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Cell surface protein engineering for high-performance whole-cell catalysts

  • Hajime Nakatani
  • Katsutoshi Hori
Review Article

Abstract

Cell surface protein engineering facilitated by accumulation of information on genome and protein structure involves heterologous production and modification of cell surface proteins using genetic engineering, and is important for the development of high-performance whole-cell catalysts. In this field, cell surface display is a major technology by exposing target proteins, such as enzymes, on the cell surface using a carrier protein. The target proteins are fused to the carrier proteins that transport and tether them to the cell surface, as well as to a secretion signal. This paper reviews cell surface display systems for prokaryotic and eukaryotic cells from the perspective of carrier proteins, which determine the number of displayed molecules, and the localization, size, and direction (N- or C-terminal anchoring) of the passengers. We also discuss advanced methods for displaying multiple enzymes and a new method for the immobilization of whole-cell catalysts using adhesive surface proteins.

Keywords

cell surface engineering surface display whole-cell catalysts bioprocess 

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References

  1. 1.
    Liljeqvist S, Samuelson P, Hansson M, Nguyen T N, Binz H, Stahl S. Surface display of the cholera toxin B subunit on Staphylococcus xylosus and Staphylococcus carnosus. Applied and Environmental Microbiology, 1997, 63(7): 2481–2488PubMedPubMedCentralGoogle Scholar
  2. 2.
    Lee J S, Shin K S, Pan J G, Kim C J. Surface-displayed viral antigens on Salmonella carrier vaccine. Nature Biotechnology, 2000, 18(6): 645–648CrossRefPubMedGoogle Scholar
  3. 3.
    Martineau P, Charbit A, Leclerc C, Werts C, O’Callaghan D, Hofnung M. A genetic system to elicit and monitor antipeptide antibodies without peptide synthesis. Bio/Technology, 1991, 9(2): 170–172PubMedGoogle Scholar
  4. 4.
    Westerlund-Wikstrom B, Tanskanen J, Virkola R, Hacker J, Lindberg M, Skurnik M, Korhonen T K. Functional expression of adhesive peptides as fusions to Escherichia coli flagellin. Protein Engineering, 1997, 10(11): 1319–1326CrossRefPubMedGoogle Scholar
  5. 5.
    Boder E T, Wittrup K D. Yeast surface display for screening combinatorial polypeptide libraries. Nature Biotechnology, 1997, 15(6): 553–557CrossRefPubMedGoogle Scholar
  6. 6.
    Xu Z, Lee S Y. Display of polyhistidine peptides on the Escherichia coli cell surface by using outer membrane protein C as an anchoring motif. Applied and Environmental Microbiology, 1999, 65(11): 5142–5147PubMedPubMedCentralGoogle Scholar
  7. 7.
    Sousa C, Kotrba P, Ruml T, Cebolla A, De Lorenzo V. Metalloadsorption by Escherichia coli cells displaying yeast and mammalian metallothioneins anchored to the outer membrane protein LamB. Journal of Bacteriology, 1998, 180(9): 2280–2284PubMedPubMedCentralGoogle Scholar
  8. 8.
    Bae W, Mulchandani A, Chen W. Cell surface display of synthetic phytochelatins using ice nucleation protein for enhanced heavy metal bioaccumulation. Journal of Inorganic Biochemistry, 2002, 88(2): 223–227CrossRefPubMedGoogle Scholar
  9. 9.
    Liu C, Yang B, Gan J, Zhang Y, Liang M, Shu X, Shu J. Heterogeneous reactions of suspended parathion, malathion, and fenthion particles with NO(3) radicals. Chemosphere, 2012, 87(5): 470–476CrossRefPubMedGoogle Scholar
  10. 10.
    Smith G P. Filamentous fusion phage: Novel expression vectors that display cloned antigens on the virion surface. Science, 1985, 228(4705): 1315–1317CrossRefPubMedGoogle Scholar
  11. 11.
    Li M. Applications of display technology in protein analysis. Nature Biotechnology, 2000, 18(12): 1251–1256CrossRefPubMedGoogle Scholar
  12. 12.
    Freudl R, MacIntyre S, Degen M, Henning U. Cell surface exposure of the outer membrane protein OmpA of Escherichia coli K-12. Journal of Molecular Biology, 1986, 188(3): 491–494CrossRefPubMedGoogle Scholar
  13. 13.
    Ishikawa M, Shigemori K, Hori K. Application of the adhesive bacterionanofiber AtaA to a novel microbial immobilization method for the production of indigo as a model chemical. Biotechnology and Bioengineering, 2014, 111(1): 16–24CrossRefPubMedGoogle Scholar
  14. 14.
    Hori K, Ohara Y, Ishikawa M, Nakatani H. Effectiveness of direct immobilization of bacterial cells onto material surfaces using the bacterionanofiber protein AtaA. Applied Microbiology and Biotechnology, 2015, 99(12): 5025–5032CrossRefPubMedGoogle Scholar
  15. 15.
    Xu X, Gao C, Zhang X, Che B, Ma C, Qiu J, Tao F, Xu P. Production of N-acetyl-d-neuraminic acid by use of an efficient spore surface display system. Applied and Environmental Microbiology, 2011, 77(10): 3197–3201CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Smith M R, Khera E, Wen F. Engineering novel and improved biocatalysts by cell surface display. Industrial & Engineering Chemistry Research, 2015, 54(16): 4021–4032CrossRefGoogle Scholar
  17. 17.
    Beerli R R, Bauer M, Buser R B, Gwerder M, Muntwiler S, Maurer P, Saudan P, Bachmann M F. Isolation of human monoclonal antibodies by mammalian cell display. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(38): 14336–14341CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Ernst W, Grabherr R, Wegner D, Borth N, Grassauer A, Katinger H. Baculovirus surface display: Construction and screening of a eukaryotic epitope library. Nucleic Acids Research, 1998, 26(7): 1718–1723CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Schneewind O, Missiakas D M. Protein secretion and surface display in Gram-positive bacteria. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 2012, 367(1592): 1123–1139CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    van Bloois E, Winter R T, Kolmar H, Fraaije M W. Decorating microbes: Surface display of proteins on Escherichia coli. Trends in Biotechnology, 2011, 29(2): 79–86CrossRefPubMedGoogle Scholar
  21. 21.
    Levin A M, Weiss G A. Optimizing the affinity and specificity of proteins with molecular display. Molecular BioSystems, 2006, 2(1): 49–57CrossRefPubMedGoogle Scholar
  22. 22.
    Francisco J A, Earhart C F, Georgiou G. Transport and anchoring of beta-lactamase to the external surface of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 1992, 89(7): 2713–2717CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Francisco J A, Campbell R, Iverson B L, Georgiou G. Production and fluorescence-activated cell sorting of Escherichia coli expressing a functional antibody fragment on the external surface. Proceedings of the National Academy of Sciences of the United States of America, 1993, 90(22): 10444–10448CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Francisco J A, Stathopoulos C, Warren R A, Kilburn D G, Georgiou G. Specific adhesion and hydrolysis of cellulose by intact Escherichia coli expressing surface anchored cellulase or cellulose binding domains. Bio/Technology, 1993, 11(4): 491–495PubMedGoogle Scholar
  25. 25.
    Wei W, Liu X, Sun P, Wang X, Zhu H, Hong M, Mao Z W, Zhao J. Simple whole-cell biodetection and bioremediation of heavy metals based on an engineered lead-specific operon. Environmental Science & Technology, 2014, 48(6): 3363–3371CrossRefGoogle Scholar
  26. 26.
    Yang C, Zhao Q, Liu Z, Li Q, Qiao C, Mulchandani A, Chen W. Cell surface display of functional macromolecule fusions on Escherichia coli for development of an autofluorescent whole-cell biocatalyst. Environmental Science & Technology, 2008, 42(16): 6105–6110CrossRefGoogle Scholar
  27. 27.
    Qu W, Xue Y, Ding Q. Display of fungi xylanase on Escherichia coli cell surface and use of the enzyme in xylan biodegradation. Current Microbiology, 2015, 70(6): 779–785CrossRefPubMedGoogle Scholar
  28. 28.
    Richins R D, Kaneva I, Mulchandani A, Chen W. Biodegradation of organophosphorus pesticides by surface-expressed organophosphorus hydrolase. Nature Biotechnology, 1997, 15(10): 984–987CrossRefPubMedGoogle Scholar
  29. 29.
    Jung H C, Lebeault J M, Pan J G. Surface display of Zymomonas mobilis levansucrase by using the ice-nucleation protein of Pseudomonas syringae. Nature Biotechnology, 1998, 16(6): 576–580CrossRefPubMedGoogle Scholar
  30. 30.
    Maurer J, Jose J, Meyer T F. Autodisplay: One-component system for efficient surface display and release of soluble recombinant proteins from Escherichia coli. Journal of Bacteriology, 1997, 179(3): 794–804CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Karami A, Latifi A M, Khodi S. Comparison of the organophosphorus hydrolase surface display using InaVN and Lpp-OmpA systems in Escherichia coli. Journal of Microbiology and Biotechnology, 2014, 24(3): 379–385CrossRefPubMedGoogle Scholar
  32. 32.
    Kawahara H. The structures and functions of ice crystal-controlling proteins from bacteria. Journal of Bioscience and Bioengineering, 2002, 94(6): 492–496CrossRefPubMedGoogle Scholar
  33. 33.
    Jung H C, Park J H, Park S H, Lebeault J M, Pan J G. Expression of carboxymethylcellulase on the surface of Escherichia coli using Pseudomonas syringae ice nucleation protein. Enzyme and Microbial Technology, 1998, 22(5): 348–354CrossRefPubMedGoogle Scholar
  34. 34.
    van Bloois E, Winter R T, Janssen D B, Fraaije M W. Export of functional Streptomyces coelicolor alditol oxidase to the periplasm or cell surface of Escherichia coli and its application in whole-cell biocatalysis. Applied Microbiology and Biotechnology, 2009, 83(4): 679–687CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Yim S K, Jung H C, Pan J G, Kang H S, Ahn T, Yun C H. Functional expression of mammalian NADPH-cytochrome P450 oxidoreductase on the cell surface of Escherichia coli. Protein Expression and Purification, 2006, 49(2): 292–298CrossRefPubMedGoogle Scholar
  36. 36.
    Yim S K, Kim D H, Jung H C, Pan J G, Kang H S, Ahn T, Yun C H. Surface display of heme-and diflavin-containing cytochrome P450 BM3 in Escherichia coli: A whole cell biocatalyst for oxidation. Journal of Microbiology and Biotechnology, 2010, 20(4): 712–717CrossRefPubMedGoogle Scholar
  37. 37.
    Benz I, Schmidt M A. Structures and functions of autotransporter proteins in microbial pathogens. International Journal of Medical Microbiology, 2011, 301(6): 461–468CrossRefPubMedGoogle Scholar
  38. 38.
    Leo J C, Grin I, Linke D. Type V secretion: Mechanism(s) of autotransport through the bacterial outer membrane. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 2012, 367(1592): 1088–1101CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Nicolay T, Vanderleyden J, Spaepen S. Autotransporter-based cell surface display in Gram-negative bacteria. Critical Reviews in Microbiology, 2013, 41(1): 109–123CrossRefPubMedGoogle Scholar
  40. 40.
    Jose J, Meyer T F. The autodisplay story, from discovery to biotechnical and biomedical applications. Microbiology and Molecular Biology Reviews, 2007, 71(4): 600–619CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Detzel C, Maas R, Tubeleviciute A, Jose J. Autodisplay of nitrilase from Klebsiella pneumoniae and whole-cell degradation of oxynil herbicides and related compounds. Applied Microbiology and Biotechnology, 2013, 97(11): 4887–4896CrossRefPubMedGoogle Scholar
  42. 42.
    Jose J, von Schwichow S. Autodisplay of active sorbitol dehydrogenase (SDH) yields a whole cell biocatalyst for the synthesis of rare sugars. ChemBioChem, 2004, 5(4): 491–499CrossRefPubMedGoogle Scholar
  43. 43.
    Lattemann C T, Maurer J, Gerland E, Meyer T F. Autodisplay: Functional display of active beta-lactamase on the surface of Escherichia coli by the AIDA-I autotransporter. Journal of Bacteriology, 2000, 182(13): 3726–3733CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Schultheiss E, Weiss S, Winterer E, Maas R, Heinzle E, Jose J. Esterase autodisplay: Enzyme engineering and whole-cell activity determination in microplates with pH sensors. Applied and Environmental Microbiology, 2008, 74(15): 4782–4791CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Li C, Zhu Y, Benz I, Schmidt MA, Chen W, Mulchandani A, Qiao C. Presentation of functional organophosphorus hydrolase fusions on the surface of Escherichia coli by the AIDA-I autotransporter pathway. Biotechnology and Bioengineering, 2008, 99(2): 485–490CrossRefPubMedGoogle Scholar
  46. 46.
    Becker S, Theile S, Heppeler N, Michalczyk A, Wentzel A, Wilhelm S, Jaeger K E, Kolmar H. A generic system for the Escherichia coli cell-surface display of lipolytic enzymes. FEBS Letters, 2005, 579(5): 1177–1182CrossRefPubMedGoogle Scholar
  47. 47.
    Shanna S, Iasson E P, Tozakidis M, Teese J J. Maximized autotransporter-mediated expression (MATE) for surface display and secretion of recombinant proteins in Escherichia coli. Food Technology and Biotechnology, 2015, 50(3): 251–260Google Scholar
  48. 48.
    Tozakidis I E, Brossette T, Lenz F, Maas R M, Jose J. Proof of concept for the simplified breakdown of cellulose by combining Pseudomonas putida strains with surface displayed thermophilic endocellulase, exocellulase and beta-glucosidase. Microbial Cell Factories, 2016, 15(1): 103CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Crampton M, Berger E, Reid S, Louw M. The development of a flagellin surface display expression system in a moderate thermophile, Bacillus halodurans Alk36. Applied Microbiology and Biotechnology, 2007, 75(3): 599–607CrossRefPubMedGoogle Scholar
  50. 50.
    Pallesen L, Poulsen L K, Christiansen G, Klemm P. Chimeric FimH adhesin of type 1 fimbriae: A bacterial surface display system for heterologous sequences. Microbiology, 1995, 141(11): 2839–2848CrossRefPubMedGoogle Scholar
  51. 51.
    Ishikawa M, Nakatani H, Hori K. AtaA, a new member of the trimeric autotransporter adhesins from Acinetobacter sp. Tol 5 mediating high adhesiveness to various abiotic surfaces. PLoS One, 2012, 7(11): e48830CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Nummelin H, Merckel M C, Leo J C, Lankinen H, Skurnik M, Goldman A. The Yersinia adhesin YadA collagen-binding domain structure is a novel left-handed parallel beta-roll. EMBO Journal, 2004, 23(4): 701–711CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    O’Rourke F, Schmidgen T, Kaiser P O, Linke D, Kempf V A. Adhesins of Bartonella spp. Advances in Experimental Medicine and Biology, 2011, 715: 51–70CrossRefPubMedGoogle Scholar
  54. 54.
    Yoshimoto S, Nakatani H, Iwasaki K, Hori K. An Acinetobacter trimeric autotransporter adhesin reaped from cells exhibits its nonspecific stickiness via a highly stable 3D structure. Scientific Reports, 2016, 6: 28020CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Schneewind O, Mihaylova-Petkov D, Model P. Cell wall sorting signals in surface proteins of gram-positive bacteria. EMBO Journal, 1993, 12(12): 4803–4811PubMedPubMedCentralGoogle Scholar
  56. 56.
    Lee S Y, Choi J H, Xu Z. Microbial cell-surface display. Trends in Biotechnology, 2003, 21(1): 45–52CrossRefPubMedGoogle Scholar
  57. 57.
    Schreuder M P, Brekelmans S, van den Ende H, Klis F M. Targeting of a heterologous protein to the cell wall of Saccharomyces cerevisiae. Yeast (Chichester, England), 1993, 9(4): 399–409CrossRefGoogle Scholar
  58. 58.
    Pepper L R, Cho Y K, Boder E T, Shusta E V. A decade of yeast surface display technology: Where are we now? Combinatorial Chemistry & High Throughput Screening, 2008, 11(2): 127–134CrossRefGoogle Scholar
  59. 59.
    Kuroda K, Ueda M. Arming technology in yeast-novel strategy for whole-cell biocatalyst and protein engineering. Biomolecules, 2013, 3(3): 632–650CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Blazic M, Kovacevic G, Prodanovic O, Ostafe R, Gavrovic-Jankulovic M, Fischer R, Prodanovic R. Yeast surface display for the expression, purification and characterization of wild-type and B11 mutant glucose oxidases. Protein Expression and Purification, 2013, 89(2): 175–180CrossRefPubMedGoogle Scholar
  61. 61.
    Gera N, Hussain M, Rao B M. Protein selection using yeast surface display. Methods (San Diego, Calif.), 2013, 60(1): 15–26CrossRefGoogle Scholar
  62. 62.
    Tanaka T, Yamada R, Ogino C, Kondo A. Recent developments in yeast cell surface display toward extended applications in biotechnology. Applied Microbiology and Biotechnology, 2012, 95(3): 577–591CrossRefPubMedGoogle Scholar
  63. 63.
    Wen F, Sethi D K, Wucherpfennig K W, Zhao H. Cell surface display of functional human MHC class II proteins: Yeast display versus insect cell display. Protein Engineering, Design & Selection, 2011, 24(9): 701–709CrossRefGoogle Scholar
  64. 64.
    Yeasmin S, Kim C H, Park H J, Sheikh M I, Lee J Y, Kim J W, Back K K, Kim S H. Cell surface display of cellulase activity-free xylanase enzyme on Saccharomyces cerevisiae EBY100. Applied Biochemistry and Biotechnology, 2011, 164(3): 294–304CrossRefPubMedGoogle Scholar
  65. 65.
    Ueda M, Tanaka A. Cell surface engineering of yeast: Construction of arming yeast with biocatalyst. Journal of Bioscience and Bioengineering, 2000, 90(2): 125–136CrossRefPubMedGoogle Scholar
  66. 66.
    Kondo A, Shigechi H, Abe M, Uyama K, Matsumoto T, Takahashi S, Ueda M, Tanaka A, Kishimoto M, Fukuda H. High-level ethanol production from starch by a flocculent Saccharomyces cerevisiae strain displaying cell-surface glucoamylase. Applied Microbiology and Biotechnology, 2002, 58(3): 291–296CrossRefPubMedGoogle Scholar
  67. 67.
    Chen Y, Stemple B, Kumar M, Wei N. Cell surface display fungal laccase as a renewable biocatalyst for degradation of persistent micropollutants bisphenol A and sulfamethoxazole. Environmental Science & Technology, 2016, 50(16): 8799–8808CrossRefGoogle Scholar
  68. 68.
    He X, Shang J, Li F, Liu H. 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. Biotechnology and Applied Biochemistry, 2014, 62(1): 1–8CrossRefPubMedGoogle Scholar
  69. 69.
    Bony M, Thines-Sempoux D, Barre P, Blondin B. Localization and cell surface anchoring of the Saccharomyces cerevisiae flocculation protein Flo1p. Journal of Bacteriology, 1997, 179(15): 4929–4936CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Matsumoto T, Fukuda H, Ueda M, Tanaka A, Kondo A. Construction of yeast strains with high cell surface lipase activity by using novel display systems based on the Flo1p flocculation functional domain. Applied and Environmental Microbiology, 2002, 68(9): 4517–4522CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Han Z L, Han S Y, Zheng S P, Lin Y. Enhancing thermostability of a Rhizomucor miehei lipase by engineering a disulfide bond and displaying on the yeast cell surface. Applied Microbiology and Biotechnology, 2009, 85(1): 117–126CrossRefPubMedGoogle Scholar
  72. 72.
    Jiang Z B, Song H T, Gupta N, Ma L X, Wu Z B. Cell surface display of functionally active lipases from Yarrowia lipolytica in Pichia pastoris. Protein Expression and Purification, 2007, 56(1): 35–39CrossRefPubMedGoogle Scholar
  73. 73.
    Moura M V, da Silva G P, Machado A C, Torres F A, Freire D M, Almeida R V. 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, 2015, 10(10): e0141454CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Kondo A, Ueda M. Yeast cell-surface display—applications of molecular display. Applied Microbiology and Biotechnology, 2004, 64(1): 28–40CrossRefPubMedGoogle Scholar
  75. 75.
    Bauer F F, Govender P, Bester M C. Yeast flocculation and its biotechnological relevance. Applied Microbiology and Biotechnology, 2010, 88(1): 31–39CrossRefPubMedGoogle Scholar
  76. 76.
    Vallejo J A, Sanchez-Perez A, Martinez J P, Villa T G. Cell aggregations in yeasts and their applications. Applied Microbiology and Biotechnology, 2013, 97(6): 2305–2318CrossRefPubMedGoogle Scholar
  77. 77.
    Abe H, Ohba M, Shimma Y, Jigami Y. Yeast cells harboring human alpha-1,3-fucosyltransferase at the cell surface engineered using Pir, a cell wall-anchored protein. FEMS Yeast Research, 2004, 4(4-5): 417–425CrossRefPubMedGoogle Scholar
  78. 78.
    Abe H, Shimma Y, Jigami Y. In vitro oligosaccharide synthesis using intact yeast cells that display glycosyltransferases at the cell surface through cell wall-anchored protein Pir. Glycobiology, 2003, 13(2): 87–95CrossRefPubMedGoogle Scholar
  79. 79.
    Andres I, Gallardo O, Parascandola P, Javier Pastor F I, Zueco J. Use of the cell wall protein Pir4 as a fusion partner for the expression of Bacillus sp. BP-7 xylanase A in Saccharomyces cerevisiae. Biotechnology and Bioengineering, 2005, 89(6): 690–697CrossRefPubMedGoogle Scholar
  80. 80.
    Shimma Y, Saito F, Oosawa F, Jigami Y. Construction of a library of human glycosyltransferases immobilized in the cell wall of Saccharomyces cerevisiae. Applied and Environmental Microbiology, 2006, 72(11): 7003–7012CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Shi B, Ke X, Yu H, Xie J, Jia Y, Guo R. Novel properties for endoglucanase acquired by cell-surface display technique. Journal of Microbiology and Biotechnology, 2015, 25(11): 1856–1862CrossRefPubMedGoogle Scholar
  82. 82.
    Yuzbasheva E Y, Yuzbashev T V, Perkovskaya N I, Mostova E B, Vybornaya T V, Sukhozhenko A V, Toropygin I Y, Sineoky S P. Cell surface display of Yarrowia lipolytica lipase Lip2p using the cell wall protein YlPir1p, its characterization, and application as a whole-cell biocatalyst. Applied Biochemistry and Biotechnology, 2015, 175(8): 3888–3900CrossRefPubMedGoogle Scholar
  83. 83.
    Castillo L, Martinez A I, Garcera A, Elorza M V, Valentin E, Sentandreu R. Functional analysis of the cysteine residues and the repetitive sequence of Saccharomyces cerevisiae Pir4/Cis3: The repetitive sequence is needed for binding to the cell wall beta-1,3-glucan. Yeast (Chichester, England), 2003, 20(11): 973–983CrossRefGoogle Scholar
  84. 84.
    Ecker M, Deutzmann R, Lehle L, Mrsa V, Tanner W. Pir proteins of Saccharomyces cerevisiae are attached to beta-1,3-glucan by a new protein-carbohydrate linkage. Journal of Biological Chemistry, 2006, 281(17): 11523–11529CrossRefPubMedGoogle Scholar
  85. 85.
    Starwalt S E, Masteller E L, Bluestone J A, Kranz D M. Directed evolution of a single-chain class II MHC product by yeast display. Protein Engineering, 2003, 16(2): 147–156CrossRefPubMedGoogle Scholar
  86. 86.
    Yang N, Yu Z, Jia D, Xie Z, Zhang K, Xia Z, Lei L, Qiao M. The contribution of Pir protein family to yeast cell surface display. Applied Microbiology and Biotechnology, 2014, 98(7): 2897–2905CrossRefPubMedGoogle Scholar
  87. 87.
    Liu R, Yang C, Xu Y, Xu P, Jiang H, Qiao C. Development of a whole-cell biocatalyst/biosensor by display of multiple heterologous proteins on the Escherichia coli cell surface for the detoxification and detection of organophosphates. Journal of Agricultural and Food Chemistry, 2013, 61(32): 7810–7816CrossRefPubMedGoogle Scholar
  88. 88.
    Tang X, Liang B, Yi T, Manco G, Palchetti I, Liu A. Cell surface display of organophosphorus hydrolase for sensitive spectrophotometric detection of p-nitrophenol substituted organophosphates. Enzyme and Microbial Technology, 2014, 55: 107–112CrossRefPubMedGoogle Scholar
  89. 89.
    Yang J, Liu R, Jiang H, Yang Y, Qiao C. Selection of a whole-cell biocatalyst for methyl parathion biodegradation. Applied Microbiology and Biotechnology, 2012, 95(6): 1625–1632CrossRefPubMedGoogle Scholar
  90. 90.
    Chen X A, Ishida N, Todaka N, Nakamura R, Maruyama J, Takahashi H, Kitamoto K. Promotion of efficient saccharification of crystalline cellulose by Aspergillus fumigatus Swo1. Applied and Environmental Microbiology, 2010, 76(8): 2556–2561CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Arantes V, Saddler J N. Access to cellulose limits the efficiency of enzymatic hydrolysis: The role of amorphogenesis. Biotechnology for Biofuels, 2010, 3(1): 4CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Nakatani Y, Yamada R, Ogino C, Kondo A. Synergetic effect of yeast cell-surface expression of cellulase and expansin-like protein on direct ethanol production from cellulose. Microbial Cell Factories, 2013, 12(1): 66CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Hyeon J E, Jeon S D, Han S O. Cellulosome-based, Clostridium-derived multi-functional enzyme complexes for advanced biotechnology tool development: Advances and applications. Biotechnology Advances, 2013, 31(6): 936–944CrossRefPubMedGoogle Scholar
  94. 94.
    Schwarz W H. The cellulosome and cellulose degradation by anaerobic bacteria. Applied Microbiology and Biotechnology, 2001, 56(5-6): 634–649CrossRefPubMedGoogle Scholar
  95. 95.
    Wen F, Sun J, Zhao H. Yeast surface display of trifunctional minicellulosomes for simultaneous saccharification and fermentation of cellulose to ethanol. Applied and Environmental Microbiology, 2010, 76(4): 1251–1260CrossRefPubMedGoogle Scholar
  96. 96.
    Tsai S L, Oh J, Singh S, Chen R, Chen W. Functional assembly of minicellulosomes on the Saccharomyces cerevisiae cell surface for cellulose hydrolysis and ethanol production. Applied and Environmental Microbiology, 2009, 75(19): 6087–6093CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Liang Y, Si T, Ang E L, Zhao H. Engineered pentafunctional minicellulosome for simultaneous saccharification and ethanol fermentation in Saccharomyces cerevisiae. Applied and Environmental Microbiology, 2014, 80(21): 6677–6684CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    You C, Zhang X Z, Sathitsuksanoh N, Lynd L R, Zhang Y H. Enhanced microbial utilization of recalcitrant cellulose by an ex vivo cellulosome-microbe complex. Applied and Environmental Microbiology, 2012, 78(5): 1437–1444CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Lin Y, Tanaka S. Ethanol fermentation from biomass resources: Current state and prospects. Applied Microbiology and Biotechnology, 2006, 69(6): 627–642CrossRefPubMedGoogle Scholar
  100. 100.
    Dervakos G A, Webb C. On the merits of viable-cell immobilisation. Biotechnology Advances, 1991, 9(4): 559–612CrossRefPubMedGoogle Scholar
  101. 101.
    Junter G A, Jouenne T. Immobilized viable microbial cells: From the process to the proteome em leader or the cart before the horse. Biotechnology Advances, 2004, 22(8): 633–658CrossRefPubMedGoogle Scholar
  102. 102.
    Carballeira J D, Quezada M A, Hoyos P, Simeo Y, Hernaiz M J, Alcantara A R, Sinisterra J V. Microbial cells as catalysts for stereoselective red-ox reactions. Biotechnology Advances, 2009, 27(6): 686–714CrossRefPubMedGoogle Scholar
  103. 103.
    Cassidy M B, Lee H, Trevors J T. Environmental applications of immobilized microbial cells: A review. Journal of Industrial Microbiology, 1996, 16(2): 79–101CrossRefGoogle Scholar
  104. 104.
    Schaeffer C R, Woods K M, Longo G M, Kiedrowski MR, Paharik A E, Buttner H, Christner M, Boissy R J, Horswill A R, Rohde H, Fey P D. Accumulation-associated protein enhances Staphylococcus epidermidis biofilm formation under dynamic conditions and is required for infection in a rat catheter model. Infection and Immunity, 2015, 83(1): 214–226CrossRefPubMedGoogle Scholar
  105. 105.
    Cotter S E, Surana N K, StGeme J W 3rd. Trimeric autotransporters: A distinct subfamily of autotransporter proteins. Trends in Microbiology, 2005, 13(5): 199–205CrossRefPubMedGoogle Scholar
  106. 106.
    Hobley L, Harkins C, MacPhee C E, Stanley-Wall N R. Giving structure to the biofilm matrix: An overview of individual strategies and emerging common themes. FEMS Microbiology Reviews, 2015, 39(5): 649–669CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Ishikawa M, Shigemori K, Suzuki A, Hori K. Evaluation of adhesiveness of Acinetobacter sp. Tol 5 to abiotic surfaces. Journal of Bioscience and Bioengineering, 2012, 113(6): 719–725CrossRefPubMedGoogle Scholar

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© Higher Education Press and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Biotechnology, Graduate School of EngineeringNagoya UniversityNagoyaJapan

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