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Cell-surface engineering of yeasts for whole-cell biocatalysts

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Abstract

Due to the unique advantages comparing with traditional free enzymes and chemical catalysis, whole-cell biocatalysts have been widely used to catalyze reactions effectively, simply and environment friendly. Cell-surface display technology provides a novel and effective approach for improved whole-cell biocatalysts expressing heterologous enzymes on the cell surface. They can overcome the substrate transport limitation of the intracellular expression and provide the enzymes with enhanced properties. Among all the host surface-displaying microorganisms, yeast is ideally suitable for constructing whole cell-surface-displaying biocatalyst, because of the large cell size, the generally regarded as safe (GRAS) status, and the perfect post-translational processing of secreted proteins. Yeast cell-surface display system has been a promising and powerful method for development of novel and improved engineered biocatalysts. In this review, the characterization and principles of yeast cell-surface display and the applications of yeast cell-surface display in engineered whole-cell biocatalysts as well as the improvement of the enzyme efficiency are summarized and discussed.

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References

  1. Jemli S, Ayadi-Zouari D, Hlima HB, Bejar S (2016) Biocatalysts: application and engineering for industrial purposes. Crit Rev Biotechnol 36(2):246–258

    Article  CAS  PubMed  Google Scholar 

  2. Bommarius AS, Riebel BR (2004) Introduction to biocatalysis. Biocatalysis: Wiley-VCH Verlag GmbH & Co. KGaA. p 1–18.

  3. Tabañag IDF, Chu I, Wei Y, Tsai S (2018) The role of yeast-surface-display techniques in creating biocatalysts for consolidated bioProcessing. Catalysts 8(3):94

    Article  Google Scholar 

  4. Frock AD, Kelly RM (2012) Extreme thermophiles: moving beyond single-enzyme biocatalysis. Curr Opin Chem Eng 1(4):363–372

    Article  PubMed  PubMed Central  Google Scholar 

  5. de Carvalho CCCR (2017) Whole cell biocatalysts: essential workers from Nature to the industry. Microb Biotechnol 10(2):250–263

    Article  PubMed  Google Scholar 

  6. Schüürmann J, Quehl P, Festel G, Jose J (2014) Bacterial whole-cell biocatalysts by surface display of enzymes: toward industrial application. Appl Microbiol Biotechnol 98(19):8031–8046

    Article  PubMed  Google Scholar 

  7. Kondo A, Liu Y, Furuta M, Fujita Y, Matsumoto T, Fukuda H (2000) Preparation of high activity whole cell biocatalyst by permeabilization of recombinant flocculent yeast with alcohol. Enzyme Microbial Technol 27(10):806–811

    Article  CAS  Google Scholar 

  8. Ni Y, Chen RR (2004) Accelerating whole-cell biocatalysis by reducing outer membrane permeability barrier. Biotechnol Bioeng 87(6):804–811

    Article  CAS  PubMed  Google Scholar 

  9. Yang J, Liu R, Jiang H, Yang Y, Qiao C (2012) Selection of a whole-cell biocatalyst for methyl parathion biodegradation. Appl Microbiol Biotechnol 95(6):1625–1632

    Article  CAS  PubMed  Google Scholar 

  10. Yang K, Li F, Qiao Y, Zhou Q, Hu Z, He Y, Yan J (2018) Design of a new multienzyme complex synthesis system based on Yarrowia lipolytica simultaneously secreted and surface displayed fusion proteins for sustainable production of fatty acid-derived hydrocarbons. Acs Sustain Chem Eng 6(12): 17035-17043

  11. Kuroda K, Ueda M (2011) Cell surface engineering of yeast for applications in white biotechnology. Biotech Lett 33(1):1–9

    Article  CAS  Google Scholar 

  12. Smith GP (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228(4705):1315–1317

    Article  CAS  PubMed  Google Scholar 

  13. Ueda M (2016) Establishment of cell surface engineering and its development. Biosci Biotechnol Biochem 80(7):1243–1253

    Article  CAS  PubMed  Google Scholar 

  14. Gera N, Hussain M, Rao BM (2013) Protein selection using yeast surface display. Methods 60(1):15–26

    Article  CAS  PubMed  Google Scholar 

  15. Grzeschik J, Hinz SC, Könning D, Pirzer T, Becker S, Zielonka S, Kolmar H (2017) A simplified procedure for antibody engineering by yeast surface display: coupling display levels and target binding by ribosomal skipping. Biotechnol J 12(2):1600454

    Article  Google Scholar 

  16. Ryu S, Karim MN (2011) A whole cell biocatalyst for cellulosic ethanol production from dilute acid-pretreated corn stover hydrolyzates. Appl Microbiol Biotechnol 91(3):529–542

    Article  CAS  PubMed  Google Scholar 

  17. Shibasaki S, Ueda M (2014) Bioadsorption strategies with yeast molecular display technology. Biocontrol Sci 19(4):157–164

    Article  CAS  PubMed  Google Scholar 

  18. Liu Z, Ho S, Hasunuma T, Chang J, Ren N, Kondo A (2016) Recent advances in yeast cell-surface display technologies for waste biorefineries. Bioresour Technol 215:324–333.

  19. Tanaka T, Kondo A (2015) Cell surface engineering of industrial microorganisms for biorefining applications. Biotechnol Adv 33(7):1403–1411

    Article  CAS  PubMed  Google Scholar 

  20. Salem M, Brim H, Hussain S, Arshad M, Leigh MB, Zia-ul-hassan (2008) Perspectives on microbial cell surface display in bioremediation. Biotechnol Adv 26(2):151–161

    Article  Google Scholar 

  21. Shibasaki S, Ninomiya Y, Ueda M, Iwahashi M, Katsuragi T, Tani Y, Tanaka A (2001) Intelligent yeast strains with the ability to self-monitor the concentrations of intra- and extracellular phosphate or ammonium ion by emission of fluorescence from the cell surface. Appl Microbiol Biotechnol 57(5–6):702–707

    CAS  PubMed  Google Scholar 

  22. Meusser B, Hirsch C, Jarosch E, Sommer T (2005) ERAD: the long road to destruction. Nat Cell Biol 7(8):766–772

    Article  CAS  PubMed  Google Scholar 

  23. Boder ET, Wittrup KD (1997) Yeast surface display for screening combinatorial polypeptide libraries. Nat Biotechnol 15(6):553–557

    Article  CAS  PubMed  Google Scholar 

  24. Kondo A, Ueda M (2004) Yeast cell-surface display—applications of molecular display. Appl Microbiol Biotechnol 64(1):28–40

    Article  CAS  PubMed  Google Scholar 

  25. Manners DJ, Masson AJ, Patterson JC (1973) The structure of a beta-(1 leads to 3)-d-glucan from yeast cell walls. Biochem J 135(1):19–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Horisberger M, Vonlanthen M (1977) Location of mannan and chitin on thin sections of budding yeasts with gold markers. Arch Microbiol 115(1):1–7

    Article  CAS  PubMed  Google Scholar 

  27. Zlotnik H, Fernandez MP, Bowers B, Cabib E (1984) Saccharomyces cerevisiae mannoproteins form an external cell wall layer that determines wall porosity. J Bacteriol 159(3):1018–1026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Smith MR, Khera E, Wen F (2015) Engineering novel and improved biocatalysts by cell surface display. Ind Eng Chem Res 54(16):4021–4032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lee SY, Choi JH, Xu ZH (2003) Microbial cell-surface display. Trends Biotechnol 21(1):45–52

    Article  CAS  PubMed  Google Scholar 

  30. Yamada R, Kimoto Y, Ogino H (2016) Combinatorial library strategy for strong overexpression of the lipase from Geobacillus thermocatenulatus on the cell surface of yeast Pichia pastoris. Biochem Eng J 113:7–11

    Article  CAS  Google Scholar 

  31. Van der Vaart JM, Te Biesebeke R, Chapman JW, Toschka HY, Klis FM, Verrips CT (1997) Comparison of cell wall proteins of Saccharomyces cerevisiae as anchors for cell surface expression of heterologous proteins. Appl Environ Microbiol 63(2):615–620

    Article  PubMed  PubMed Central  Google Scholar 

  32. Liu Y, Zhang R, Lian Z, Wang S, Wright AT (2014) Yeast cell surface display for lipase whole cell catalyst and its applications. J Mol Catal B Enzym 106:17–25

    Article  CAS  Google Scholar 

  33. De Groot PWJ, Ram AF, Klis FM (2005) Features and functions of covalently linked proteins in fungal cell walls. Fungal Genet Biol 42(8):657–675

    Article  PubMed  Google Scholar 

  34. Kollar R, Reinhold BB, Petrakova E, Yeh H, Ashwell G, Drgonova J, Cabib E (1997) Architecture of the yeast cell wall— β-(1–6)-glucan interconnects mannoprotein, β-(1–3)-glucan, and chitin. J Biol Chem 272(28):17762–17775

    CAS  PubMed  Google Scholar 

  35. Lipke PN, Kurjan J (1992) Sexual agglutination in budding yeasts: structure, function, and regulation of adhesion glycoproteins. Microbiol Rev 56(1):180–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Terrance K, Heller P, Wu YS, Lipke PN (1987) Identification of glycoprotein components of alpha-agglutinin, a cell adhesion protein from Saccharomyces cerevisiae. J Bacteriol 169(2):475–482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Watzele M, Klis F, Tanner W (1988) Purification and characterization of the inducible a agglutinin of Saccharomyces cerevisiae. EMBO J 7(5):1483–1488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Cappellaro C, Hauser K, Mrsa V, Watzele M, Watzele G, Gruber C, Tanner W (1991) Saccharomyces cerevisiae a- and alpha-agglutinin: characterization of their molecular interaction. EMBO J 10(13):4081–4088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Roy A, Lu CF, Marykwas DL, Lipke PN, Kurjan J (1991) The AGA1 product is involved in cell surface attachment of the Saccharomyces cerevisiae cell adhesion glycoprotein a-agglutinin. Mol Cell Biol 11(8):4196–4206

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Wang Z, Mathias A, Stavrou S, Neville DM (2005) A new yeast display vector permitting free scFv amino termini can augment ligand binding affinities. Protein Eng Des Sel 18(7):337–343

    Article  PubMed  Google Scholar 

  41. Tanaka T, Yamada R, Ogino C, Kondo A (2012) Recent developments in yeast cell surface display toward extended applications in biotechnology. Appl Microbiol Biotechnol 95(3):577–591

    Article  CAS  PubMed  Google Scholar 

  42. Yang X, Tang H, Song M, Shen Y, Hou J, Bao X (2019) Development of novel surface display platforms for anchoring heterologous proteins in Saccharomyces cerevisiae. Microb Cell Fact 18:85

    Article  PubMed  PubMed Central  Google Scholar 

  43. Goyal G, Tsai SL, Madan B, DaSilva NA, Chen W (2011) Simultaneous cell growth and ethanol production from cellulose by an engineered yeast consortium displaying a functional mini-cellulosome. Microb Cell Fact 10:89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Inokuma K, Hasunuma T, Kondo A (2014) Efficient yeast cell-surface display of exo- and endo-cellulase using the SED1 anchoring region and its original promoter. Biotechnol Biofuels 7(1):8

    Article  PubMed  PubMed Central  Google Scholar 

  45. Vallejo JA, Sanchez-Perez A, Martinez JP, Villa TG (2013) Cell aggregations in yeasts and their applications. Appl Microbiol Biotechnol 97(6):2305–2318

    Article  CAS  PubMed  Google Scholar 

  46. Yuzbasheva EY, Yuzbashev TV, Laptev IA, Konstantinova TK, Sineoky SP (2011) Efficient cell surface display of Lip2 lipase using C-domains of glycosylphosphatidylinositol-anchored cell wall proteins of Yarrowia lipolytica. Appl Microbiol Biotechnol 91(3):645–654

    Article  CAS  PubMed  Google Scholar 

  47. Bauer FF, Govender P, Bester MC (2010) Yeast flocculation and its biotechnological relevance. Appl Microbiol Biotechnol 88(1):31–39

    Article  CAS  PubMed  Google Scholar 

  48. Matsumoto T, Fukuda H, Ueda M, Tanaka A, Kondo A (2002) Construction of yeast strains with high cell surface lipase activity by using novel display systems based on the Flo1p flocculation functional domain. Appl Environ Microbiol 68(9):4517–4522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Bulani SI, Moleleki L, Albertyn J, Moleleki N (2012) Development of a novel rDNA based plasmid for enhanced cell surface display on Yarrowia lipolytica. 2(1): 1–8

  50. Andreu C, Olmo MD (2017) Development of a new yeast surface display system based on Spi1 as an anchor protein. Appl Microbiol Biotechnol 101(1):287–299

    Article  CAS  PubMed  Google Scholar 

  51. Zhang L, Liang S, Zhou X, Jin Z, Jiang F, Han S, Lin Y (2013) Screening for glycosylphosphatidylinositol-modified cell wall proteins inPichia pastoris and their recombinant expression on the cell surface. Appl Environ Microbiol 79(18):5519–5526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Wang P, He J, Sun Y, Reynolds M, Zhang L, Han S, Lin Y (2016) Display of fungal hydrophobin on the Pichia pastoris cell surface and its influence on Candida antarctica lipase B. Appl Microbiol Biotechnol 100(13):5883–5895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Phienluphon A, Mhuantong W, Boonyapakron K, Deenarn P, Champreda V, Wichadakul D, Suwannarangsee S (2019) Identification and evaluation of novel anchoring proteins for cell surface display on Saccharomyces cerevisiae. Appl Microbiol Biotechnol 103(7):3085–3097

    Article  CAS  PubMed  Google Scholar 

  54. Mrsa V, Seidl T, Gentzsch M, Tanner W (1997) Specific labelling of cell wall proteins by biotinylation. Identification of four covalently linked O-mannosylated proteins of Saccharomyces cerevisiae. Yeast 13(12): 1145–1154.

  55. Tohe A, Yasunaga S, Nisogi H, Tanaka K, Oguchi T, Matsui Y (1993) Three yeast genes, PIR1, PIR2 and PIR3, containing internal tendem repeats, are related to each other, and PIR1 and PIR2 are required for tolerance to heat-shock. Yeast 9(5):481–494

    Article  CAS  Google Scholar 

  56. Yang N, Yu Z, Jia D, Xie Z, Zhang K, Xia Z, Qiao M (2014) The contribution of Pir protein family to yeast cell surface display. Appl Microbiol Biotechnol 98(7):2897–2905

    Article  CAS  PubMed  Google Scholar 

  57. Goergens JF, Bressler DC, van Rensburg E (2015) Engineering Saccharomyces cerevisiae for direct conversion of raw, uncooked or granular starch to ethanol. Crit Rev Biotechnol 35(3):369–391

    Article  Google Scholar 

  58. Andres I, Gallardo O, Parascandola P, Pastor F, Zueco J (2005) Use of the cell wall protein pir4 as a fusion partner for the expression of Bacillus sp. BP-7 xylanase A in Saccharomyces cerevisiae. Biotechnol Bioeng 89(6): 690–697.

  59. Gao G, Mao R, Xiao Y, Zhou J, Liu Y, Li G (2017) Efficient yeast cell-surface display of an endoglucanase of Aspergillus flavus and functional characterization of the whole-cell enzyme. World J Microbiol Biotechnol 33(6):114

    Article  PubMed  Google Scholar 

  60. Motone K, Takagi T, Sasaki Y, Kuroda K, Ueda M (2016) Direct ethanol fermentation of the algal storage polysaccharide laminarin with an optimized combination of engineered yeasts. J Biotechnol 231:129–135

    Article  CAS  PubMed  Google Scholar 

  61. Takagi T, Yokoi T, Shibata T, Morisaka H, Kuroda K, Ueda M (2016) Engineered yeast whole-cell biocatalyst for direct degradation of alginate from macroalgae and production of non-commercialized useful monosaccharide from alginate. Appl Microbiol Biotechnol 100(4):1723–1732

    Article  CAS  PubMed  Google Scholar 

  62. Khatun MM, Liu C, Zhao X, Yuan W, Bai F (2017) Consolidated ethanol production from Jerusalem artichoke tubers at elevated temperature by Saccharomyces cerevisiae engineered with inulinase expression through cell surface display. J Ind Microbiol Biotechnol 44(2):295–301

    Article  CAS  PubMed  Google Scholar 

  63. Takenaka M, Kobayashi T, Inokuma K, Hasunuma T, Maruyama T, Ogino C, Kondo A (2017) Mapping of endoglucanases displayed on yeast cell surface using atomic force microscopy. Colloids Surf B 151:134–142

    Article  CAS  Google Scholar 

  64. Sasaki Y, Takagi T, Motone K, Kuroda K, Ueda M (2017) Enhanced direct ethanol production by cofactor optimization of cell surface-displayed xylose isomerase in yeast. Biotechnol Prog 33(4):1068–1076

    Article  CAS  PubMed  Google Scholar 

  65. Raoufi Z, Mousavi Gargari SL (2018) Biodiesel production from microalgae oil by lipase from Pseudomonas aeruginosa displayed on yeast cell surface. Biochem Eng J 140:1–8

    Article  CAS  Google Scholar 

  66. Qiao Y, Yang K, Zhou Q, Xu Z, Yan Y, Xu L, Yan J (2018) Engineering Yarrowia lipolytica for sustainable production of fatty acid methyl esters using in Situ self-cycled glycerol as a carbon source. Acs Sustain Chem Eng 6(6):7645–7651

    Article  CAS  Google Scholar 

  67. Becker J, Wittmann C (2012) Bio-based production of chemicals, materials and fuels—Corynebacterium glutamicum as versatile cell factory. Curr Opin Biotechnol 23(4):631–640

    Article  CAS  PubMed  Google Scholar 

  68. Zhang L, An J, Li L, Wang H, Liu D, Li N, Deng Z (2016) Highly efficient fructooligosaccharides production by an erythritol-producing yeast Yarrowia lipolytica displaying fructosyltransferase. J Agric Food Chem 64(19):3828–3837

    Article  CAS  PubMed  Google Scholar 

  69. Li N, Wang H, Li L, Cheng H, Liu D, Cheng H, Deng Z (2016) Integrated approach to producing high-purity trehalose from maltose by the yeast Yarrowia lipolytica displaying trehalose synthase (TreS) on the cell surface. J Agric Food Chem 64(31):6179–6187

    Article  CAS  PubMed  Google Scholar 

  70. Wang Z, Wang Q, Liu S, Liu X, Yu X, Jiang Y (2019) Efficient conversion of cane molasses towards high-purity isomaltulose and cellular lipid using an engineered Yarrowia lipolytica strain in fed-batch fermentation. Molecules 24(7):1228

    Article  PubMed Central  Google Scholar 

  71. Cejnar R, Hložková K, Kotrba P, Dostálek P (2016) Surface-engineered Saccharomyces cerevisiae displaying α-acetolactate decarboxylase from Acetobacter aceti ssp xylinum. Biotech Lett 38(12):2145–2151

    Article  CAS  Google Scholar 

  72. Zhang Y, Min Z, Qin Y, Ye DQ, Song YY, Liu YL (2019) Efficient display of Aspergillus niger beta-glucosidase on Saccharomyces cerevisiae cell wall for aroma enhancement in Wine. J Agric Food Chem 67(18):5169–5176

    Article  CAS  PubMed  Google Scholar 

  73. Gal I, Schlesinger O, Amir L, Alfonta L (2016) Yeast surface display of dehydrogenases in microbial fuel-cells. Bioelectrochemistry 112:53–60

    Article  CAS  PubMed  Google Scholar 

  74. Lei Y, Mulchandani A, Chen W (2005) Improved degradation of organophosphorus nerve agents and p-nitrophenol by Pseudomonas putida JS444 with surface-expressed organophosphorus hydrolase. Biotechnol Prog 21(3):678–681

    Article  CAS  PubMed  Google Scholar 

  75. Richins RD, Kaneva I, Mulchandani A, Chen W (1997) Biodegradation of organophosphorus pesticides by surface-expressed organophosphorus hydrolase. Nat Biotechnol 15(10):984–987

    Article  CAS  PubMed  Google Scholar 

  76. Takayama K, Suye S, Kuroda K, Ueda M, Kitaguchi T, Tsuchiyama K, Mulchandani A (2006) Surface display of organophosphorus hydrolase on Saccharomyces cerevisiae. Biotechnol Prog 22(4):939–943

    Article  CAS  PubMed  Google Scholar 

  77. Fukuda T, Tsuchiyama K, Makishima H, Takayama K, Mulchandani A, Kuroda K, Suye S (2010) Improvement in organophosphorus hydrolase activity of cell surface-engineered yeast strain using Flo1p anchor system. Biotechnol Lett 32(5):655–659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Wang X, Chi Z, Ru S, Chi Z (2012) Genetic surface-display of methyl parathion hydrolase on Yarrowia lipolytica for removal of methyl parathion in water. Biodegradation 23(5):763–774

    Article  CAS  PubMed  Google Scholar 

  79. Leng S, Yang C, Tsai S (2016) Designer oleosomes as efficient biocatalysts for enhanced degradation of organophosphate nerve agents. Chem Eng J 287:568–574

    Article  CAS  Google Scholar 

  80. Liang B, Wang G, Yan L, Ren H, Feng R, Xiong Z, Liu A (2019) Functional cell surface displaying of acetylcholinesterase for spectrophotometric sensing organophosphate pesticide. Sensors and Actu B Chem 279:483–489

    Article  CAS  Google Scholar 

  81. Shibasaki S, Kawabata A, Tanino T, Kondo A, Ueda M, Tanaka M (2009) Evaluation of the biodegradability of polyurethane and its derivatives by using lipase-displaying arming yeast. Biocontrol Sci 14(4):171–175

    Article  CAS  PubMed  Google Scholar 

  82. Chen Z, Wang Y, Cheng Y, Wang X, Tong S, Yang H, Wang Z (2020) Efficient biodegradation of highly crystallized polyethylene terephthalate through cell surface display of bacterial PETase. Sci Total Environ 709:136138

    Article  CAS  PubMed  Google Scholar 

  83. Zhu B, Wei N (2018) Biocatalytic degradation of parabens mediated by cell surface displayed cutinase. Environ Sci Technol 53(1):354–364

    Article  PubMed  Google Scholar 

  84. Nissum M, Schiodt CB, Welinder KG (2001) Reactions of soybean peroxidase and hydrogen peroxide pH 2.4–12.0, and veratryl alcohol at pH 2.4. Biochim Biophys Acta 1545(1–2): 339–48.

  85. Wang J, Wang C, Men X, Yue T, Madzak C, Xiang X, Zhang H (2020) Construction of arming Yarrowia lipolytica surface-displaying soybean seed coat peroxidase for use as whole-cell biocatalyst. Enzyme Microbial Technol 135:109498

    Article  CAS  Google Scholar 

  86. Liang H, Wang Q, Shen S, Jia Y, Li P, Zeng F, Dong J (2020) Yeast surface displayed xylanase is an efficient strategy to induce corn defence response. Biotechnol Biotechnol Equip 34(1):665–672

    Article  CAS  Google Scholar 

  87. Peng X (2013) Improved thermostability of Lipase B from Candida antarctica by directed evolution and display on yeast surface. Appl Biochem Biotechnol 169(2):351–358

    Article  CAS  PubMed  Google Scholar 

  88. Moura MVH, Da Silva GP, Machado ACDO, Torres FAG, Freire DMG, Almeida RV (2015) Displaying lipase B from Candida antarctica in Pichia pastoris using the yeast surface display approach: Prospection of a new anchor and characterization of the whole cell biocatalyst. PLoS One 10(10):e0141454

    Article  PubMed  PubMed Central  Google Scholar 

  89. Kato M, Fuchimoto J, Tanino T, Kondo A, Fukuda H, Ueda M (2007) Preparation of a whole-cell biocatalyst of mutated Candida antarctica lipase B (mCALB) by a yeast molecular display system and its practical properties. Appl Microbiol Biotechnol 75(3):549–555

    Article  CAS  PubMed  Google Scholar 

  90. Su G, Zhang X, Lin Y (2010) Surface display of active lipase in Pichia pastoris using Sed1 as an anchor protein. Biotech Lett 32(8):1131–1136

    Article  CAS  Google Scholar 

  91. Yuzbasheva EY, Yuzbashev TV, Perkovskaya NI, Mostova EB, Vybornaya TV, Sukhozhenko AV, Sineoky SP (2015) Cell surface display of Yarrowia lipolytica Lipase Lip2p using the cell wall protein YlPir1p, its characterization, and application as a whole-cell biocatalyst. Appl Biochem Biotechnol 175(8):3888–3900

    Article  CAS  PubMed  Google Scholar 

  92. Tokuhiro K, Ishida N, Kondo A, Takahashi H (2008) Lactic fermentation of cellobiose by a yeast strain displaying β-glucosidase on the cell surface. Appl Microbiol Biotechnol 79(3):481–488

    Article  CAS  PubMed  Google Scholar 

  93. Kaya M, Ito J, Kotaka A, Matsumura K, Bando H, Sahara H, Hata Y (2008) Isoflavone aglycones production from isoflavone glycosides by display of β-glucosidase from Aspergillus oryzae on yeast cell surface. Appl Microbiol Biotechnol 79(1):51–60

    Article  CAS  PubMed  Google Scholar 

  94. Shi B, Ke X, Yu H, Xie J, Jia Y, Guo R (2015) Novel properties for endoglucanase acquired by cell-surface display technique. J Microbiol Biotechnol 25(11):1856–1862

    Article  CAS  PubMed  Google Scholar 

  95. Yang S, Lv X, Wang X, Wang J, Wang R, Wang T (2017) Cell-surface displayed expression of trehalose synthase from Pseudomonas putida ATCC 47054 in Pichia Pastoris using Pir1p as an anchor protein. Front Microbiol 8:2583

    Article  PubMed  PubMed Central  Google Scholar 

  96. Fukuda T, Isogawa D, Takagi M, Kato-Murai M, Kimoto H, Kusaoke H, Suye S (2007) Yeast cell-surface expression of chitosanase from Paenibacillus fukuinensis. Biosci Biotechnol Biochem 71(11):2845–2847

    Article  CAS  PubMed  Google Scholar 

  97. He X, Shang J, Li F, Liu H (2015) Yeast cell surface display of linoleic acid isomerase from Propionibacterium acnes and its application for the production of trans-10, cis-12 conjugated linoleic acid. Biotechnol Appl Biochem 62(1):1–8

    Article  CAS  PubMed  Google Scholar 

  98. Liu X, Chi Z, Liu G, Wang F, Madzak C, Chi Z (2010) Inulin hydrolysis and citric acid production from inulin using the surface-engineered Yarrowia lipolytica displaying inulinase. Metab Eng 12(5):469–476

    Article  CAS  PubMed  Google Scholar 

  99. Hara KY, Kim S, Yoshida H, Kiriyama K, Kondo T, Okai N, Kondo A (2012) Development of a glutathione production process from proteinaceous biomass resources using protease-displayingSaccharomyces cerevisiae. Appl Microbiol Biotechnol 93(4):1495–1502

    Article  CAS  PubMed  Google Scholar 

  100. Qiu Z, Tan H, Zhou S, Cao L (2014) Surface display of a bifunctional glutathione synthetase on Saccharomyces cerevisiae for converting chicken feather hydrolysate into glutathione. Mol Biotechnol 56(8):726–730

    Article  CAS  PubMed  Google Scholar 

  101. Ilić Đurđić K, Ostafe R, Đurđević Đelmaš A, Popović N, Schillberg S, Fischer R, Prodanović R (2020) Saturation mutagenesis to improve the degradation of azo dyes by versatile peroxidase and application in form of VP-coated yeast cell walls. Enzyme and Microbial Technol 136:109509

    Article  Google Scholar 

  102. Yamada R, Hasunuma T, Kondo A (2013) Endowing non-cellulolytic microorganisms with cellulolytic activity aiming for consolidated bioprocessing. Biotechnol Adv 31(6):754–763

    Article  CAS  PubMed  Google Scholar 

  103. Fan L, Zhang Z, Mei S, Lu Y, Li M, Wang Z, Tan T (2016) Engineering yeast with bifunctional minicellulosome and cellodextrin pathway for co-utilization of cellulose-mixed sugars. Biotechnol Biofuels 9(1):137

    Article  PubMed  PubMed Central  Google Scholar 

  104. Lynd LR, Van Zyl WH, McBride JE, Laser M (2005) Consolidated bioprocessing of cellulosic biomass: an update. 16(5): 577–583

  105. Fujita Y, Takahashi S, Ueda M, Tanaka A, Okada H, Morikawa Y, Kondo A (2002) Direct and efficient production of ethanol from cellulosic material with a yeast strain displaying cellulolytic enzymes. Appl Environ Microbiol 68(10):5136–5141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Fujita Y, Ito J, Ueda M, Fukuda H, Kondo A (2004) Synergistic saccharification, and direct fermentation to ethanol, of amorphous cellulose by use of an engineered yeast strain codisplaying three types of cellulolytic enzyme. Appl Environ Microbiol 70(2):1207–1212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Katahira S, Fujita Y, Mizuike A, Fukuda H, Kondo A (2004) Construction of a xylan-fermenting yeast strain through codisplay of xylanolytic enzymes on the surface of xylose-utilizing Saccharomyces cerevisiae cells. Appl Environ Microbiol 70(9):5507–5514

    Article  Google Scholar 

  108. Shigechi H, Fujita Y, Koh J, Ueda M, Fukuda H, Kondo A (2004) Energy-saving direct ethanol production from low-temperature-cooked corn starch using a cell-surface engineered yeast strain co-displaying glucoamylase and α-amylase. Biochem Eng J 18(2):149–153

    Article  CAS  Google Scholar 

  109. Ishii J, Okazaki F, Djohan AC, Hara KY, Asai-Nakashima N, Teramura H, Kondo A (2016) From mannan to bioethanol: cell surface co-display of beta-mannanase and beta-mannosidase on yeast Saccharomyces cerevisiae. Biotechnol Biofuels 9:188

    Article  PubMed  PubMed Central  Google Scholar 

  110. Apiwatanapiwat W, Murata Y, Kosugi A, Yamada R, Kondo A, Arai T, Mori Y (2011) Direct ethanol production from cassava pulp using a surface-engineered yeast strain co-displaying two amylases, two cellulases, and β-glucosidase. Appl Microbiol Biotechnol 90(1):377–384

    Article  CAS  PubMed  Google Scholar 

  111. Bae J, Kuroda K, Ueda M (2014) Proximity effect among cellulose-degrading enzymes displayed on the Saccharomyces cerevisiae cell surface. Appl Environ Microbiol 81(1):59–66

    Article  PubMed  PubMed Central  Google Scholar 

  112. Chen L, Du J, Zhan Y, Li J, Zuo R, Tian S (2018) Consolidated bioprocessing for cellulosic ethanol conversion by cellulase–xylanase cell-surfaced yeast consortium. Prep Biochem Biotechnol 48(7):653–661

    Article  CAS  PubMed  Google Scholar 

  113. Guirimand G, Inokuma K, Bamba T, Matsuda M, Morita K, Sasaki K, Kondo A (2019) Cell-surface display technology and metabolic engineering of Saccharomyces cerevisiae for enhancing xylitol production from woody biomass. Green Chemistry 21(7):1795–1808

    Article  CAS  Google Scholar 

  114. Inokuma K, Yoshida T, Ishii J, Hasunuma T, Kondo A (2015) Efficient co-displaying and artificial ratio control of α-amylase and glucoamylase on the yeast cell surface by using combinations of different anchoring domains. Appl Microbiol Biotechnol 99(4):1655–1663

    Article  CAS  PubMed  Google Scholar 

  115. Yan Y, Xu L, Dai M (2012) A synergetic whole-cell biocatalyst for biodiesel production. Rsc Adv 2(15):6170–6173

    Article  CAS  Google Scholar 

  116. Liang B, Lang Q, Tang X, Liu A (2013) Simultaneously improving stability and specificity of cell surface displayed glucose dehydrogenase mutants to construct whole-cell biocatalyst for glucose biosensor application. Biores Technol 147:492–498

    Article  CAS  Google Scholar 

  117. Bae J, Morisaka H, Kuroda K, Ueda M (2013) Cellulosome complexes: natural biocatalysts as arming microcompartments of enzymes. J Mol Microbiol Biotechnol 23(4–5):370–378

    CAS  PubMed  Google Scholar 

  118. Hyeon JE, Shin SK, Han SO (2016) Design of nanoscale enzyme complexes based on various scaffolding materials for biomass conversion and immobilization. Biotechnol J 11(11):1386–1396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Han Z, Zhang B, Wang YE, Zuo YY, Su WW (2012) Self-assembled amyloid-like oligomeric-cohesin scaffoldin for augmented protein display on the Saccharomyces cerevisiae cell surface. Appl Environ Microbiol 78(9):3249–3255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Beguin P, Lemaire M (1996) The cellulosome: an exocellular, multiprotein complex specialized in cellulose degradation. Crit Rev Biochem Mol Biol 31(3):201–236

    Article  CAS  PubMed  Google Scholar 

  121. Felix C, Ljungdahl L (1993) The cellulosome—the exocellular organelle of clostridium. Annu Rev Microbiol 47:791–819

    Article  CAS  PubMed  Google Scholar 

  122. Fierobe H, Mingardon F, Mechaly A, Bélaïch A, Rincon MT, Pagès S, Bayer EA (2005) Action of designer cellulosomes on homogeneous Versuscomplex substrates: controlled incorporation of three distinct enzymes into a defined trifunctional scaffoldin. J Biol Chem 280(16):16325–16334

    Article  CAS  PubMed  Google Scholar 

  123. Doi RH, Kosugi A (2004) Cellulosomes: plant-cell-wall-degrading enzyme complexes. Nat Rev Microbiol 2(7): 541–551.

  124. Demain A, Newcomb M, Wu J (2005) Cellulase, clostridia, and ethanol. Microbiol Mol Biol Rev 69(1):124–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Fan LH, Zhang ZJ, Yu XY, Xue YX, Tan TW (2012) Self-surface assembly of cellulosomes with two miniscaffoldins on Saccharomyces cerevisiae for cellulosic ethanol production. Proc Natl Acad Sci 109(33):13260–13265

    Article  CAS  PubMed  Google Scholar 

  126. Wen F, Sun J, Zhao H (2010) Yeast surface display of trifunctional minicellulosomes for simultaneous saccharification and fermentation of cellulose to ethanol. Appl Environ Microbiol 76(4):1251–1260

    Article  CAS  PubMed  Google Scholar 

  127. Tsai SL, Goyal G, Chen W (2010) Surface display of a functional minicellulosome by intracellular complementation using a synthetic yeast consortium and its application to cellulose hydrolysis and ethanol production. Appl Environ Microbiol 76(22):7514–7520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Tsai S, DaSilva NA, Chen W (2013) Functional display of complex cellulosomes on the yeast surface via adaptive assembly. Acs Synthetic Biol 2(1):14–21

    Article  CAS  Google Scholar 

  129. Liang Y, Si T, Ang EL, Zhao H (2014) Engineered pentafunctional minicellulosome for simultaneous saccharification and ethanol fermentation in Saccharomyces cerevisiae. Appl Environ Microbiol 80(21):6677–6684

    Article  PubMed  PubMed Central  Google Scholar 

  130. Kim S, Baek S, Lee K, Hahn J (2013) Cellulosic ethanol production using a yeast consortium displaying a minicellulosome and beta-glucosidase. Microb Cell Fact 12:14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Tang H, Wang J, Wang S, Shen Y, Petranovic D, Hou J, Bao X (2018) Efficient yeast surface-display of novel complex synthetic cellulosomes. Microb Cell Fact 17(1):122

    Article  PubMed  PubMed Central  Google Scholar 

  132. Dong C, Qiao J, Wang X, Sun W, Chen L, Li S, Liu Y (2020) Engineering Pichia pastoris with surface-display minicellulosomes for carboxymethyl cellulose hydrolysis and ethanol production. Biotechnolo Biofuels 13:108

    Article  CAS  Google Scholar 

  133. Anandharaj M, Lin Y, Rani RP, Nadendla EK, Ho M, Huang C, Li W (2019) Constructing a yeast to express the largest cellulosome complex on the cell surface. Proc Natl Acad Sci USA 117(5):2385–2394

    Article  Google Scholar 

  134. den Haan R, Kroukamp H, van Zyl JD, van Zyl WH (2013) Cellobiohydrolase secretion by yeast: current state and prospects for improvement. Process Biochem 48(1):1–12

    Article  Google Scholar 

  135. Bertrand B, Trejo-Hernández MR, Morales-Guzmán D, Caspeta L, Suárez Rodríguez R, Martínez-Morales F (2016) Functional expression, production, and biochemical characterization of a laccase using yeast surface display technology. Fungal Biol 120(12):1609–1622

    Article  CAS  PubMed  Google Scholar 

  136. Tang H, Song M, He Y, Wang J, Wang S, Shen Y, Bao X (2017) Engineering vesicle trafficking improves the extracellular activity and surface display efficiency of cellulases in Saccharomyces cerevisiae. Biotechnol Biofuels 10(1):53

    Article  PubMed  PubMed Central  Google Scholar 

  137. Sato N, Matsumoto T, Ueda M, Tanaka A, Fukuda H, Kondo A (2002) Long anchor using Flo1 protein enhances reactivity of cell surface-displayed glucoamylase to polymer substrates. Appl Microbiol Biotechnol 60(4):469–474

    Article  CAS  PubMed  Google Scholar 

  138. Tanino T, Fukuda H, Kondo A (2006) Construction of a Pichia pastoris cell-surface display system using Flo1p anchor system. Biotechnol Prog 22(4):989–993

    Article  CAS  PubMed  Google Scholar 

  139. Washida M, Takahashi S, Ueda M, Tanaka A (2001) Spacer-mediated display of active lipase on the yeast cell surface. Appl Microbiol Biotechnol 56(5–6):681–686

    Article  CAS  PubMed  Google Scholar 

  140. Matsuoka H, Hashimoto K, Saijo A, Takada Y, Kondo A, Ueda M, Azuma M (2014) Cell wall structure suitable for surface display of proteins in Saccharomyces cerevisiae. Yeast 31(2):67–76

    Article  CAS  PubMed  Google Scholar 

  141. Wentz AE, Shusta EV (2007) A novel high-throughput screen reveals yeast genes that increase secretion of heterologous proteins. Appl Environ Microbiol 73(4):1189–1198

    Article  CAS  PubMed  Google Scholar 

  142. Bamba T, Inokuma K, Hasunuma T, Kondo A (2018) Enhanced cell-surface display of a heterologous protein using SED1 anchoring system in SED1-disrupted Saccharomyces cerevisiae strain. J Biosci Bioeng 125(3):306–310

    Article  CAS  PubMed  Google Scholar 

  143. Fan S, Liang B, Xiao X, Bai L, Tang X, Lojou E, Liu A (2020) Controllable display of sequential enzymes on yeast surface with enhanced biocatalytic activity toward efficient enzymatic biofuel cells. J Am Chem Soc 142(6):3222–3230

    Article  CAS  PubMed  Google Scholar 

  144. Rao B, Zhou R, Dong Q, Liao X, Liu F, Chen W, Wang Y (2020) Efficient surface display of l-glutamate oxidase and l-amino acid oxidase on Pichia pastorisusing multi-copy expression strains. Biotechnol Bioprocess Eng 25(4):571–579

    Article  CAS  Google Scholar 

  145. Smith SP, Bayer EA, Czjzek M (2017) Continually emerging mechanistic complexity of the multi-enzyme cellulosome complex. Curr Opin Struct Biol 44:151–160

    Article  CAS  PubMed  Google Scholar 

  146. Li S, Qiao J, Lin S, Liu Y, Ma L (2019) A highly efficient indirect P. pastoris surface display method based on the CL7/Im7 ultra-high-affinity system. Molecules (Basel, Switzerland) 24(8): 1483.

  147. Puthenveetil S, Liu DS, White KA, Thompson S, Ting AY (2009) Yeast display evolution of a kinetically efficient 13-amino acid substrate for lipoic acid ligase. J Am Chem Soc 131(45):16430–16438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Andreu C, Olmo MD (2013) Yeast arming by the Aga2p system: effect of growth conditions in galactose on the efficiency of the display and influence of expressing leucine-containing peptides. Appl Microbiol Biotechnol 97(20):9055–9069

    Article  CAS  PubMed  Google Scholar 

  149. Blazic M, Kovacevic G, Prodanovic O, Ostafe R, Gavrovic-Jankulovic M, Fischer R, Prodanovic R (2013) Yeast surface display for the expression, purification and characterization of wild-type and B11 mutant glucose oxidases. Protein Expr Purif 89(2):175–180

    Article  CAS  PubMed  Google Scholar 

  150. Madzak C, Otterbein L, Chamkha M, Moukha S, Asther M, Gaillardin C, Beckerich J (2005) Heterologous production of a laccase from the basidiomycete in the dimorphic yeast. FEMS Yeast Res 5(6–7):635–646

    Article  CAS  PubMed  Google Scholar 

  151. Görgens JF, Planas J, van Zyl WH, Knoetze JH, Hahn-Hägerdal B (2004) Comparison of three expression systems for heterologous xylanase production by S. cerevisiae in defined medium. Yeast 21(14): 1205–1217.

  152. Zhang J, Reddy J, Buckland B, Greasham R (2003) Toward consistent and productive complex media for industrial fermentations: Studies on yeast extract for a recombinant yeast fermentation process. Biotechnol Bioeng 82(6):640–652

    Article  CAS  PubMed  Google Scholar 

  153. Aguilar-Uscanga B, Francois JM (2003) A study of the yeast cell wall composition and structure in response to growth conditions and mode of cultivation. Lett Appl Microbiol 37(3):268–274

    Article  CAS  PubMed  Google Scholar 

  154. Anita K, Ester F, Ľudovít V, Martin S (2009) Spontaneous and protein-induced secretion of proteinases from Saccharomyces cerevisiae. J Basic Microbiol 49(6):542–552

    Google Scholar 

  155. Hackel BJ, Huang D, Bubolz JC, Wang XX, Shusta EV (2006) Production of soluble and active transferrin receptor-targeting single-chain antibody using Saccharomyces cerevisiae. Pharm Res 23(4):790–797

    Article  CAS  PubMed  Google Scholar 

  156. Dong M, Gong Y, Guo J, Ma J, Li S, Li T (2020) Optimization of production conditions of rice α-galactosidase II displayed on yeast cell surface. Protein Expr Purif 171:105611

    Article  CAS  PubMed  Google Scholar 

  157. Guirimand G, Sasaki K, Inokuma K, Bamba T, Hasunuma T, Kondo A (2016) Cell surface engineering of Saccharomyces cerevisiae combined with membrane separation technology for xylitol production from rice straw hydrolysate. Appl Microbiol Biotechnol 100(8):3477–3487

    Article  CAS  PubMed  Google Scholar 

  158. Nakanishi A, Bae JG, Fukai K, Tokumoto N, Kuroda K, Ogawa J, Ueda M (2012) Effect of pretreatment of hydrothermally processed rice straw with laccase-displaying yeast on ethanol fermentation. Appl Microbiol Biotechnol 94(4):939–948

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by Postdoctoral Science Foundation of China (2016M590631) and Postdoctoral innovation Project in Shandong Province of China (201603034).

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  1. Marine College, Shandong University, Weihai, 264209, China

    Mengqi Ye, Yuqi Ye, Zongjun Du & Guanjun Chen

  2. State Key Laboratory of Microbial Technology, Shandong University, Qingdao, 266237, China

    Zongjun Du & Guanjun Chen

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Ye, M., Ye, Y., Du, Z. et al. Cell-surface engineering of yeasts for whole-cell biocatalysts. Bioprocess Biosyst Eng 44, 1003–1019 (2021). https://doi.org/10.1007/s00449-020-02484-5

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