Towards the directed evolution of protein materials

Protein-based materials are a powerful instrument for a new generation of biological materials, with many chemical and mechanical capabilities. Through the manipulation of DNA, researchers can design proteins at the molecular level, engineering a vast array of structural building blocks. However, our capability to rationally design and predict the properties of such materials is limited by the vastness of possible sequence space. Directed evolution has emerged as a powerful tool to improve biological systems through mutation and selection, presenting another avenue to produce novel protein materials. In this prospective review, we discuss the application of directed evolution for protein materials, reviewing current examples and developments that could facilitate the evolution of protein for material applications.

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References

  1. A.A. Cheng and T.K. Lu: Synthetic biology: an emerging engineering discipline. Annu. Rev. Biomed. Eng.14, 155–178 (2012). ArticleCASGoogle Scholar
  2. Y.-J. Chen. P. Liu, A.A.K. Nielsen, J.A.N. Brophy, K. Clancy, T. Peterson, and C.A. Voigt: Characterization of 582 natural and synthetic terminators and quantification of their design constraints. Nat. Methods10, 659–664 (2013). ArticleCASGoogle Scholar
  3. A.A.K. Nielsen, B.S. Der, J. Shin, P. Vaidyanathan, V. Paralanov, E.A. Strychalski, D. Ross, D. Densmore, and C.A. Voigt: Genetic circuit design automation. Science352, aac7341 (2016). ArticleGoogle Scholar
  4. K.M. Esvelt and H.H. Wang: Genome-scale engineering for systems and synthetic biology. Mol. Syst. Biol.9, 641 (2013). ArticleGoogle Scholar
  5. M.T. Mee, J.J. Collins, G.M. Church, and H.H. Wang: Syntrophic exchange in synthetic microbial communities. Proc. Natl. Acad. Sci. USA111, E2149–E2156 (2014). ArticleCASGoogle Scholar
  6. M. Elowitz and W.A. Lim: Build life to understand it. Nature468, 889–890 (2010). ArticleCASGoogle Scholar
  7. C.J. Paddon, P.J. Westfall, D.J. Pitera, K. Benjamin, K. Fisher, D. McPhee, M.D. Leavell, A. Tai, A. Main, D. Eng, D.R. Polichuk, K.H. Teoh, D.W. Reed, T. Treynor, J. Lenihan, H. Jiang, M. Fleck, S. Bajad, G. Dang, D. Dengrove, D. Diola, G. Dorin, K.W. Ellens, S. Fickes, J. Galazzo, S.P. Gaucher, T. Geistlinger, R. Henry, M. Hepp, T. Horning, T. Iqbal, L. Kizer, B. Lieu, D. Melis, N. Moss, R. Regentin, S. Secrest, H. Tsuruta, R. Vazquez, L.F. Westblade, L. Xu, M. Yu, Y. Zhang, L. Zhao, J. Lievense, P.S. Covello, J.D. Keasling, K.K. Reiling, N.S. Renninger, and J.D. Newman: High-level semi-synthetic production of the potent antimalarial artemisinin. Nature496, 528–532 (2013). ArticleCASGoogle Scholar
  8. P. Ball: Synthetic biology—Engineering nature to make materials. MRS Bull.43, 477–484 (2018). ArticleGoogle Scholar
  9. R.A. Le Feuvre and N.S. Scrutton: A living foundry for synthetic biological materials: a synthetic biology roadmap to new advanced materials. Synth. Syst. Biotechnol.3, 105–112 (2018). ArticleGoogle Scholar
  10. M.K. Rice and W.C. Ruder: Creating biological nanomaterials using synthetic biology. Sci. Technol. Adv. Mater.15, 014401 (2013). ArticleGoogle Scholar
  11. S.R. MacEwan and A. Chilkoti: Applications of elastin-like polypeptides in drug delivery. J. Controlled Release190, 314–330 (2014). ArticleCASGoogle Scholar
  12. K.G. DeFrates, R. Moore, J. Borgesi, G. Lin, T. Mulderig, V. Beachley, and X. Hu: Protein-based fiber materials in medicine: a review. Nanomaterials (Basel, Switz.)8, 457 (2018). ArticleGoogle Scholar
  13. N.H. Romano, D. Sengupta, C. Chung, and S.C. Heilshorn: Protein-engineered biomaterials: nanoscale mimics of the extracellular matrix. Biochim. Biophys. Acta1810, 339–349 (2011). ArticleCASGoogle Scholar
  14. G. Chan and D.J. Mooney: New materials for tissue engineering: towards greater control over the biological response. Trends Biotechnol.26, 382–392 (2008). ArticleCASGoogle Scholar
  15. J.M. Caves, V.A. Kumar, A.W. Martinez, J. Kim, C.M. Ripberger, C.A. Haller, and E.L. Chaikof: The use of microfiber composites of elastin-like protein matrix reinforced with synthetic collagen in the design of vascular grafts. Biomaterials31, 7175–7182 (2010). ArticleCASGoogle Scholar
  16. C. Gilbert and T. Ellis: Biological engineered living materials: growing functional materials with genetically programmable properties. ACS Synth. Biol.8, 1–15 (2019). ArticleCASGoogle Scholar
  17. P.Q. Nguyen, N.-M.D. Courchesne, A. Duraj-Thatte, P. Praveschotinunt, and N.S. Joshi: Engineered living materials: prospects and challenges for using biological systems to direct the assembly of smart materials. Adv. Mater.30, 1704847 (2018). ArticleGoogle Scholar
  18. S.E. Naleway, M.M. Porter, J. McKittrick, and M.A. Meyers: Structural design elements in biological materials: application to bioinspiration. Adv. Mater.27, 5455–5476 (2015). ArticleCASGoogle Scholar
  19. K.A. Dill and J.L. MacCallum: The protein-folding problem, 50 years on. Science338, 1042–1046 (2012). ArticleCASGoogle Scholar
  20. R.E. Cobb, N. Sun, and H. Zhao: Directed evolution as a powerful synthetic biology tool. Methods60, 81–90 (2013). ArticleCASGoogle Scholar
  21. J.C.M. van Hest and D.A. Tirrell: Protein-based materials, toward a new level of structural control. Chem. Commun. 1897–1904 (2001). Google Scholar
  22. Y.J. Yang, A.L. Holmberg, and B.D. Olsen: Artificially engineered protein polymers. Annu. Rev. Chem. Biomol. Eng.8, 549–575 (2017). ArticleCASGoogle Scholar
  23. L. Yang, A. Liu, S. Cao, R.M. Putri, P. Jonkheijm, and J.J.L.M. Cornelissen: Self-assembly of proteins: towards supramolecular materials. Chem.–Eur. J.22, 15570–15582 (2016). ArticleCASGoogle Scholar
  24. M.S. Ekiz, G. Cinar, M.A. Khalily, and M.O. Guler: Self-assembled peptide nanostructures for functional materials. Nanotechnology27, 402002 (2016). ArticleGoogle Scholar
  25. B.O. Okesola and A. Mata: Multicomponent self-assembly as a tool to harness new properties from peptides and proteins in material design. Chem. Soc. Rev.47, 3721–3736 (2018). ArticleCASGoogle Scholar
  26. C. Vepari and D.L. Kaplan: Silk as a biomaterial. Prog. Polym. Sci.32, 991–1007 (2007). ArticleCASGoogle Scholar
  27. O. Tokareva, V.A. Michalczechen-Lacerda, E.L. Rech, and D.L. Kaplan: Recombinant DNA production of spider silk proteins. Microb. Biotechnol.6, 651–663 (2013). ArticleCASGoogle Scholar
  28. Q. Peng, Y. Zhang, L. Lu, H. Shao, K. Qin, X. Hu, and X. Xia: Recombinant spider silk from aqueous solutions via a bio-inspired microfluidic chip. Sci. Rep.6, 36473 (2016). ArticleCASGoogle Scholar
  29. C.L. Craig: Evolution of arthropod silks. Annu. Rev. Entomol.42, 231–267 (1997). ArticleCASGoogle Scholar
  30. F. Vollrath and P. Selden: The role of behavior in the evolution of spiders, silks, and webs. Annu. Rev. Ecol. Evol. Syst.38, 819–846 (2007). ArticleGoogle Scholar
  31. X. Hu, K. Vasanthavada, K. Kohler, S. McNary, A.M.F. Moore, and C.A. Vierra: Molecular mechanisms of spider silk. Cell. Mol. Life Sci.63, 1986–1999 (2006). CASGoogle Scholar
  32. L. Römer and T. Scheibel: The elaborate structure of spider silk. Prion2, 154–161 (2008). ArticleGoogle Scholar
  33. L.P. Gage and R.F. Manning: Internal structure of the silk fibroin gene of Bombyx mori. I. The fibroin gene consists of a homogeneous alternating array of repetitious crystalline and amorphous coding sequences. J. Biol. Chem.255, 9444–9450 (1980). ArticleCASGoogle Scholar
  34. K.M. Rudall and W. Kenchington: Arthropod silks: the problem of fibrous proteins in animal tissues. Annu. Rev. Entomol.16, 73–96 (1971). ArticleCASGoogle Scholar
  35. A. Rising, H. Nimmervoll, S. Grip, A. Fernandez-Arias, E. Storckenfeldt, D.P. Knight, F. Vollrath, and W. Engström: Spider silk proteins— mechanical property and gene sequence. Zool. Sci.22, 273–281 (2005). ArticleCASGoogle Scholar
  36. T. Kowalczyk, K. Hnatuszko-Konka, A. Gerszberg, and A.K. Kononowicz: Elastin-like polypeptides as a promising family of genetically-engineered protein based polymers. World J. Microbiol. Biotechnol.30, 2141–2152 (2014). ArticleCASGoogle Scholar
  37. W. Hassouneh, T. Christensen, and A. Chilkoti: Elastin-like Polypeptides as a Purification Tag for Recombinant Proteins. Curr. Protoc. Protein Sci. Editor. Board John E Coligan Al CHAPTER, Unit–6.11 (2010). Google Scholar
  38. R. Saxena and M.J. Nanjan: Elastin-like polypeptides and their applications in anticancer drug delivery systems: a review. Drug Deliv.22, 156–167 (2015). ArticleCASGoogle Scholar
  39. K.E. Inostroza-Brito, E. Collin, O. Siton-Mendelson, K.H. Smith, A. Monge-Marcet, D.S. Ferreira, R.P. Rodríguez, M. Alonso, J.C. Rodríguez-Cabello, R.L. Reis, F. Sagués, L. Botto, R. Bitton, H.S. Azevedo, and A. Mata: Co-assembly, spatiotemporal control and morphogenesis of a hybrid protein–peptide system. Nat. Chem.7, 897 (2015). ArticleCASGoogle Scholar
  40. H. Wang, A. Paul, D. Nguyen, A. Enejder, and S.C. Heilshorn: Tunable control of hydrogel microstructure by kinetic competition between selfassembly and crosslinking of elastin-like proteins. ACS Appl. Mater. Interfaces10, 21808–21815 (2018). ArticleCASGoogle Scholar
  41. F.G. Quiroz and A. Chilkoti: Sequence heuristics to encode phase behaviour in intrinsically disordered protein polymers. Nat. Mater.14, 1164 (2015). ArticleCASGoogle Scholar
  42. N.K. Li, S. Roberts, F.G. Quiroz, A. Chilkoti, and Y.G. Yingling: Sequence directionality dramatically affects LCST behavior of elastin-like polypeptides. Biomacromolecules19, 2496–2505 (2018). ArticleCASGoogle Scholar
  43. M.D. Shoulders and R.T. Raines: Collagen structure and stability. Annu. Rev. Biochem.78, 929–958 (2009). ArticleCASGoogle Scholar
  44. K. Gelse, E. Pöschl, and T. Aigner: Collagens—structure, function, and biosynthesis. Adv. Drug Deliv. Rev.55, 1531–1546 (2003). ArticleCASGoogle Scholar
  45. A.V. Persikov, J.A.M. Ramshaw, and B. Brodsky: Prediction of collagen stability from amino acid sequence. J. Biol. Chem.280, 19343–19349 (2005). ArticleCASGoogle Scholar
  46. S. Lukomski, K. Nakashima, I. Abdi, V.J. Cipriano, R.M. Ireland, S.D. Reid, G.G. Adams, and J.M. Musser: Identification and characterization of the scl gene encoding a group a streptococcus extracellular protein virulence factor with similarity to human collagen. Infect. Immun.68, 6542–6553 (2000). ArticleCASGoogle Scholar
  47. Z. Yu, B. An, J.A.M. Ramshaw, and B. Brodsky: Bacterial collagen-like proteins that form triple-helical structures. J. Struct. Biol.186, 451–461 (2014). ArticleCASGoogle Scholar
  48. E. Cosgriff-Hernandez, M.S. Hahn, B. Russell, T. Wilems, D. Munoz-Pinto, M.B. Browning, J. Rivera, and M. Höök: Bioactive hydrogels based on designer collagens. Acta Biomater.6, 3969–3977 (2010). ArticleCASGoogle Scholar
  49. M.M. Barnhart and M.R. Chapman: Curli biogenesis and function. Annu. Rev. Microbiol.60, 131–147 (2006). ArticleCASGoogle Scholar
  50. S.K. Collinson, L. Emödy, K.H. Müller, T.J. Trust, and W.W. Kay: Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J. Bacteriol.173, 4773–4781 (1991). ArticleCASGoogle Scholar
  51. P.Q. Nguyen, Z. Botyanszki, P.K.R. Tay, and N.S. Joshi: Programmable biofilm-based materials from engineered curli nanofibres. Nat. Commun.5, 4945 (2014). ArticleCASGoogle Scholar
  52. N.-M. Dorval Courchesne, A. Duraj-Thatte, P.K.R. Tay, P.Q. Nguyen, and N.S. Joshi: Scalable production of genetically engineered nanofibrous macroscopic materials via Filtration. ACS Biomater. Sci. Eng.3, 733–741 (2017). ArticleGoogle Scholar
  53. P.K.R. Tay, P.Q. Nguyen, and N.S. Joshi: A synthetic circuit for mercury bioremediation using self-assembling functional amyloids. ACS Synth. Biol.6, 1841 (2017). ArticleGoogle Scholar
  54. A.M. Duraj-Thatte, P. Praveschotinunt, T.R. Nash, F.R. Ward, and N.S. Joshi: Modulating bacterial and gut mucosal interactions with engineered biofilm matrix proteins. Sci. Rep.8, 3475 (2018). ArticleGoogle Scholar
  55. G. Zeng, B.S. Vad, M.S. Dueholm, G. Christiansen, M. Nilsson, T. Tolker-Nielsen, P.H. Nielsen, R.L. Meyer, and D.E. Otzen: Functional bacterial amyloid increases Pseudomonas biofilm hydrophobicity and stiffness. Front. Microbiol.6, 1099 (2015). ArticleGoogle Scholar
  56. E. Axpe, A. Duraj-Thatte, Y. Chang, D.-M. Kaimaki, A. Sanchez-Sanchez, H.B. Caliskan, N.-M. Dorval Courchesne, and N.S. Joshi: Fabrication of amyloid curli fibers–alginate nanocomposite hydrogels with enhanced stiffness. ACS Biomater. Sci. Eng.4, 2100–2105 (2018). ArticleCASGoogle Scholar
  57. M.S. Dueholm, M. Albertsen, D. Otzen, and P.H. Nielsen: Curli functional amyloid systems are phylogenetically widespread and display large diversity in operon and protein structure. PLoS ONE7, e51274 (2012). ArticleCASGoogle Scholar
  58. N.P. King, J.B. Bale, W. Sheffler, D.E. McNamara, S. Gonen, T. Gonen, T. O. Yeates, and D. Baker: Accurate design of co-assembling multicomponent protein nanomaterials. Nature510, 103–108 (2014). ArticleCASGoogle Scholar
  59. A. Leaver-Fay, M. Tyka, S.M. Lewis, O.F. Lange, J. Thompson, R. Jacak, K. Kaufman, P.D. Renfrew, C.A. Smith, W. Sheffler, I.W. Davis, S. Cooper, A. Treuille, D.J. Mandell, F. Richter, Y.-E. A. Ban, S.J. Fleishman, J.E. Corn, D.E. Kim, S. Lyskov, M. Berrondo, S. Mentzer, Z. Popović, J.J. Havranek, J. Karanicolas, R. Das, J. Meiler, T. Kortemme, J.J. Gray, B. Kuhlman, D. Baker, and P. Bradley: Rosetta3: an object-oriented software suite for the simulation and design of macromolecules. Methods Enzymol.487, 545–574 (2011). ArticleCASGoogle Scholar
  60. H. Shen, J.A. Fallas, E. Lynch, W. Sheffler, B. Parry, N. Jannetty, J. Decarreau, M. Wagenbach, J.J. Vicente, J. Chen, L. Wang, Q. Dowling, G. Oberdorfer, L. Stewart, L. Wordeman, J.D. Yoreo, C. Jacobs-Wagner, J. Kollman, and D. Baker: De novo design of selfassembling helical protein filaments. Science362, 705–709 (2018). ArticleCASGoogle Scholar
  61. A.S. Cristie-David, A. Sciore, S. Badieyan, J.D. Escheweiler, P. Koldewey, J.C.A. Bardwell, B.T. Ruotolo, and E.N.G. Marsh: Evaluation of de novodesigned coiled coils as off-the-shelf components for protein assembly. Mol. Syst. Des. Eng.2, 140–148 (2017). ArticleCASGoogle Scholar
  62. J.M. Fletcher, R.L. Harniman, F.R.H. Barnes, A.L. Boyle, A. Collins, J. Mantell, T.H. Sharp, M. Antognozzi, P.J. Booth, N. Linden, M.J. Miles, R.B. Sessions, P. Verkade, and D.N. Woolfson: Self-assembling cages from coiled-coil peptide modules. Science340, 595–599 (2013). ArticleCASGoogle Scholar
  63. F. Thomas, W.M. Dawson, E.J.M. Lang, A.J. Burton, G.J. Bartlett, G.G. Rhys, A.J. Mulholland, and D.N. Woolfson: De novo-designed α-helical barrels as receptors for small molecules. ACS Synth. Biol.7, 1808 (2018). ArticleCASGoogle Scholar
  64. A. Ljubetič, F. Lapenta, H. Gradišar, I. Drobnak, J. Aupič, Ž. Strmšek, D. Lainšček, I. Hafner-Bratkovič, A. Majerle, N. Krivec, M. Benčina, T. Pisanski, T. Ć. Veličković, A. Round, J.M. Carazo, R. Melero, and R. Jerala: Design of coiled-coil protein-origami cages that self-assemble in vitro and in vivo. Nat. Biotechnol.35, 1094 (2017). ArticleGoogle Scholar
  65. O.S. Rabotyagova, P. Cebe, and D.L. Kaplan: Protein-based block copolymers. Biomacromolecules12, 269–289 (2011). ArticleCASGoogle Scholar
  66. R. Valluzzi, S. Winkler, D. Wilson, and D.L. Kaplan: Silk: molecular organization and control of assembly. Philos. Trans. R. Soc. B: Biol. Sci.357, 165–167 (2002). ArticleCASGoogle Scholar
  67. O.S. Rabotyagova, P. Cebe, and D.L. Kaplan: Self-assembly of genetically engineered spider silk block copolymers. Biomacromolecules10, 229–236 (2009). ArticleCASGoogle Scholar
  68. M.C. Huber, A. Schreiber, P. von Olshausen, B.R. Varga, O. Kretz, B. Joch, S. Barnert, R. Schubert, S. Eimer, P. Kele, and S.M. Schiller: Designer amphiphilic proteins as building blocks for the intracellular formation of organelle-like compartments. Nat. Mater.14, 125 (2015). ArticleCASGoogle Scholar
  69. N. Dinjaski and D.L. Kaplan: Recombinant protein blends: silk beyond natural design. Curr. Opin. Biotechnol.39, 1–7 (2016). ArticleCASGoogle Scholar
  70. A.Y. Chen, Z. Deng, A.N. Billings, U.O.S. Seker, M.Y. Lu, R.J. Citorik, B. Zakeri, and T.K. Lu: Synthesis and patterning of tunable multiscale materials with engineered cells. Nat. Mater.13, 515–523 (2014). ArticleCASGoogle Scholar
  71. J.K. Polka, S.G. Hays, and P.A. Silver: Building spatial synthetic biology with compartments, scaffolds, and communities. Cold Spring Harb. Perspect. Biol.8, a024018 (2016). ArticleGoogle Scholar
  72. H. Garcia-Seisdedos, C. Empereur-Mot, N. Elad, and E.D. Levy: Proteins evolve on the edge of supramolecular self-assembly. Nature548, 244 (2017). ArticleCASGoogle Scholar
  73. Y. Suzuki, G. Cardone, D. Restrepo, P.D. Zavattieri, T.S. Baker, and F.A. Tezcan: Self-assembly of coherently dynamic, auxetic, two-dimensional protein crystals. Nature533, 369–373 (2016). ArticleCASGoogle Scholar
  74. B. Zakeri, J.O. Fierer, E. Celik, E.C. Chittock, U. Schwarz-Linek, V.T. Moy, and M. Howarth: Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Proc. Natl. Acad. Sci. USA109, E690–E697 (2012). ArticleCASGoogle Scholar
  75. F. Sun, W.-B. Zhang, A. Mahdavi, F.H. Arnold, and D.A. Tirrell: Synthesis of bioactive protein hydrogels by genetically encoded SpyTag-SpyCatcher chemistry. Proc. Natl. Acad. Sci. USA111, 11269–11274 (2014). ArticleCASGoogle Scholar
  76. R.E. Cobb, R. Chao and H. Zhao: Directed evolution: past, present and future. AIChE J. Am. Inst. Chem. Eng.59, 1432–1440 (2013). ArticleCASGoogle Scholar
  77. K.L. Tee and T.S. Wong: Polishing the craft of genetic diversity creation in directed evolution. Biotechnol. Adv.31, 1707–1721 (2013). ArticleCASGoogle Scholar
  78. M.S. Packer and D.R. Liu: Methods for the directed evolution of proteins. Nat. Rev. Genet.16, 379–394 (2015). ArticleCASGoogle Scholar
  79. F.H. Arnold: Design by directed evolution. Acc. Chem. Res.31, 125–131 (1998). ArticleCASGoogle Scholar
  80. A. Currin, N. Swainston, P.J. Day, and D.B. Kell: Synthetic biology for the directed evolution of protein biocatalysts: navigating sequence space intelligently. Chem. Soc. Rev.44, 1172–1239 (2015). ArticleCASGoogle Scholar
  81. W.P.C. Stemmer: Rapid evolution of a protein in vitro by DNA shuffling. Nature370, 389–391 (1994). ArticleCASGoogle Scholar
  82. H. Zhao and F.H. Arnold: Optimization of DNA shuffling for high fidelity recombination. Nucleic Acids Res.25, 1307–1308 (1997). ArticleCASGoogle Scholar
  83. A. Crameri, S.-A. Raillard, E. Bermudez, and W.P.C. Stemmer: DNA shuffling of a family of genes from diverse species accelerates directed evolution. Nature391, 288–291 (1998). ArticleCASGoogle Scholar
  84. C. Engler, R. Gruetzner, R. Kandzia, and S. Marillonnet: Golden gate shuffling: a one-pot DNA shuffling method based on type IIs restriction enzymes. PLoS ONE4, e5553 (2009). ArticleGoogle Scholar
  85. M. Ostermeier, J.H. Shim, and S.J. Benkovic: A combinatorial approach to hybrid enzymes independent of DNA homology. Nat. Biotechnol.17, 1205 (1999). ArticleCASGoogle Scholar
  86. D. Bikard, S. Julié-Galau, G. Cambray, and D. Mazel: The synthetic integron: an in vivo genetic shuffling device. Nucleic Acids Res.38, e153–e153 (2010). ArticleGoogle Scholar
  87. P.L. Foster: In vivo mutagenesis. Methods Enzymol.204, 114–125 (1991). ArticleCASGoogle Scholar
  88. H.H. Wang, F.J. Isaacs, P.A. Carr, Z.Z. Sun, G. Xu, C.R. Forest, and G.M. Church: Programming cells by multiplex genome engineering and accelerated evolution. Nature460, 894–898 (2009). ArticleCASGoogle Scholar
  89. S.O. Halperin, C.J. Tou, E.B. Wong, C. Modavi, D.V. Schaffer, and J.E. Dueber: CRISPR-guided DNA polymerases enable diversification of all nucleotides in a tunable window. Nature560, 248 (2018). ArticleCASGoogle Scholar
  90. S. Lutz: Beyond directed evolution—semi-rational protein engineering and design. Curr. Opin. Biotechnol.21, 734–743 (2010). ArticleCASGoogle Scholar
  91. P. Heinzelman, C.D. Snow, I. Wu, C. Nguyen, A. Villalobos, S. Govindarajan, J. Minshull, and F.H. Arnold: A family of thermostable fungal cellulases created by structure-guided recombination. Proc. Natl. Acad. Sci. USA106, 5610–5615 (2009). ArticleCASGoogle Scholar
  92. P.A.G. Tizei, E. Csibra, L. Torres, and V.B. Pinheiro: Selection platforms for directed evolution in synthetic biology. Biochem. Soc. Trans.44, 1165–1175 (2016). ArticleCASGoogle Scholar
  93. S. Raman, J.K. Rogers, N.D. Taylor, and G.M. Church: Evolution-guided optimization of biosynthetic pathways. Proc. Natl. Acad. Sci. USA111, 17803–17808 (2014). ArticleCASGoogle Scholar
  94. J.-D. Pédelacq, S. Cabantous, T. Tran, T.C. Terwilliger, and G.S. Waldo: Engineering and characterization of a superfolder green fluorescent protein. Nat. Biotechnol.24, 79–88 (2006). ArticleGoogle Scholar
  95. S.-A. Morgan, D.C. Nadler, R. Yokoo, and D.F. Savage: Biofuel metabolic engineering with biosensors. Curr. Opin. Chem. Biol.35, 150–158 (2016). ArticleCASGoogle Scholar
  96. S.R.A. Devenish, M. Kaltenbach, M. Fischlechner, and F. Hollfelder: Droplets as Reaction Compartments for Protein Nanotechnology. In Protein Nanotechnology: Protocols, Instrumentation, and Applications, 2nd ed., edited by J A. Gerrard (Humana Press, 2013), pp. 269–286. ChapterGoogle Scholar
  97. K.T. O’Neil and R.H. Hoess: Phage display: protein engineering by directed evolution. Curr. Opin. Struct. Biol.5, 443–449 (1995). ArticleGoogle Scholar
  98. A. Fernandez-Gacio, M. Uguen, and J. Fastrez: Phage display as a tool for the directed evolution of enzymes. Trends Biotechnol.21, 408–414 (2003). ArticleCASGoogle Scholar
  99. K.M. Esvelt, J.C. Carlson, and D.R. Liu: A system for the continuous directed evolution of biomolecules. Nature472, 499 (2011). ArticleCASGoogle Scholar
  100. H. Leemhuis, V. Stein, A.D. Griffiths, and F. Hollfelder: New genotype–phenotype linkages for directed evolution of functional proteins. Curr. Opin. Struct. Biol.15, 472–478 (2005). ArticleCASGoogle Scholar
  101. S. Kosuri, D.B. Goodman, G. Cambray, V.K. Mutalik, Y. Gao, A.P. Arkin, D. Endy, and G.M. Church: Composability of regulatory sequences controlling transcription and translation in Escherichia coli. Proc. Natl. Acad. Sci. USA.110, 14024 (2013). ArticleCASGoogle Scholar
  102. A. Zinchenko, S.R.A. Devenish, B. Kintses, P.-Y. Colin, M. Fischlechner, and F. Hollfelder: One in a million: flow cytometric sorting of single celllysate assays in monodisperse picolitre double emulsion droplets for directed evolution. Anal. Chem.86, 2526–2533 (2014). ArticleCASGoogle Scholar
  103. J.J. Agresti, E. Antipov, A.R. Abate, K. Ahn, A.C. Rowat, J.-C. Baret, M. Marquez, A.M. Klibanov, A.D. Griffiths, and D.A. Weitz: Ultrahigh-throughput screening in drop-based microfluidics for directed evolution. Proc. Natl. Acad. Sci. USA107, 4004–4009 (2010). ArticleCASGoogle Scholar
  104. P.-Y. Colin, B. Kintses, F. Gielen, C.M. Miton, G. Fischer, M.F. Mohamed, M. Hyvönen, D.P. Morgavi, D.B. Janssen, and F. Hollfelder: Ultrahigh-throughput discovery of promiscuous enzymes by picodroplet functional metagenomics. Nat. Commun.6, 10008 (2015). ArticleCASGoogle Scholar
  105. F. Gielen, R. Hours, S. Emond, M. Fischlechner, U. Schell, and F. Hollfelder: Ultrahigh-throughput–directed enzyme evolution by absorbance-activated droplet sorting (AADS). Proc. Natl. Acad. Sci. USA113, E7383–E7389 (2016). ArticleCASGoogle Scholar
  106. M. Girault, H. Kim, H. Arakawa, K. Matsuura, M. Odaka, A. Hattori, H. Terazono, and K. Yasuda: An on-chip imaging droplet-sorting system: a real-time shape recognition method to screen target cells in droplets with single cell resolution. Sci. Rep.7, 40072 (2017). ArticleCASGoogle Scholar
  107. H.-D. Xi, H. Zheng, W. Guo, A.M. Gañán-Calvo, Y. Ai, C.-W. Tsao, J. Zhou, W. Li, Y. Huang, N.-T. Nguyen, and S.H. Tan: Active droplet sorting in microfluidics: a review. Lab Chip17, 751–771 (2017). ArticleCASGoogle Scholar
  108. S.S. Terekhov, I.V. Smirnov, A.V. Stepanova, T.V. Bobik, Y.A. Mokrushina, N.A. Ponomarenko, A.A. Belogurov, M.P. Rubtsova, O.V. Kartseva, M.O. Gomzikova, A.A. Moskovtsev, A.S. Bukatin, M.V. Dubina, E.S. Kostryukova, V.V. Babenko, M.T. Vakhitova, A.I. Manolov, M.V. Malakhova, M.A. Kornienko, A.V. Tyakht, A.A. Vanyushkina, E.N. Ilina, P. Masson, A.G. Gabibov, and S. Altman: Microfluidic droplet platform for ultrahigh-throughput single-cell screening of biodiversity. Proc. Natl. Acad. Sci. USA114, 2550–2555 (2017). ArticleCASGoogle Scholar
  109. P.A. Romero and F.H. Arnold: Exploring protein fitness landscapes by directed evolution. Nat. Rev. Mol. Cell Biol.10, 866–876 (2009). ArticleCASGoogle Scholar
  110. J.D. Bloom and F.H. Arnold: In the light of directed evolution: pathways of adaptive protein evolution. Proc. Natl. Acad. Sci. USA106, 9995–10000 (2009). ArticleCASGoogle Scholar
  111. S. Kauffman and S. Levin: Towards a general theory of adaptive walks on rugged landscapes. J. Theor. Biol.128, 11–45 (1987). ArticleCASGoogle Scholar
  112. J.G. Heddle, S. Chakraborti, and K. Iwasaki: Natural and artificial protein cages: design, structure and therapeutic applications. Curr. Opin. Struct. Biol.43, 148–155 (2017). ArticleCASGoogle Scholar
  113. B. Wörsdörfer, K.J. Woycechowsky, and D. Hilvert: Directed evolution of a protein container. Science331, 589–592 (2011). ArticleGoogle Scholar
  114. G.L. Butterfield, M.J. Lajoie, H.H. Gustafson, D.L. Sellers, U. Nattermann, D. Ellis, J.B. Bale, S. Ke, G.H. Lenz, A. Yehdego, R. Ravichandran, S.H. Pun, N.P. King, and D. Baker: Evolution of a designed protein assembly encapsulating its own RNA genome. Nature552, 415–420 (2017). ArticleCASGoogle Scholar
  115. J.B. Bale, S. Gonen, Y. Liu, W. Sheffler, D. Ellis, C. Thomas, D. Cascio, T. O. Yeates, T. Gonen, N.P. King, and D. Baker: Accurate design of megadalton-scale two-component icosahedral protein complexes. Science353, 389–394 (2016). ArticleCASGoogle Scholar
  116. N.C. Tang and A. Chilkoti: Combinatorial codon scrambling enables scalable gene synthesis and amplification of repetitive proteins. Nat. Mater.15, 419 (2016). ArticleCASGoogle Scholar
  117. N.G. Bednarska, J. Schymkowitz, F. Rousseau, and J. Van Eldere: Protein aggregation in bacteria: the thin boundary between functionality and toxicity. Microbiology159, 1795–1806 (2013). ArticleCASGoogle Scholar
  118. M.L. Evans, E. Chorell, J.D. Taylor, J. Åden, A. Götheson, F. Li, M. Koch, L. Sefer, S.J. Matthews, P. Wittung-Stafshede, F. Almqvist, and M.R. Chapman: The bacterial curli system possesses a potent and selective inhibitor of amyloid formation. Mol. Cell57, 445–455 (2015). ArticleCASGoogle Scholar
  119. B. Kintses, C. Hein, M.F. Mohamed, M. Fischlechner, F. Courtois, C. Lainé, and F. Hollfelder: Picoliter cell lysate assays in microfluidic droplet compartments for directed enzyme evolution. Chem. Biol.19, 1001–1009 (2012). ArticleCASGoogle Scholar
  120. Cappello Joseph, Crissman John, Dorman Mary, Mikolajczak Marcia, Textor Garret, Marquet Magda, and Ferrari Franco: Genetic engineering of structural protein polymers. Biotechnol. Prog.6, 198–202 (1990). ArticleGoogle Scholar
  121. M.C. Huber, A. Schreiber, W. Wild, K. Benz, and S.M. Schiller: Introducing a combinatorial DNA-toolbox platform constituting defined protein-based biohybrid-materials. Biomaterials35, 8767–8779 (2014). ArticleCASGoogle Scholar
  122. E.M. Darling and D. Di Carlo: High-throughput assessment of cellular mechanical properties. Annu. Rev. Biomed. Eng.17, 35–62 (2015). ArticleCASGoogle Scholar
  123. N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda: Intelligent image-activated cell sorting. Cell, 175, 266–276.e13 (2018). ArticleCASGoogle Scholar
  124. J.S. Dudani, D.R. Gossett, H.T.K. Tse, and D.D. Carlo: Pinched-flow hydrodynamic stretching of single-cells. Lab Chip13, 3728–3734 (2013). ArticleCASGoogle Scholar
  125. M.Y. Hwang, S.G. Kim, H.S. Lee, and S.J. Muller: Elastic particle deformation in rectangular channel flow as a measure of particle stiffness. Soft Matter14, 216 (2017). doi: 10.1039/C7SM01829K. ArticleGoogle Scholar
  126. P.-H. Wu, C.M. Hale, W.-C. Chen, J.S.H. Lee, Y. Tseng, and D. Wirtz: High-throughput ballistic injection nanorheology to measure cell mechanics. Nat. Protoc.7, 155 (2012). ArticleCASGoogle Scholar
  127. T. Liu, X. Liu, D.R. Spring, X. Qian, J. Cui, and Z. Xu: Quantitatively mapping cellular viscosity with detailed organelle information via a designed PET fluorescent probe. Sci. Rep.4, 5418 (2014). ArticleCASGoogle Scholar
  128. X. Ding, Z. Peng, S.-C. S. Lin, M. Geri, S. Li, P. Li, Y. Chen, M. Dao, S. Suresh, and T.J. Huang: Cell separation using tilted-angle standing surface acoustic waves. Proc. Natl. Acad. Sci. USA111, 12992–12997 (2014). ArticleCASGoogle Scholar
  129. M. Islam, H. Brink, S. Blanche, C. DiPrete, T. Bongiorno, N. Stone, A. Liu, A. Philip, G. Wang, W. Lam, A. Alexeev, E.K. Waller, and T. Sulchek: Microfluidic sorting of cells by viability based on differences in cell stiffness. Sci. Rep.7, 1997 (2017). ArticleGoogle Scholar
  130. N.K. Gill, C. Ly, K.D. Nyberg, L. Lee, D. Qi, B. Tofig, M. Reis-Sobreiro, O. Dorigo, J. Rao, R. Wiedemeyer, B. Karlan, K. Lawrenson, M.R. Freeman, R. Damoiseaux, and A.C. Rowat: A scalable filtration method for high throughput screening based on cell deformability. Lab Chip19, 343–357 (2019). ArticleCASGoogle Scholar
  131. M.D. Vahey and J. Voldman: High-throughput cell and particle characterization using ISO-dielectric separation. Anal. Chem.81, 2446–2455 (2009). ArticleCASGoogle Scholar
  132. M.D. Vahey, L.Q. Pesudo, J.P. Svensson, L.D. Samson, and J. Voldman: Microfluidic genome-wide profiling of intrinsic electrical properties in Saccharomyces cerevisiae. Lab Chip13, 2754–2763 (2013). ArticleCASGoogle Scholar
  133. A. Tay, C. Murray, and D. Di Carlo: Phenotypic selection of Magnetospirillum magneticum (AMB-1) overproducers using magnetic ratcheting. Adv. Funct. Mater.27, 1703106 (2017). ArticleGoogle Scholar
  134. H.B. Fraser, A.E. Hirsh, L.M. Steinmetz, C. Scharfe, and M.W. Feldman: Evolutionary rate in the protein interaction network. Science296, 750–752 (2002). ArticleCASGoogle Scholar
  135. D.A. Drummond, J.D. Bloom, C. Adami, C.O. Wilke, and F.H. Arnold: Why highly expressed proteins evolve slowly. Proc. Natl. Acad. Sci. USA102, 14338–14343 (2005). ArticleCASGoogle Scholar
  136. P.Q. Nguyen. Synthetic biology engineering of biofilms as nanomaterials factories. Biochem. Soc. Trans.45, 585–597 (2017). ArticleCASGoogle Scholar
  137. J. Shin and V. Noireaux: An E. coli cell-free expression toolbox: application to synthetic gene circuits and artificial cells. ACS Synth. Biol.1, 29–41 (2012). ArticleCASGoogle Scholar
  138. Y. Schaerli and F. Hollfelder: The potential of microfluidic water-in-oil droplets in experimental biology. Mol. Biosyst.5, 1392–1404 (2009). ArticleCASGoogle Scholar
  139. A.J. Mach, J.H. Kim, A. Arshi, S.C. Hur, and D.D. Carlo: Automated cellular sample preparation using a centrifuge-on-a-chip. Lab Chip11, 2827–2834 (2011). ArticleCASGoogle Scholar
  140. N. Cheney, R. MacCurdy, J. Clune, and H. Lipson: Unshackling Evolution: Evolving Soft Robots with Multiple Materials and a Powerful Generative Encoding. In Proceedings of the 15th Annual Conference on Genetic and Evolutionary Computation (ACM, New York, NY, USA, 2013), pp. 167–174. ChapterGoogle Scholar
  141. G. Mackenzie, A.N. Boa, A. Diego-Taboada, S.L. Atkin, and T. Sathyapalan: Sporopollenin, The least known yet toughest natural biopolymer. Front. Mater.2, 66 (2015). ArticleGoogle Scholar
  142. M. Nokelainen, H. Tu, A. Vuorela, H. Notbohm, K.I. Kivirikko, and J. Myllyharju: High-level production of human type I collagen in the yeast Pichia pastoris. Yeast18, 797–806 (2001). ArticleCASGoogle Scholar

Acknowledgments

This work was supported by NSF Grant 1410751 (Division of Materials Research), the National Institutes of Health (1R01DK11077001A1), and the Wyss Institute for Biologically Inspired Engineering. The authors would also like to thank the reviewers for their time and insightful contributions to the article.