeast. Appl Environ Microbiol 67:3058–3063
13. Ciani M, Comitini F (2011) Non-Saccharomyces wine yeasts have a promising role in biotechnological approaches to winemaking. Ann Microbiol 61:25–32
14. Comitini F, Ciani M (2009) The zymocidial activity of Tetrapisispora phaffii in the control of Hanseniaspora uvarum during the early stages of winemaking. Lett Appl Microbiol 50:50–56
15. Comitini F, Di Pietro N, Zacchi L, Mannazzu I, Ciani M (2004a) Kluyveromyces phaffii killer toxin active against wine spoilage yeasts: purification and characterization. Microbiology 150:2535–2541
16. Comitini F, De Ingeniis J, Pepe L, Mannazzu I, Ciani M (2004b) Pichia anomala and Kluyveromyces wickerhamii killer toxins as new tools against Dekkera/Brettanomyces spoilage yeasts. FEMS Microbiol Lett 238:235–240
17. Comitini F, Mannazzu I, Ciani M (2009) Tetrapisispora phaffii killer toxin is a highly specific β-glucanase that disrupts the integrity of the yeast cell wall. Microb Cell Factories 8(55). doi:10.1186/1475-2859-8-55
18. 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(4):1129–1134
19. De la Pena P, Barros F, Gascon S, Lazo PS, Ramos S (1981) The effect of yeast killer toxin on sensitive cells of Saccharomyces cerevisiae. J Biol Chem 256:10420–10425
20. Eisfeld K, Riffer F, Mentges J, Schmitt MJ (2000) Endocytotic uptake and retrograde transport of a virally encoded killer toxin in yeast. Mol Microbiol 37:926–940
21. Hatoum R, Labrie S, Fliss I (2012) Antimicrobial and probiotic properties of yeasts: from fundamental to novel applications. Front Microbiol 3(421). doi:10.3389/fmicb.2012.00421
22. Hodgson VJ, Button D, Walker GM (1995) Anti-Candida activity of a novel killer toxin from the yeast Williopsis mrakii. Microbiology 141:2003–2012
23. Hong F, Meinander NQ, Jönsson LJ (2002) Fermentation strategies for improved heterologous expression of laccase in Pichia pastoris. Biotechnol Bioeng 79:438–449
24. Kandel JS, Stern TA (1979) Killer phenomenon in pathogenic yeast. Antimicrob Agents Chemother 15:568–571
25. Kast A, Klassen R, Meinhardt F (2014) rRNA fragmentation induced by a yeast killer toxin. Mol Microbiol 91(3):606–617
26. Kimchi-Sarfaty C, JM O, Kim I-W, Sauna ZE, Calcagno AM, Ambudkar SV, Gottesman MM (2007) A ‘silent’ polymorphism in the MDR1 gene changes substrate specificity. Science 315:525–528
27. Gln. Mol Microbiol 69(3):681–697
28. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685
29. Liu SQ, Tsao M (2009) Inhibition of spoilage yeasts in cheese by killer yeast Williopsis saturnus var. saturnus. Int J Food Microbiol 131(2–3):280–292
30. Lu J, Huang B, Esberg A, Johansson MJ, Byström AS (2005) The Kluyveromyces lactis gamma-toxin targets tRNA anticodons. RNA 11:1648–1654
31. Lowes KF, Shearman CA, Mackenzie D, Archer DB, Merry RJ, Gasson MJ (2000) Prevention of yeast spoilage in feed and food by the yeast mycocin HMK. Appl Environ Microbiol 66:1066–1076
32. Lucera A, Costa C, Conte A, Del Nobile MA (2012) Food applications of natural antimicrobial compounds. Front Microbiol 3(287). doi:10.3389/fmicb.2012.00287
33. Magliani W, Conti S, Gerloni M, Bertolotti D, Polonelli L (1997) Yeast killer systems. Clin Microbiol Rev 10:369–400
34. Macauley-Patrick S, Fazenda ML, McNeil B Harvey LM (2005) Heterologous protein production using the Pichia pastoris expression system. Yeast 22(4): 249–270.
35. Middelbeek EJ, Hermans JMH, Stumm C (1979) Production, purification and properties of a Pichia kluyveri killer toxin. A van Leeuw J Microb 45:437–450
36. Notario V (1982) β-glucanases from Candida albicans: purification, characterization and the nature of their attachment to cell wall components. J Gen Microbiol 128:747–759
37. Oro L, Zara S, Fancellu F, Mannazzu I, Budroni M, Ciano M, Comitini F (2014) TpBGL2 codes for a Tetrapisispora phaffii killer toxin active against wine spoilage yeasts. FEMS Yeast Res 14:464–471. doi:10.1111/1567-1364.12126
38. Palfree RG, Bussey H (1979) Yeast killer toxin: purification and characterization of the protein toxin from Saccharomyces cerevisiae. Eur J Biochem 93:487–493
39. Palpacelli V, Ciani M, Rosini G (1991) Activity of different ‘killer’ yeasts on strains of yeast species undesirable in the food industry. FEMS Microbiol Lett 68:75–78
40. Rosini G (1983) The occurrence of killer characters in yeasts. Can J Microbiol 29:1462–1464
41. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Laboratory Press, Cold Spring Harbor, NY
42. Schmitt MJ, Klavehn P, Wang J, Shoning I, Tipper DJ (1996) Cell cycle studies on the mode of action of yeast K28 killer toxin. Microbiology 142:2655–2662
43. Schifferdecker AJ, Dashko S, Ishchuk OP, Piškur J (2014) The wine and beer yeast Dekkera bruxellensis. Yeast 31:323–332
44. Sugisaki Y, Gunge N, Sakaguchi K, Yamasaky M, Tamura G (1984) Characterization of a novel killer toxin encoded by a double-stranded linear DNA plasmid of Kluyveromyces lactis. Eur J Biochem 141:241–245
45. Tiwari B, Valdramidis V, O’ Donnell CP, Muthukumarappan K, Cullen PJ, Bourke P (2009) Application of natural antimicrobials for food preservation. J Agric Food Chem 57(14):5987–6000. doi:10.1021/jf900668n
46. Todd BEN, Fleet GH, Henschke PA (2000) Promotion of autolysis through the interaction of killer and sensitive yeasts: potential application in sparkling wine production. Am J Enol Vitic 51:65–72
47. Ueda-Nishimura K, Mikata K (1999) A new yeast genus, Tetrapisispora gen. nov. Tetrapisispora iriomotensis sp. nov., Tetrapisispora nanseiensis sp. nov. and Tetrapisispora arboricola sp. nov., from the Nansei Islands, and reclassification Kluyveromyces phaffii (van der Walt) van der Walt as Tetrapisispora phaffii comb. nov. Int J Syst Bacteriol 49:1915–1924
48. Weiler F, Schmitt MJ (2003) Zygocin, a secreted antifungal toxin of the yeast Zygosaccharomyces bailii, and its effect on sensitive fungal cells. FEMS Yeast Res 3:69–76
49. Yamamoto T, Hiratani T, Hirata H, Imani M, Yamaguchi H (1986) Killer toxin from Hansenula mrakii selectively inhibits cell wall synthesis in a sensitive yeast. FEBS Lett 197:50–54
50. Yang Y-L, Chang S-H, Gong X, Wu J, Liu B (2012) Expression, purification and characterization of low-glycosylation influenza neuraminidase in α-1,6-mannosyltransferase defective Pichia pastoris. Mol Biol Rep 39:857–864
51. Yokomori Y, Akiyama H, Shimizu K (1988) Toxin of wild Candida killer yeast with a novel killer property. Agric Biol Chem 52:2797–2801
52. Young TW, Yagiu M (1978) A comparison of the killer character in different yeasts and its classification. Antonie Van Leeuwenhoek 44:59–77
53. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalisation of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Gen Biol 3:1–12
54. Zagorc T, Maraz A, Cadez N, Jemec KP, Peter G, Resnik M, Nemanic J, Raspor P (2001) Indigenous wine killer yeasts and their application as a starter culture in wine fermentation. Food Microbiol 18:441–451
55. Zhao H, Blazanovic K, Choi Y, Bailey-Kellogg C, Griswold KE (2014) Gene and protein sequence optimization for high level production of fully active and aglycosylated lysostaphin in Pichia pastoris. Appl Environ Microbiol 89(9):2746–2753