Extracellular Self-Assembly of Functional and Tunable Protein Conjugates from Bacillus subtilis

ACS Synthetic Biology

Volumn 6, Issue 6, 2017, Pages 957-967

  Gilbert, Charlie ^a   Howarth, Mark ^b   Harwood, Colin R ^c   Ellis, Tom ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

extracellular self assembly; microbial consortia; protein conjugation; SpyTag SpyCatcher; thermotolerance; tunability

Indexed keywords

BACTERIAL PROTEIN; INDUSTRIAL ENZYME; RECOMBINANT PROTEIN; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; XYNA PROTEIN; ENDO 1,4 BETA XYLANASE; HYBRID PROTEIN;

ARTICLE; BACILLUS SUBTILIS; CONJUGATE; CONJUGATION; COVALENT BOND; CULTURE MEDIUM; CYCLIZATION; HEAT TOLERANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECRETION; CHEMISTRY; EXTRACELLULAR SPACE; GENETICS; HEAT; METABOLISM; PROCEDURES; SYNTHETIC BIOLOGY;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; ENDO-1,4-BETA XYLANASES; EXTRACELLULAR SPACE; HOT TEMPERATURE; PROTEIN ENGINEERING; RECOMBINANT FUSION PROTEINS; SYNTHETIC BIOLOGY;

EID: 85020894803     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.6b00292     Document Type: Article

References (67)

1. Hartwell, L. H., Hopfield, J. J., Leibler, S., and Murray, A. W. (1999) From molecular to modular cell biology Nature 402, C47-C52 10.1038/35011540
2. Parmar, P. A., Chow, L. W., St-Pierre, J.-P., Horejs, C.-M., Peng, Y. Y., Werkmeister, J. A., Ramshaw, J. A. M., and Stevens, M. M. (2015) Collagen-mimetic peptide-modifiable hydrogels for articular cartilage regeneration Biomaterials 54, 213-225 10.1016/j.biomaterials.2015.02.079
3. Minamihata, K., Yamaguchi, S., Nakajima, K., and Nagamune, T. (2016) Tyrosine Coupling Creates a Hyperbranched Multivalent Protein Polymer Using Horseradish Peroxidase via Bipolar Conjugation Points Bioconjugate Chem. 27, 1348-1359 10.1021/acs.bioconjchem.6b00138
4. Vidal, G., Blanchi, T., Mieszawska, A. J., Calabrese, R., Rossi, C., Vigneron, P., Duval, J. L., Kaplan, D. L., and Egles, C. (2013) Enhanced cellular adhesion on titanium by silk functionalized with titanium binding and RGD peptides Acta Biomater. 9, 4935-4943 10.1016/j.actbio.2012.09.003
5. Chen, A. Y., Deng, Z., Billings, A. N., Seker, U. O. S., Lu, M. Y., Citorik, R. J., Zakeri, B., and Lu, T. K. (2014) Synthesis and patterning of tunable multiscale materials with engineered cells Nat. Mater. 13, 515-23 10.1038/nmat3912
6. Nguyen, P. Q., Botyanszki, Z., Tay, P. K. R., and Joshi, N. S. (2014) Programmable biofilm-based materials from engineered curli nanofibres Nat. Commun. 5, 4945 10.1038/ncomms5945
7. Myhrvold, C., Polka, J. K., and Silver, P. A. (2016) Synthetic Lipid-Containing Scaffolds Enhance Production by Colocalizing Enzymes ACS Synth. Biol. 5, 1396-1403 10.1021/acssynbio.6b00141
8. Giessen, T. W. and Silver, P. (2016) A catalytic nanoreactor based on in vivo encapsulation of multiple enzymes in an engineered protein nanocompartment ChemBioChem 17, 1931-1935 10.1002/cbic.201600431
9. Brune, K. D., Leneghan, D. B., Brian, I. J., Ishizuka, A. S., Bachmann, M. F., Draper, S. J., Biswas, S., and Howarth, M. (2016) Plug-and-Display: decoration of Virus-Like Particles via isopeptide bonds for modular immunization Sci. Rep. 6, 19234 10.1038/srep19234
10. Thrane, S., Janitzek, C. M., Matondo, S., Resende, M., Gustavsson, T., de Jongh, W. A., Clemmensen, S., Roeffen, W., van de Vegte-Bolmer, M., van Gemert, G. J., Sauerwein, R., Schiller, J. T., Nielsen, M. A., Theander, T. G., Salanti, A., and Sander, A. F. (2016) Bacterial superglue enables easy development of efficient virus-like particle based vaccines J. Nanobiotechnol. 14, 30 10.1186/s12951-016-0181-1
11. Liu, Z., Zhou, H., Wang, W., Tan, W., Fu, Y.-X., and Zhu, M. (2014) A novel method for synthetic vaccine construction based on protein assembly Sci. Rep. 4, 7266 10.1038/srep07266
12. Kan, S.-H., Aoyagi-Scharber, M., Le, S. Q., Vincelette, J., Ohmi, K., Bullens, S., Wendt, D. J., Christianson, T. M., Tiger, P. M. N., Brown, J. R., Lawrence, R., Yip, B. K., Holtzinger, J., Bagri, A., Crippen-Harmon, D., Vondrak, K. N., Chen, Z., Hague, C. M., Woloszynek, J. C., Cheung, D. S., Webster, K. A., Adintori, E. G., Lo, M. J., Wong, W., Fitzpatrick, P. A., LeBowitz, J. H., Crawford, B. E., Bunting, S., Dickson, P. I., and Neufeld, E. F. (2014) Delivery of an enzyme-IGFII fusion protein to the mouse brain is therapeutic for mucopolysaccharidosis type IIIB Proc. Natl. Acad. Sci. U. S. A. 111, 14870-5 10.1073/pnas.1416660111
13. Chen, X., Zaro, J. L., and Shen, W.-C. (2013) Fusion protein linkers: property, design and functionality Adv. Drug Delivery Rev. 65, 1357-69 10.1016/j.addr.2012.09.039
14. Yang, H., Liu, L., and Xu, F. (2016) The promises and challenges of fusion constructs in protein biochemistry and enzymology Appl. Microbiol. Biotechnol. 100, 8273-8281 10.1007/s00253-016-7795-y
15. Albayrak, C. and Swartz, J. R. (2014) Direct polymerization of proteins ACS Synth. Biol. 3, 353-62 10.1021/sb400116x
16. Zhang, M., Lin, S., Song, X., Liu, J., Fu, Y., Ge, X., Fu, X., Chang, Z., and Chen, P. R. (2011) A genetically incorporated crosslinker reveals chaperone cooperation in acid resistance Nat. Chem. Biol. 7, 671-7 10.1038/nchembio.644
17. Hudak, J. E., Barfield, R. M., Dehart, G. W., Grob, P., Nogales, E., Bertozzi, C. R., and Rabuka, D. (2012) Synthesis of heterobifunctional protein fusions using copper-free click chemistry and the aldehyde tag Angew. Chem., Int. Ed. 51, 4161-4165 10.1002/anie.201108130
18. Zakeri, B., Fierer, J. O., Celik, E., Chittock, E. C., Schwarz-Linek, U., Moy, V. T., and Howarth, M. (2012) Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin Proc. Natl. Acad. Sci. U. S. A. 109, E690 10.1073/pnas.1115485109
19. Zhang, W.-B., Sun, F., Tirrell, D. a, and Arnold, F. H. (2013) Controlling macromolecular topology with genetically encoded SpyTag-SpyCatcher chemistry J. Am. Chem. Soc. 135, 13988-97 10.1021/ja4076452
20. Veggiani, G., Nakamura, T., Brenner, M. D., Gayet, R. V., Yan, J., Robinson, C. V., and Howarth, M. (2016) Programmable polyproteams built using twin peptide superglues Proc. Natl. Acad. Sci. U. S. A. 113, 1202-7 10.1073/pnas.1519214113
21. Wang, X. W. and Zhang, W. B. (2016) Cellular Synthesis of Protein Catenanes Angew. Chem., Int. Ed. 55, 3442-3446 10.1002/anie.201511640
22. Sun, F., Zhang, W.-B., Mahdavi, A., Arnold, F. H., and Tirrell, D. a. (2014) Synthesis of bioactive protein hydrogels by genetically encoded SpyTag-SpyCatcher chemistry Proc. Natl. Acad. Sci. U. S. A. 111, 11269 10.1073/pnas.1401291111
23. Botyanszki, Z., Tay, P. K. R., Nguyen, P. Q., Nussbaumer, M. G., and Joshi, N. S. (2015) Engineered catalytic biofilms: Site-specific enzyme immobilization onto E. coli curli nanofibers Biotechnol. Bioeng. 110, 2016-2024 10.1002/bit.25638
24. Gao, X., Fang, J., Xue, B., Fu, L., and Li, H. (2016) Engineering Protein Hydrogels Using SpyCatcher-SpyTag Chemistry Biomacromolecules 17, 2812-2819 10.1021/acs.biomac.6b00566
25. Dorval Courchesne, N.-M., Duraj-Thatte, A., Tay, P. K. R., Nguyen, P. Q., and Joshi, N. S. (2016) Scalable Production of Genetically Engineered Nanofibrous Macroscopic Materials via Filtration ACS Biomater. Sci. Eng. 10.1021/acsbiomaterials.6b00437
26. Schoene, C., Fierer, J. O., Bennett, S. P., and Howarth, M. (2014) SpyTag/SpyCatcher cyclization confers resilience to boiling on a mesophilic enzyme Angew. Chem., Int. Ed. 53, 6101-4 10.1002/anie.201402519
27. Wang, J., Wang, Y., Wang, X., Zhang, D., Wu, S., and Zhang, G. (2016) Enhanced thermal stability of lichenase from Bacillus subtilis 168 by SpyTag/SpyCatcher-mediated spontaneous cyclization Biotechnol. Biofuels 9, 79 10.1186/s13068-016-0490-5
28. Schoene, C., Bennett, S. P., and Howarth, M. (2016) SpyRing interrogation: analyzing how enzyme resilience can be achieved with phytase and distinct cyclization chemistries Sci. Rep. 6, 1-12 10.1038/srep21151
29. Alves, N. J., Turner, K. B., Daniele, M. A., Oh, E., Medintz, I. L., and Walper, S. A. (2015) Bacterial Nanobioreactors-Directing Enzyme Packaging into Bacterial Outer Membrane Vesicles ACS Appl. Mater. Interfaces 7, 24963-24972 10.1021/acsami.5b08811
30. Alves, N. J., Turner, K. B., Medintz, I. L., and Walper, S. A. (2016) Protecting enzymatic function through directed packaging into bacterial outer membrane vesicles Sci. Rep. 6, 24866 10.1038/srep24866
31. Fierer, J. O., Veggiani, G., and Howarth, M. (2014) SpyLigase peptide-peptide ligation polymerizes affibodies to enhance magnetic cancer cell capture Proc. Natl. Acad. Sci. U. S. A. 111, E1176-81 10.1073/pnas.1315776111
32. Lakshmanan, A., Farhadi, A., Nety, S. P., Lee-Gosselin, A., Bourdeau, R. W., Maresca, D., and Shapiro, M. G. (2016) Molecular Engineering of Acoustic Protein Nanostructures ACS Nano 10, 7314-7322 10.1021/acsnano.6b03364
33. Bedbrook, C. N., Kato, M., Ravindra kumar, S., Lakshmanan, A., Nath, R. D., Sun, F., Sternberg, P. W., Arnold, F. H., and Gradinaru, V. (2015) Genetically Encoded Spy Peptide Fusion System to Detect Plasma Membrane-Localized Proteins In Vivo Chem. Biol. 22, 1108-1121 10.1016/j.chembiol.2015.06.020
34. Moon, H., Bae, Y., Kim, H., and Kang, S. (2016) Plug-and-playable fluorescent cell imaging modular toolkits using the bacterial superglue, SpyTag/SpyCatcher Chem. Commun. 52, 14051-14054 10.1039/C6CC07363H
35. Dovala, D., Sawyer, W. S., Rath, C. M., and Metzger, L. E. (2016) Rapid analysis of protein expression and solubility with the SpyTag-SpyCatcher system Protein Expression Purif. 117, 44-51 10.1016/j.pep.2015.09.021
36. Schloss, A. C., Liu, W., Williams, D. M., Kaufman, G., Hendrickson, H. P., Rudshteyn, B., Fu, L., Wang, H., Batista, V. S., Osuji, C., Yan, E. C. Y., and Regan, L. (2016) Fabrication of Modularly Functionalizable Microcapsules Using Protein-Based Technologies ACS Biomater. Sci. Eng. 2, 1856 10.1021/acsbiomaterials.6b00447
37. Peschke, T., Rabe, K. S., and Niemeyer, C. M. (2017) Orthogonal Surface Tags for Whole-Cell Biocatalysis Angew. Chem., Int. Ed. 56, 1-5 10.1002/anie.201609590
38. Mergulhão, F. J. M., Summers, D. K., and Monteiro, G. a. (2005) Recombinant protein secretion in Escherichia coli Biotechnol. Adv. 23, 177-202 10.1016/j.biotechadv.2004.11.003
39. Azam, A., Li, C., Metcalf, K. J., and Tullman-Ercek, D. (2016) Type III Secretion as a Generalizable Strategy for the Production of Full-Length Biopolymer-Forming Proteins Biotechnol. Bioeng. 113, 1-8 10.1002/bit.25656
40. Goers, L., Freemont, P., and Polizzi, K. M. (2014) Co-culture systems and technologies: taking synthetic biology to the next level J. R. Soc., Interface 11, 20140065 10.1098/rsif.2014.0065
41. Hays, S. G., Patrick, W. G., Ziesack, M., Oxman, N., and Silver, P. A. (2015) Better together: Engineering and application of microbial symbioses Curr. Opin. Biotechnol. 36, 40-49 10.1016/j.copbio.2015.08.008
42. Zhou, K., Qiao, K., Edgar, S., and Stephanopoulos, G. (2015) Distributing a metabolic pathway among a microbial consortium enhances production of natural products Nat. Biotechnol. 33, 377-383 10.1038/nbt.3095
43. Brenner, K., You, L., and Arnold, F. H. (2008) Engineering microbial consortia: a new frontier in synthetic biology Trends Biotechnol. 26, 483-9 10.1016/j.tibtech.2008.05.004
44. Jones, J. A., Vernacchio, V. R., Sinkoe, A. L., Collins, S. M., Ibrahim, M. H. A., Lachance, D. M., Hahn, J., and Koffas, M. A. G. (2016) Experimental and computational optimization of an Escherichia coli co-culture for the efficient production of flavonoids Metab. Eng. 35, 55-63 10.1016/j.ymben.2016.01.006
45. Harwood, C. R. and Cranenburgh, R. (2008) Bacillus protein secretion: an unfolding story Trends Microbiol. 16, 73-79 10.1016/j.tim.2007.12.001
46. van Dijl, J. M. and Hecker, M. (2013) Bacillus subtilis: from soil bacterium to super-secreting cell factory Microb. Cell Fact. 12, 3 10.1186/1475-2859-12-3
47. Scott, C. P., Abel-Santos, E., Wall, M., Wahnon, D. C., and Benkovic, S. J. (1999) Production of cyclic peptides and proteins in vivo Proc. Natl. Acad. Sci. U. S. A. 96, 13638-13643 10.1073/pnas.96.24.13638
48. Trabi, M. and Craik, D. J. (2002) Circular proteins-no end in sight Trends Biochem. Sci. 27, 132-138 10.1016/S0968-0004(02)02057-1
49. Iwai, H. and Plu, A. (1999) Circular L-lactamase: stability enhancement by cyclizing the backbone FEBS Lett. 459, 166-172 10.1016/S0014-5793(99)01220-X
50. Waldhauer, M. C., Schmitz, S. N., Ahlmann-Eltze, C., Gleixner, J. G., Schmelas, C. C., Huhn, A. G., Bunne, C., Büscher, M., Horn, M., Klughammer, N., Kreft, J., Schäfer, E., Bayer, P. A., Krämer, S. G., Neugebauer, J., Wehler, P., Mayer, M. P., Eils, R., and Di Ventura, B. (2015) Backbone circularization of Bacillus subtilis family 11 xylanase increases its thermostability and its resistance against aggregation Mol. BioSyst. 11, 3231-43 10.1039/C5MB00341E
51. Schoene, C., Bennett, S. P., and Howarth, M. (2016) SpyRings Declassified: A Blueprint for Using Isopeptide-Mediated Cyclization to Enhance Enzyme Thermal Resilience. In Pept. Protein Enzym. Des., 1 st ed., Elsevier Inc.
52. Kumar, V., Marín-Navarro, J., and Shukla, P. (2016) Thermostable microbial xylanases for pulp and paper industries: trends, applications and further perspectives World J. Microbiol. Biotechnol. 32, 1-10 10.1007/s11274-015-2005-0
53. Juturu, V. and Wu, J. C. (2012) Microbial xylanases: Engineering, production and industrial applications Biotechnol. Adv. 30, 1219-1227 10.1016/j.biotechadv.2011.11.006
54. Kuhad, R. C., Gupta, R., and Singh, A. (2011) Microbial cellulases and their industrial applications Enzyme Res. 2011, 280696 10.4061/2011/280696
55. Zhang, X. Z. and Zhang, Y. H. P. (2010) One-step production of biocommodities from lignocellulosic biomass by recombinant cellulolytic Bacillus subtilis: Opportunities and challenges Eng. Life Sci. 10, 398-406 10.1002/elsc.201000011
56. Moraïs, S., Barak, Y., Caspi, J., and Hadar, Y. (2010) Cellulase-xylanase synergy in designer cellulosomes for enhanced degradation of a complex cellulosic substrate mBio 1, 3-10 10.1128/mBio.00285-10
57. Fontes, C. M. G. A. and Gilbert, H. J. (2010) Cellulosomes: Highly Efficient Nanomachines Designed to Deconstruct Plant Cell Wall Complex Carbohydrates Annu. Rev. Biochem. 79, 655-681 10.1146/annurev-biochem-091208-085603
58. Arai, T., Matsuoka, S., Cho, H.-Y., Yukawa, H., Inui, M., Wong, S.-L., and Doi, R. H. (2007) Synthesis of Clostridium cellulovorans minicellulosomes by intercellular complementation Proc. Natl. Acad. Sci. U. S. A. 104, 1456-1460 10.1073/pnas.0610740104
59. Moraïs, S., Shterzer, N., Lamed, R., Bayer, E. A., and Mizrahi, I. (2014) A combined cell-consortium approach for lignocellulose degradation by specialized Lactobacillus plantarum cells Biotechnol. Biofuels 7, 112 10.1186/1754-6834-7-112
60. Stahl, S. W., Nash, M. A., Fried, D. B., Slutzki, M., Barak, Y., Bayer, E. A., and Gaub, H. E. (2012) Single-molecule dissection of the high-affinity cohesin-dockerin complex Proc. Natl. Acad. Sci. U. S. A. 109, 20431-20436 10.1073/pnas.1211929109
61. Bellingham, C. M., Woodhouse, K. A., Robson, P., Rothstein, S. J., and Keeley, F. W. (2001) Self-aggregation characteristics of recombinantly expressed human elastin polypeptides Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1550, 6-19 10.1016/S0167-4838(01)00262-X
62. Scott, S. R. and Hasty, J. (2016) Quorum Sensing Communication Modules for Microbial Consortia ACS Synth. Biol. 5, 969-977 10.1021/acssynbio.5b00286
63. Abe, H., Wakabayashi, R., Yonemura, H., Yamada, S., Goto, M., and Kamiya, N. (2013) Split Spy0128 as a potent scaffold for protein cross-linking and immobilization Bioconjugate Chem. 24, 242-250 10.1021/bc300606b
64. Woolfson, D. N. (2005) The design of coiled-coil structures and assemblies Adv. Protein Chem. 70, 79 10.1016/S0065-3233(05)70004-8
65. Lee, M. E., DeLoache, W. C., Cervantes, B., and Dueber, J. E. (2015) A Highly-characterized Yeast Toolkit for Modular, Multi-part Assembly ACS Synth. Biol. 4, 975-986 10.1021/sb500366v
66. Cormack, B. P., Valdivia, R. H., and Falkow, S. (1996) FACS-optimized mutants of the green fluorescent protein (GFP) Gene 173, 33-38 10.1016/0378-1119(95)00685-0
67. Li, L., Fierer, J. O., Rapoport, T. a, and Howarth, M. (2014) Structural analysis and optimization of the covalent association between SpyCatcher and a peptide Tag J. Mol. Biol. 426, 309-17 10.1016/j.jmb.2013.10.021