Facilitation of cascade biocatalysis by artificial multi-enzyme complexes—A review

doi:10.1016/j.cjche.2020.05.022

摘要/Abstract

摘要： Multi-enzyme complexes are the results of natural evolution to facilitate cascade biocatalysis. Through enzyme colocalization within a complex, the transfer efficiency of reaction intermediates between adjacent cascade enzymes can be promoted, resulting in enhanced overall reaction efficiency. Inspired by nature, a variety of approaches have been developed for the assembly of artificial multi-enzyme complexes with different spatial organizations, aiming at improving the catalytic efficiency of enzyme cascade. A recent trend of this research area is the creation of enzyme complexes with a controllable spatial organization which helps with the mechanistic studies and bears the potential to further increase metabolic productivity. In this review, we summarize versatile strategies for the assembly of artificial multi-enzyme complexes, followed by an inspection of the mechanistic studies of artificial multi-enzyme complexes for their enhancement of catalytic efficiency. Furthermore, we provide some highlighted in vivo, ex vivo, and in vitro examples that demonstrate the ability of artificial multi-enzyme complexes for enhancing the overall production efficiency of value-added compounds. Recent research progress has revealed the great biotechnological potential of artificial multi-enzyme complexes as a powerful tool for biomanufacturing.

关键词: Enzyme, Biocatalysis, Cascade reaction, scaffold, substrate channeling, synthetic biology

Abstract: Multi-enzyme complexes are the results of natural evolution to facilitate cascade biocatalysis. Through enzyme colocalization within a complex, the transfer efficiency of reaction intermediates between adjacent cascade enzymes can be promoted, resulting in enhanced overall reaction efficiency. Inspired by nature, a variety of approaches have been developed for the assembly of artificial multi-enzyme complexes with different spatial organizations, aiming at improving the catalytic efficiency of enzyme cascade. A recent trend of this research area is the creation of enzyme complexes with a controllable spatial organization which helps with the mechanistic studies and bears the potential to further increase metabolic productivity. In this review, we summarize versatile strategies for the assembly of artificial multi-enzyme complexes, followed by an inspection of the mechanistic studies of artificial multi-enzyme complexes for their enhancement of catalytic efficiency. Furthermore, we provide some highlighted in vivo, ex vivo, and in vitro examples that demonstrate the ability of artificial multi-enzyme complexes for enhancing the overall production efficiency of value-added compounds. Recent research progress has revealed the great biotechnological potential of artificial multi-enzyme complexes as a powerful tool for biomanufacturing.

Key words: Enzyme, Biocatalysis, Cascade reaction, scaffold, substrate channeling, synthetic biology

Xinlei Wei, Pingping Han, Chun You. Facilitation of cascade biocatalysis by artificial multi-enzyme complexes—A review[J]. 中国化学工程学报, 2020, 28(11): 2799-2809.

Xinlei Wei, Pingping Han, Chun You. Facilitation of cascade biocatalysis by artificial multi-enzyme complexes—A review[J]. Chinese Journal of Chemical Engineering, 2020, 28(11): 2799-2809.

参考文献

[1] U.T. Bornscheuer, G.W. Huisman, R.J. Kazlauskas, S. Lutz, J.C. Moore, K. Robins, Engineering the third wave of biocatalysis, Nature 485(7397) (2012) 185-194.
[2] J. Muschiol, C. Peters, N. Oberleitner, M.D. Mihovilovic, U.T. Bornscheuer, F. Rudroff, Cascade catalysis-strategies and challenges en route to preparative synthetic biology, Chem. Commun. (Cambridge, U. K.) 51(27) (2015) 5798-5811.
[3] J.H. Schrittwieser, S. Velikogne, M. Hall, W. Kroutil, Artificial biocatalytic linear cascades for preparation of organic molecules, Chem. Rev. 118(1) (2018) 270-348.
[4] J.M. Sperl, V. Sieber, Multienzyme cascade reactions-status and recent advances, ACS Catal. 8(3) (2018) 2385-2396.
[5] C. You, H. Chen, S. Myung, N. Sathitsuksanoh, H. Ma, X.Z. Zhang, J. Li, Y.-H.P. Zhang, Enzymatic transformation of nonfood biomass to starch, Proc. Natl. Acad. Sci. U. S. A. 110(18) (2013) 7182-7187.
[6] C. You, T. Shi, Y.J. Li, P.P. Han, X.G. Zhou, Y.-H.P. Zhang, An in vitro synthetic biology platform for the industrial biomanufacturing of myo-inositol from starch, Biotechnol. Bioeng. 114(8) (2017) 1855-1864.
[7] X. Luo, M.A. Reiter, L. d'Espaux, J. Wong, C.M. Denby, A. Lechner, Y. Zhang, A.T. Grzybowski, S. Harth, W. Lin, H. Lee, C. Yu, J. Shin, K. Deng, V.T. Benites, G. Wang, E.E.K. Baidoo, Y. Chen, I. Dev, C.J. Petzold, J.D. Keasling, Complete biosynthesis of cannabinoids and their unnatural analogues in yeast, Nature 567(7746) (2019) 123-126.
[8] M.A. Valliere, T.P. Korman, N.B. Woodall, G.A. Khitrov, R.E. Taylor, D. Baker, J.U. Bowie, A cell-free platform for the prenylation of natural products and application to cannabinoid production, Nat. Commun. 10(1) (2019) 565.
[9] J.K. Ko, S.M. Lee, Advances in cellulosic conversion to fuels:engineering yeasts for cellulosic bioethanol and biodiesel production, Curr. Opin. Biotechnol. 50(2017) 72-80.
[10] H.M. Kim, T.U. Chae, S.Y. Choi, W.J. Kim, S.Y. Lee, Engineering of an oleaginous bacterium for the production of fatty acids and fuels, Nat. Chem. Biol. 15(7) (2019) 721-729.
[11] T.O. Yeates, C.A. Kerfeld, S. Heinhorst, G.C. Cannon, J.M. Shively, Protein-based organelles in bacteria:carboxysomes and related microcompartments, Nat. Rev. Microbiol. 6(9) (2008) 681-691.
[12] J.C. Cameron, S.C. Wilson, S.L. Bernstein, C.A. Kerfeld, Biogenesis of a bacterial organelle:The carboxysome assembly pathway, Cell 155(5) (2013) 1131-1140.
[13] Z.H. Zhou, D.B. McCarthy, C.M. O'Connor, L.J. Reed, J.K. Stoops, The remarkable structural and functional organization of the eukaryotic pyruvate dehydrogenase complexes, Proc. Natl. Acad. Sci. U. S. A. 98(26) (2001) 14802-14807.
[14] M.S. Patel, N.S. Nemeria, W. Furey, F. Jordan, The pyruvate dehydrogenase complexes:Structure-based function and regulation, J. Biol. Chem. 289(24) (2014) 16615-16623.
[15] K. Jorgensen, A.V. Rasmussen, M. Morant, A.H. Nielsen, N. Bjarnholt, M. Zagrobelny, S. Bak, B.L. Moller, Metabolon formation and metabolic channeling in the biosynthesis of plant natural products, Curr. Opin. Plant Biol. 8(3) (2005) 280-291.
[16] P. Bauler, G. Huber, T. Leyh, J.A. McCammon, Channeling by proximity:the catalytic advantages of active site colocalization using Brownian dynamics, J. Phys. Chem. Lett. 1(9) (2010) 1332-1335.
[17] B. Bulutoglu, K.E. Garcia, F. Wu, S.D. Minteer, S. Banta, Direct evidence for metabolon formation and substrate channeling in recombinant TCA cycle enzymes, ACS Chem. Biol. 11(10) (2016) 2847-2853.
[18] E.W. Miles, S. Rhee, D.R. Davies, The molecular basis of substrate channeling, J. Biol. Chem. 274(18) (1999) 12193-12196.
[19] H.O. Spivey, J. Ovádi, Substrate channeling, Methods 19(2) (1999) 306-321.
[20] P.A. Srere, Complexes of sequential metabolic enzymes, Annu. Rev. Biochem. 56(1987) 89-124.
[21] R.J. Conrado, J.D. Varner, M.P. DeLisa, Engineering the spatial organization of metabolic enzymes:mimicking nature's synergy, Curr. Opin. Biotechnol. 19(5) (2008) 492-499.
[22] R.A. Sheldon, S. van Pelt, Enzyme immobilisation in biocatalysis:Why, what and how, Chem. Soc. Rev. 42(15) (2013) 6223-6235.
[23] L. Cao, F. van Rantwijk, R.A. Sheldon, Cross-linked enzyme aggregates:A simple and effective method for the immobilization of penicillin acylase, Org. Lett. 2(10) (2000) 1361-1364.
[24] N.L.St. Clair, M.A. Navia, Cross-linked enzyme crystals as robust biocatalysts, J. Am. Chem. Soc. 114(18) (1992) 7314-7316.
[25] S. Schoffelen, J. Beekwilder, M.F. Debets, D. Bosch, J.C. van Hest, Construction of a multifunctional enzyme complex via the strain-promoted azide-alkyne cycloaddition, Bioconjug. Chem. 24(6) (2013) 987-996.
[26] S. Shah, A. Sharma, M.N. Gupta, Preparation of cross-linked enzyme aggregates by using bovine serum albumin as a proteic feeder, Anal. Biochem. 351(2) (2006) 207-213.
[27] R.A. Scism, B.O. Bachmann, Five-component cascade synthesis of nucleotide analogues in an engineered self-immobilized enzyme aggregate, ChemBioChem 11(1) (2010) 67-70.
[28] C. Mateo, A. Chmura, S. Rustler, F. van Rantwijk, A. Stolz, R.A. Sheldon, Synthesis of enantiomerically pure (S)-mandelic acid using an oxynitrilase-nitrilase bienzymatic cascade:a nitrilase surprisingly shows nitrile hydratase activity, Tetrahedron Asymmetry 17(3) (2006) 320-323.
[29] J. Jegan Roy, T. Emilia Abraham, Strategies in making cross-linked enzyme crystals, Chem. Rev. 104(9) (2004) 3705-3722.
[30] I. Orita, H. Yurimoto, R. Hirai, Y. Kawarabayasi, Y. Sakai, N. Kato, The archaeon Pyrococcus horikoshii possesses a bifunctional enzyme for formaldehyde fixation via the ribulose monophosphate pathway, J. Bacteriol. 187(11) (2005) 3636-3642.
[31] I. Orita, T. Sato, H. Yurimoto, N. Kato, H. Atomi, T. Imanaka, Y. Sakai, The ribulose monophosphate pathway substitutes for the missing pentose phosphate pathway in the archaeon Thermococcus kodakaraensis, J. Bacteriol. 188(13) (2006) 4698-4704.
[32] I. Orita, N. Sakamoto, N. Kato, H. Yurimoto, Y. Sakai, Bifunctional enzyme fusion of 3-hexulose-6-phosphate synthase and 6-phospho-3-hexuloisomerase, Appl. Microbiol. Biotechnol. 76(2) (2007) 439-445.
[33] H.S. Seo, Y.J. Koo, J.Y. Lim, J.T. Song, C.H. Kim, J.K. Kim, J.S. Lee, Y.D. Choi, Characterization of a bifunctional enzyme fusion of trehalose-6-phosphate synthetase and trehalose-6-phosphate phosphatase of Escherichia coli, Appl. Environ. Microbiol. 66(6) (2000) 2484-2490.
[34] N. Adlakha, S. Sawant, A. Anil, A. Lali, S.S. Yazdani, Specific fusion of beta-1,4-endoglucanase and beta-1,4-glucosidase enhances cellulolytic activity and helps inchannelingofintermediates, Appl. Environ. Microbiol.78(20)(2012)7447-7454.
[35] H.L. Lee, C.K. Chang, K.H. Teng, P.H. Liang, Construction and characterization of different fusion proteins between cellulases and beta-glucosidase to improve glucose production and thermostability, Bioresour. Technol. 102(4) (2011) 3973-3976.
[36] M. Rizk, S. Elleuche, G. Antranikian, Generating bifunctional fusion enzymes composed of heat-active endoglucanase (Cel5A) and endoxylanase (XylT), Biotechnol. Lett. 37(1) (2015) 139-145.
[37] S.Y. Hong, J.S. Lee, K.M. Cho, R.K. Math, Y.H. Kim, S.J. Hong, Y.U. Cho, H. Kim, H.D. Yun, Assembling a novel bifunctional cellulase-xylanase from Thermotoga maritima by end-to-end fusion, Biotechnol. Lett. 28(22) (2006) 1857-1862.
[38] Y.M. Kim, E.A. Ko, H.K. Kang, D. Kim, Construction, expression and characterization of fusion enzyme from Arthrobacter oxydans dextranase and Klebsiella pneumoniae amylase, Biotechnol. Lett. 31(7) (2009) 1019-1024.
[39] K. Kufner, G. Lipps, Construction of a chimeric thermoacidophilic betaendoglucanase, BMC Biochem. 14(2013) 11.
[40] L.W. Fan, Y. Wang, P. Tuyishime, N. Gao, Q.G. Li, P. Zheng, J.B. Sun, Y.H. Ma, Engineering artificial fusion proteins for enhanced methanol bioconversion, ChemBioChem 19(23) (2018) 2465-2471.
[41] H.P. Fierobe, A. Mechaly, C. Tardif, A. Belaich, R. Lamed, Y. Shoham, J.P. Belaich, E.A. Bayer, Design and production of active cellulosome chimeras. Selective incorporation of dockerin-containing enzymes into defined functional complexes, J. Biol. Chem. 276(24) (2001) 21257-21261.
[42] R. Haimovitz, Y. Barak, E. Morag, M. Voronov-Goldman, Y. Shoham, R. Lamed, E.A. Bayer, Cohesin-dockerin microarray:diverse specificities between two complementary families of interacting protein modules, Proteomics 8(5) (2008) 968-979.
[43] W.R. Whitaker, J.E. Dueber, Metabolic pathway flux enhancement by synthetic protein scaffolding, Methods Enzymol. 497(2011) 447-468.
[44] L.A. Banaszynski, C.W. Liu, T.J. Wandless, Characterization of the FKBP.rapamycin. FRB ternary complex, J. Am. Chem. Soc. 127(13) (2005) 4715-4721.
[45] A.S. Kim, L.T. Kakalis, N. Abdul-Manan, G.A. Liu, M.K. Rosen, Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein, Nature 404(6774) (2000) 151-158.
[46] T. Thomik, I. Wittig, J.Y. Choe, E. Boles, M. Oreb, An artificial transport metabolon facilitates improved substrate utilization in yeast, Nat. Chem. Biol. 13(11) (2017) 1158-1163.
[47] T. Yu, X. Gao, Y.H. Ren, D.Z. Wei, Assembly of cellulases with synthetic protein scaffolds in vitro, Bioresour. Bioprocess. 2(1) (2015) 16.
[48] A. Acharya, S.B. Ruvinov, J. Gal, J.R. Moll, C. Vinson, A heterodimerizing leucine zipper coiled coil system for examining the specificity of a position interactions:Amino acids I, V, L, N, A, and K, Biochemistry 41(48) (2002) 14122-14131.
[49] J.R. Newman, A.E. Keating, Comprehensive identification of human bZIP interactions with coiled-coil arrays, Science 300(5628) (2003) 2097-2101.
[50] R. Tonikian, Y. Zhang, S.L. Sazinsky, B. Currell, J.H. Yeh, B. Reva, H.A. Held, B.A. Appleton, M. Evangelista, Y. Wu, X. Xin, A.C. Chan, S. Seshagiri, L.A. Lasky, C. Sander, C. Boone, G.D. Bader, S.S. Sidhu, A specificity map for the PDZ domain family, PLoS Biol. 6(9) (2008) e239.
[51] G. Posern, J. Zheng, B.S. Knudsen, C. Kardinal, K.B. Muller, J. Voss, T. Shishido, D. Cowburn, G. Cheng, B. Wang, G.D. Kruh, S.K. Burrell, C.A. Jacobson, D.M. Lenz, T.J. Zamborelli, K. Adermann, H. Hanafusa, S.M. Feller, Development of highly selective SH3 binding peptides for Crk and CRKL which disrupt Crk-complexes with DOCK180, SoS and C3G, Oncogene 16(15) (1998) 1903-1912.
[52] G. Veggiani, T. Nakamura, M.D. Brenner, R.V. Gayet, J. Yan, C.V. Robinson, M. Howarth, Programmable polyproteams built using twin peptide superglues, Proc. Natl. Acad. Sci. U. S. A. 113(5) (2016) 1202-1207.
[53] B. Zakeri, J.O. Fierer, E. Celik, E.C. Chittock, U. Schwarz-Linek, V.T. Moy, M. Howarth, Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin, Proc. Natl. Acad. Sci. U. S. A. 109(12) (2012) E690-E697.
[54] S. Voss, A. Skerra, Mutagenesis of a flexible loop in streptavidin leads to higher affinity for the strep-tag Ⅱ peptide and improved performance in recombinant protein purification, Protein Eng. 10(8) (1997) 975-982.
[55] T.G.M. Schmidt, A. Skerra, The Strep-tag system for one-step purification and highaffinity detection or capturing of proteins, Nat. Protoc. 2(2007) 1528.
[56] B.Z. Harris, W.A. Lim, Mechanism and role of PDZ domains in signaling complex assembly, J. Cell Sci. 114(Pt 18) (2001) 3219-3231.
[57] M. Sheng, C. Sala, PDZ domains and the organization of supramolecular complexes, Annu. Rev. Neurosci. 24(2001) 1-29.
[58] X. Gao, S. Yang, C. Zhao, Y. Ren, D. Wei, Artificial multienzyme supramolecular device:Highly ordered self-assembly of oligomeric enzymes in vitro and in vivo, Angew. Chem. Int. Ed. Engl. 53(51) (2014) 14027-14030.
[59] W.H. Landschulz, P.F. Johnson, S.L. McKnight, The leucine zipper:A hypothetical structure common to A new class of DNA binding proteins, Science 240(4860) (1988) 1759-1764.
[60] H. Robson Marsden, A. Kros, Self-assembly of coiled coils in synthetic biology:Inspiration and progress, Angew. Chem. Int. Ed. Engl. 49(17) (2010) 2988-3005.
[61] Y.H. Kim, E. Campbell, J. Yu, S.D. Minteer, S. Banta, Complete oxidation of methanol in biobattery devices using a hydrogel created from three modified dehydrogenases, Angew. Chem. Int. Ed. 52(5) (2013) 1437-1440.
[62] A.N. Lupas, J. Bassler, Coiled coils-A model system for the 21st century, Trends Biochem. Sci. 42(2) (2017) 130-140.
[63] A.W. Reinke, R.A. Grant, A.E. Keating, A synthetic coiled-coil interactome provides heterospecific modules for molecular engineering, J. Am. Chem. Soc. 132(17) (2010) 6025-6031.
[64] H.F. Ozbakir, K.E. Garcia, S. Banta, Creation of a formate:Malate oxidoreductase by fusion of dehydrogenase enzymes with PEGylated cofactor swing arms, Protein Eng. Des. Sel. 31(4) (2018) 103-108.
[65] F. Liu, S. Banta, W. Chen, Functional assembly of a multi-enzyme methanol oxidation cascade on a surface-displayed trifunctional scaffold for enhanced NADH production, Chem. Commun. 49(36) (2013) 3766-3768.
[66] J. Fu, M. Liu, Y. Liu, H. Yan, Spatially-interactive biomolecular networks organized by nucleic acid nanostructures, Acc. Chem. Res. 45(8) (2012) 1215-1226.
[67] Y.F. Zhang, H. Hess, Toward rational design of high-efficiency enzyme cascades, ACS Catal. 7(9) (2017) 6018-6027.
[68] T.A. Ngo, E. Nakata, M. Saimura, T. Morii, Spatially organized enzymes drive cofactor-coupled cascade reactions, J. Am. Chem. Soc. 138(9) (2016) 3012-3021.
[69] O.I. Wilner, Y. Weizmann, R. Gill, O. Lioubashevski, R. Freeman, I. Willner, Enzyme cascades activated on topologically programmed DNA scaffolds, Nat. Nanotechnol. 4(4) (2009) 249-254.
[70] C.J. Delebecque, A.B. Lindner, P.A. Silver, F.A. Aldaye, Organization of intracellular reactions with rationally designed RNA assemblies, Science 333(6041) (2011) 470-474.
[71] H.P. Fierobe, E.A. Bayer, C. Tardif, M. Czjzek, A. Mechaly, A. Belaich, R. Lamed, Y. Shoham, J.P. Belaich, Degradation of cellulose substrates by cellulosome chimeras. Substrate targeting versus proximity of enzyme components, J. Biol. Chem. 277(51) (2002) 49621-49630.
[72] L. Davidi, S. Morais, L. Artzi, D. Knop, Y. Hadar, Y. Arfi, E.A. Bayer, Toward combined delignification and saccharification of wheat straw by a laccase-containing designer cellulosome, Proc. Natl. Acad. Sci. U. S. A. 113(39) (2016) 10854-10859.
[73] G. Gefen, M. Anbar, E. Morag, R. Lamed, E.A. Bayer, Enhanced cellulose degradation by targeted integration of a cohesin-fused beta-glucosidase into the Clostridium thermocellum cellulosome, Proc. Natl. Acad. Sci. U. S. A. 109(26) (2012) 10298-10303.
[74] S. Morais, Y. Barak, Y. Hadar, D.B. Wilson, Y. Shoham, R. Lamed, E.A. Bayer, Assembly of xylanases into designer cellulosomes promotes efficient hydrolysis of the xylan component of a natural recalcitrant cellulosic substrate, mBio 2(6) (2011) e00233-00211.
[75] J. Stern, A. Kahn, Y. Vazana, M. Shamshoum, S. Morais, R. Lamed, E.A. Bayer, Significance of relative position of cellulases in designer cellulosomes for optimized cellulolysis, PLoS One 10(5) (2015) e0127326.
[76] C.You,S.Myung,Y.-H.P. Zhang,Facilitatedsubstrate channelingina self-assembled trifunctional enzyme complex, Angew. Chem. Int. Ed. 51(35) (2012) 8787-8790.
[77] C. You, Y.H.P. Zhang, Self-assembly of synthetic metabolons through synthetic protein scaffolds:one-step purification, co-immobilization, and substrate channeling, ACS Synth. Biol. 2(2) (2013) 102-110.
[78] J.M. Baek, S. Mazumdar, S.W. Lee, M.Y. Jung, J.H. Lim, S.W. Seo, G.Y. Jung, M.K. Oh, Butyrate production in engineered Escherichia coli with synthetic scaffolds, Biotechnol. Bioeng. 110(10) (2013) 2790-2794.
[79] J.E. Dueber, G.C. Wu, G.R. Malmirchegini, T.S. Moon, C.J. Petzold, A.V. Ullal, K.L. Prather, J.D. Keasling, Synthetic protein scaffolds provide modular control over metabolic flux, Nat. Biotechnol. 27(8) (2009) 753-759.
[80] T.S. Moon, J.E. Dueber, E. Shiue, K.L. Prather, Use of modular, synthetic scaffolds for improved production of glucaric acid in engineered E. coli, Metab. Eng. 12(3) (2010) 298-305.
[81] S. Zhao, J.A. Jones, D.M. Lachance, N. Bhan, O. Khalidi, S. Venkataraman, Z. Wang, M.A. Koffas, Improvement of catechin production in Escherichia coli through combinatorial metabolic engineering, Metab. Eng. 28(2015) 43-53.
[82] G.J. Williams, K. Johnson, J. Rudolf, S.A. McMahon, L. Carter, M. Oke, H. Liu, G.L. Taylor, M.F. White, J.H. Naismith, Structure of the heterotrimeric PCNA from Sulfolobus solfataricus, Acta Crystallogr, Sect. F:Struct. Biol. Cryst. Commun. 62(Pt 10) (2006) 944-948.
[83] H. Hirakawa, A. Kakitani, T. Nagamune, Introduction of selective intersubunit disulfide bonds into self-assembly protein scaffold to enhance an artificial multienzyme complex's activity, Biotechnol. Bioeng. 110(7) (2013) 1858-1864.
[84] H. Hirakawa, T. Nagamune, Molecular assembly of P450 with ferredoxin and ferredoxin reductase by fusion to PCNA, ChemBioChem 11(11) (2010) 1517-1520.
[85] G.Q. Zhang, M.B. Quin, C. Schmidt-Dannert, Self-assembling protein scaffold system for easy in vitro coimmobilization of biocatalytic cascade enzymes, ACS Catal. 8(6) (2018) 5611-5620.
[86] G. Zhang, T. Johnston, M.B. Quin, C. Schmidt-Dannert, Developing a protein scaffolding system for rapid enzyme immobilization and optimization of enzyme functions for biocatalysis, ACS Synth. Biol. 8(8) (2019) 1867-1876.
[87] N.P. King, J.B. Bale, W. Sheffler, D.E. McNamara, S. Gonen, T. Gonen, T.O. Yeates, D. Baker, Accurate design of co-assembling multi-component protein nanomaterials, Nature 510(7503) (2014) 103-108.
[88] S.A. McConnell, K.A. Cannon, C. Morgan, R. McAllister, B.R. Amer, R.T. Clubb, T.O. Yeates, Designed protein cages as scaffolds for building multienzyme materials, ACS Synth. Biol. 9(2) (2020) 381-391.
[89] Y.Lu,F.Huang,J.Wang,J.Xia,Affinity-guided covalentconjugationreactionsbasedon PDZ-peptide and SH3-peptide interactions, Bioconjug. Chem. 25(5) (2014) 989-999.
[90] B. El-Zahab, D. Donnelly, P. Wang, Particle-tethered NADH for production of methanol from CO(2) catalyzed by coimmobilized enzymes, Biotechnol. Bioeng. 99(3) (2008) 508-514.
[91] F. Jia, B. Narasimhan, S.K. Mallapragada, Biomimetic multienzyme complexes based on nanoscale platforms, AIChE J. 59(2) (2013) 355-360.
[92] H. Qiu, Y. Li, G. Ji, G. Zhou, X. Huang, Y. Qu, P. Gao, Immobilization of lignin peroxidase on nanoporous gold:enzymatic properties and in situ release of H2O2 by co-immobilized glucose oxidase, Bioresour. Technol. 100(17) (2009) 3837-3842.
[93] J.D. Keighron, C.D. Keating, Enzyme:nanoparticle bioconjugates with two sequential enzymes:stoichiometry and activity of malate dehydrogenase and citrate synthase on Au nanoparticles, Langmuir 26(24) (2010) 18992-19000.
[94] R. Obert, B.C. Dave, Enzymatic conversion of carbon dioxide to methanol:enhanced methanol production in silica sol-gel matrices, J. Am. Chem. Soc. 121(51) (1999) 12192-12193.
[95] W. Liu, S. Zhang, P. Wang, Nanoparticle-supported multi-enzyme biocatalysis with in situ cofactor regeneration, J. Biotechnol. 139(1) (2009) 102-107.
[96] Y. Fang, H. Bullock, S.A. Lee, N. Sekar, M.A. Eiteman, W.B. Whitman, R.P. Ramasamy, Detection of methyl salicylate using bi-enzyme electrochemical sensor consisting salicylate hydroxylase and tyrosinase, Biosens. Bioelectron. 85(2016) 603-610.
[97] R. Yasujima, K. Yasueda, T. Horiba, S. Komaba, Multi-enzyme immobilized anodes utilizing maltose fuel for biofuel cell applications, ChemElectroChem 5(16) (2018) 2271-2278.
[98] F. Jia, Y. Zhang, B. Narasimhan, S.K. Mallapragada, Block copolymer-quantum dot micelles for multienzyme colocalization, Langmuir 28(50) (2012) 17389-17395.
[99] S.J. Chen, L.Y. Wen, F. Svec, T.W. Tan, Y.Q. Lv, Magnetic metal-organic frameworks as scaffolds for spatial co-location and positional assembly of multi-enzyme systems enabling enhanced cascade biocatalysis, RSC Adv. 7(34) (2017) 21205-21213.
[100] J. Luo, A.S. Meyer, R.V. Mateiu, M. Pinelo, Cascade catalysis in membranes with enzyme immobilization for multi-enzymatic conversion of CO₂ to methanol, New Biotechnol. 32(3) (2015) 319-327.
[101] K. Mosbach, B. Mattiasson, Matrix-bound enzymes. Ⅱ. Studies on a matrix-bound two-enzyme-system, Acta Chem. Scand. 24(6) (1970) 2093-2100.
[102] S. Talekar, A. Joshi, S. Kambale, S. Jadhav, S. Nadar, M. Ladole, A tri-enzyme magnetic nanobiocatalyst with one pot starch hydrolytic activity, Chem. Eng. J. 325(2017) 80-90.
[103] M. Yu, D. Liu, L. Sun, J. Li, Q. Chen, L. Pan, J. Shang, S. Zhang, W. Li, Facile fabrication of 3D porous hybrid sphere by co-immobilization of multi-enzyme directly from cell lysates as an efficient and recyclable biocatalyst for asymmetric reduction with coenzyme regeneration in situ, Int. J. Biol. Macromol. 103(2017) 424-434.
[104] C. Mukai, L.Z. Gao, J.L. Nelson, J.P. Lata, R. Cohen, L.R. Wu, M.M. Hinchman, M. Bergkvist, R.W. Sherwood, S. Zhang, A.J. Travis, Biomimicry promotes the efficiency of a 10-step sequential enzymatic reaction on nanoparticles, converting glucose to lactate, Angew. Chem. Int. Ed. 56(1) (2017) 235-238.
[105] C.Y. Tan, H. Hirakawa, R. Suzuki, T. Haga, F. Iwata, T. Nagamune, Immobilization of a bacterial cytochrome P450 monooxygenase system on a solid support, Angew. Chem. Int. Ed. 55(48) (2016) 15002-15006.
[106] A. Kuchler, J. Adamcik, R. Mezzenga, A.D. Schluter, P. Walde, Enzyme immobilization on silicate glass through simple adsorption of dendronized polymer-enzyme conjugates for localized enzymatic cascade reactions, RSC Adv. 5(55) (2015) 44530-44544.
[107] J. Ovadi, Physiological significance of metabolic channelling, J. Theor. Biol. 152(1) (1991) 1-22.
[108] H.O. Spivey, J.M. Merz, Metabolic compartmentation, Bioessays 10(4) (1989) 127-130.
[109] I. Wheeldon, S.D. Minteer, S. Banta, S.C. Barton, P. Atanassov, M. Sigman, Substrate channelling as an approach to cascade reactions, Nat. Chem. 8(4) (2016) 299-309.
[110] Y.-H.P. Zhang, Substrate channeling and enzyme complexes for biotechnological applications, Biotechnol. Adv. 29(6) (2011) 715-725.
[111] J.S. Easterby, A generalized theory of the transition time for sequential enzyme reactions, Biochem. J. 199(1) (1981) 155-161.
[112] J. Rudolph, J. Stubbe, Investigation of the mechanism of phosphoribosylamine transfer from glutamine phosphoribosylpyrophosphate amidotransferase to glycinamide ribonucleotide synthetase, Biochemistry 34(7) (1995) 2241-2250.
[113] M.K. Geck, J.F. Kirsch, A novel, definitive test for substrate channeling illustrated with the aspartate aminotransferase/malate dehydrogenase system, Biochemistry 38(25) (1999) 8032-8037.
[114] M.J. Dewar, D.M. Storch, Alternative view of enzyme reactions, Proc. Natl. Acad. Sci. U. S. A. 82(8) (1985) 2225-2229.
[115] J. Fu, Y.R. Yang, A. Johnson-Buck, M. Liu, Y. Liu, N.G. Walter, N.W. Woodbury, H. Yan, Multi-enzyme complexes on DNA scaffolds capable of substrate channelling with an artificial swinging arm, Nat. Nanotechnol. 9(7) (2014) 531-536.
[116] G.C. Robinson, M. Kaufmann, C. Roux, T.B. Fitzpatrick, Structural definition of the lysine swing in Arabidopsis thaliana PDX1:Intermediate channeling facilitating vitamin B6 biosynthesis, Proc. Natl. Acad. Sci. U. S. A. 113(40) (2016) e5821-e5829.
[117] Y.R. Yang, J. Fu, S. Wootten, X. Qi, M. Liu, H. Yan, Y. Liu, 2D enzyme cascade network with efficient substrate channeling by swinging arms, ChemBioChem 19(3) (2018) 212-216.
[118] J. Fu, M. Liu, Y. Liu, N.W. Woodbury, H. Yan, Interenzyme substrate diffusion for an enzyme cascade organized on spatially addressable DNA nanostructures, J. Am. Chem. Soc. 134(12) (2012) 5516-5519.
[119] Y. Zhang, S. Tsitkov, H. Hess, Proximity does not contribute to activity enhancement in the glucose oxidase-horseradish peroxidase cascade, Nat. Commun. 7(2016) 13982.
[120] C.C. Lee, R.E. Kibblewhite, C.D. Paavola, W.J. Orts, K. Wagschal, Production of Dxylonic acid from hemicellulose using artificial enzyme complexes, J. Microbiol. Biotechnol. 27(1) (2017) 77-83.
[121] H. Shen, M. Schmuck, I. Pilz, N.R. Gilkes, D.G. Kilburn, R.C. Miller Jr., R.A. Warren, Deletion of the linker connecting the catalytic and cellulose-binding domains of endoglucanase A (CenA) of Cellulomonas fimi alters its conformation and catalytic activity, J. Biol. Chem. 266(17) (1991) 11335-11340.
[122] G. Li, Z. Huang, C. Zhang, B.J. Dong, R.H. Guo, H.W. Yue, L.T. Yan, X.H. Xing, Construction of a linker library with widely controllable flexibility for fusion protein design, Appl. Microbiol. Biotechnol. 100(1) (2016) 215-225.
[123] D. Meng, J. Wang, C. You, The properties of the linker in a mini-scaffoldin influence the catalytic efficiency of scaffoldin-mediated enzyme complexes, Enzym. Microb. Technol. 133(2020) 109460.
[124] C.M. Agapakis, D.C. Ducat, P.M. Boyle, E.H. Wintermute, J.C. Way, P.A. Silver, Insulation of a synthetic hydrogen metabolism circuit in bacteria, J. Biol. Eng. 4(2010) 3.
[125] Z. Yang, H. Wang, Y. Wang, Y. Ren, D. Wei, Manufacturing multienzymatic complex reactors in vivo by self-assembly to improve the biosynthesis of itaconic acid in Escherichia coli, ACS Synth. Biol. 7(5) (2018) 1244-1250.
[126] J. Qu, S. Cao, Q. Wei, H. Zhang, R. Wang, W. Kang, T. Ma, L. Zhang, T. Liu, S. Wing-Ngor Au, F. Sun, J. Xia, Synthetic multienzyme complexes, catalytic nanomachineries for cascade biosynthesis in vivo, ACS Nano 13(9) (2019) 9895-9906.
[127] X. Lv, Y. Wu, R. Tian, Y. Gu, Y. Liu, J. Li, G. Du, R. Ledesma-Amaro, L. Liu, Synthetic metabolic channel by functional membrane microdomains for compartmentalized flux control, Metab. Eng. 59(2020) 106-118.
[128] L.R. Lynd, P.J. Weimer, W.H. van Zyl, I.S. Pretorius, Microbial cellulose utilization:fundamentals and biotechnology, Microbiol. Mol. Biol. Rev. 66(3) (2002) 506-577.
[129] L.R. Lynd, X. Liang, M.J. Biddy, A. Allee, H. Cai, T. Foust, M.E. Himmel, M.S. Laser, M. Wang, C.E. Wyman, Cellulosic ethanol:Status and innovation, Curr. Opin. Biotechnol. 45(2017) 202-211.
[130] E.A. Bayer, R. Kenig, R. Lamed, Adherence of Clostridium thermocellum to cellulose, J. Bacteriol. 156(2) (1983) 818-827.
[131] N. Vita, R. Borne, H.P. Fierobe, Cell-surface exposure of a hybrid 3-cohesin scaffoldin allowing the functionalization of Escherichia coli envelope, Biotechnol. Bioeng. 117(3) (2020) 626-636.
[132] E. Nevoigt, Progress in metabolic engineering of Saccharomyces cerevisiae, Microbiol. Mol. Biol. Rev. 72(3) (2008) 379-412.
[133] L.R. Lynd, W.H. van Zyl, J.E. McBride, M. Laser, Consolidated bioprocessing of cellulosic biomass:an update, Curr. Opin. Biotechnol. 16(5) (2005) 577-583.
[134] L.H. Fan, Z.J. Zhang, X.Y. Yu, Y.X. Xue, T.W. Tan, Self-surface assembly of cellulosomes with two miniscaffoldins on Saccharomyces cerevisiae for cellulosic ethanol production, Proc. Natl. Acad. Sci. U. S. A. 109(33) (2012) 13260-13265.
[135] Y. Fujita, J. Ito, M. Ueda, H. Fukuda, A. Kondo, 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) (2004) 1207-1212.
[136] Y. Fujita, S. Takahashi, M. Ueda, A. Tanaka, H. Okada, Y. Morikawa, T. Kawaguchi, M. Arai, H. Fukuda, A. Kondo, Direct and efficient production of ethanol from cellulosic material with a yeast strain displaying cellulolytic enzymes, Appl. Environ. Microbiol. 68(10) (2002) 5136-5141.
[137] S.L. Tsai, J. Oh, S. Singh, R. Chen, W. Chen, Functional assembly of minicellulosomes on the Saccharomyces cerevisiae cell surface for cellulose hydrolysis and ethanol production, Appl. Environ. Microbiol. 75(19) (2009) 6087-6093.
[138] Y. Liang, T. Si, E.L. Ang, H. Zhao, Engineered pentafunctional minicellulosome for simultaneous saccharification and ethanol fermentation in Saccharomyces cerevisiae, Appl. Environ. Microbiol. 80(21) (2014) 6677-6684.
[139] L. Xia, K. Van Nguyen, Y. Holade, H. Han, K. Dooley, P. Atanassov, S. Banta, S.D. Minteer, Improving the performance of methanol biofuel cells utilizing an enzyme cascade bioanode with DNA-bridged substrate channeling, ACS Energy Lett. 2(6) (2017) 1435-1438.
[140] D. Meng, R. Wu, J. Wang, Z. Zhu, C. You, Acceleration of cellodextrin phosphorolysis for bioelectricity generation from cellulosic biomass by integrating a synthetic two-enzyme complex into an in vitro synthetic enzymatic biosystem, Biotechnol. Biofuels 12(2019) 267.
[141] E.T. Hwang, S. Lee, Multienzymatic cascade reactions via enzyme complex by immobilization, ACS Catal. 9(5) (2019) 4402-4425.
[142] J.L. Lin, L. Palomec, I. Wheeldon, Design and analysis of enhanced catalysis in scaffolded multienzyme cascade reactions, ACS Catal. 4(2) (2014) 505-511.
[143] C.M. Agapakis, P.M. Boyle, P.A. Silver, Natural strategies for the spatial optimization of metabolism in synthetic biology, Nat. Chem. Biol. 8(6) (2012) 527-535.