Browse > Article
http://dx.doi.org/10.4014/jmb.1807.06066

Bacillus subtilis Spore Surface Display Technology: A Review of Its Development and Applications  

Zhang, Guoyan (School of Food and Biological Engineering, Jiangsu University)
An, Yingfeng (College of Biosciences and Biotechnology, Shenyang Agricultural University)
Zabed, Hossain M. (School of Food and Biological Engineering, Jiangsu University)
Guo, Qi (School of Food and Biological Engineering, Jiangsu University)
Yang, Miaomiao (School of Food and Biological Engineering, Jiangsu University)
Yuan, Jiao (School of Food and Biological Engineering, Jiangsu University)
Li, Wen (School of Food and Biological Engineering, Jiangsu University)
Sun, Wenjin (School of Food and Biological Engineering, Jiangsu University)
Qi, Xianghui (School of Food and Biological Engineering, Jiangsu University)
Publication Information
Journal of Microbiology and Biotechnology / v.29, no.2, 2019 , pp. 179-190 More about this Journal
Abstract
Bacillus subtilis spore surface display (BSSD) technology is considered to be one of the most promising approaches for expressing heterologous proteins with high activity and stability. Currently, this technology is used for various purposes, such as the production of enzymes, oral vaccines, drugs and multimeric proteins, and the control of environmental pollution. This paper presents an overview of the latest developments in BSSD technology and its application in protein engineering. Finally, the major limitations of this technology and future directions for its research are discussed.
Keywords
Bacillus subtilis; spore surface display technology; biocatalysis; gene engineering; anchor protein; linker peptide;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Sibley L, Reljic R, Radford DS, Huang JM, Hong HA, Cranenburgh RM, et al. 2014. Recombinant Bacillus subtilis spores expressing MPT64 evaluated as a vaccine against tuberculosis in the murine model. FEMS Microbiol. Lett. 358: 170-179.   DOI
2 Nguyen QA, Schumann W. 2014. Use of IPTG-inducible promoters for anchoring recombinant proteins on the Bacillus subtilis spore surface. Protein Expr. Purif. 95: 67-76.   DOI
3 Hinc K, Stasilojc M, Piatek I, Peszynska-Sularz G, Isticato R, Ricca E, et al. 2014. Mucosal adjuvant activity of IL-2 presenting spores of bacillus subtilis in a murine model of Helicobacter pylori vaccination. PLoS One 9: e95187.   DOI
4 Chen H, Zhang T, Jia J, Vastermark A, Tian R, Ni Z, et al. 2015. Expression and display of a novel thermostable esterase from Clostridium thermocellum on the surface of Bacillus subtilis using the CotB anchor protein. J. Ind. Microbiol. Biotechnol. 42: 1439-1448.   DOI
5 Chen H, Tian R, Ni Z, Zhang Q, Zhang T, Chen Z, et al. 2015. Surface display of the thermophilic lipase Tm1350 on the spore of Bacillus subtilis by the CotB anchor protein. Extremophiles 19: 799-808.   DOI
6 Mauriello EM, Duc le H, Isticato R, Cangiano G, Hong HA, De Felice M, et al. 2004. Display of heterologous antigens on the Bacillus subtilis spore coat using CotC as a fusion partner. Vaccine 22: 1177-1187.   DOI
7 Falahati-Pour SK, Lotfi AS, Ahmadian G, Baghizadeh A. 2015. Covalent immobilization of recombinant organophosphorus hydrolase on spores of Bacillus subtilis. J. Appl. Microbiol. 118: 976-988.   DOI
8 Hinc K, Ghandili S, Karbalaee G, Shali A, Noghabi KA, Ricca E, et al. 2010. Efficient binding of nickel ions to recombinant Bacillus subtilis spores. Res. Microbiol. 161: 757-764.   DOI
9 Cho EA, Seo J, Lee DW, Pan JG. 2011. Decolorization of indigo carmine by laccase displayed on Bacillus subtilis spores. Enzyme Microb. Technol. 49: 100-104.   DOI
10 Hwang BY, Kim BG, Kim JH. 2011. Bacterial surface display of a co-factor containing enzyme, $\omega$-transaminase from Vibrio fluvialis using the Bacillus subtilis spore display system. Biosci.Biotechnol. Biochem. 75: 1862-1865.   DOI
11 Kim JH, Lee CS, Kim BG. 2005. Spore-displayed streptavidin: a live diagnostic tool in biotechnology. Biochem. Biophys. Res. Commun. 331: 210-214.   DOI
12 Kwon SJ, Jung HC, Pan JG. 2007. Transgalactosylation in a water-solvent biphasic reaction system with $\beta$-galactosidase displayed on the surfaces of Bacillus subtilis spores. Appl. Environ. Microbiol. 73: 2251-2256.   DOI
13 Isticato R, Ricca E. 2014. Spore Surface Display. Microbiol. Spectr. 2(5).
14 JinaCheon, Bokim S, Wonpark S, Kwonhan J, Pil Kim. 2009. Characterization of L-arabinose isomerase in Bacillus subtilis, a GRAS host, for the production of edible tagatose. Food Biotechnol. 23: 8-16.   DOI
15 Isticato R, Cangiano G, Tran HT, Ciabattini A, Medaglini D, Oggioni MR, et al. 2001. Surface display of recombinant proteins on Bacillus subtilis spores. J. Bacteriol. 183: 6294-6301.   DOI
16 Wang H, Wang Y, Yang R. 2017. Recent progress in Bacillus subtilis spore-surface display: concept, progress, and future. Appl. Microbiol. Biotechnol. 101: 933-949.   DOI
17 Tan IS, Ramamurthi KS. 2014. Spore formation in Bacillus subtilis. Environ. Microbiol. Rep. 6: 212-225.   DOI
18 Setlow P. 2007. I will survive: DNA protection in bacterial spores. Trends Microbiol. 15: 172-180.   DOI
19 Moeller R, Schuerger AC, Reitz G, Nicholson WL. 2012. Protective role of spore structural components in determining Bacillus subtilis spore resistance to simulated mars surface conditions. Appl. Environ. Microbiol. 78: 8849-8853.   DOI
20 Guo Q, An Y, Yun J, Yang M, Magocha TA, Zhu J, et al. 2018. Enhanced d-tagatose production by spore surface-displayed l -arabinose isomerase from isolated Lactobacillus brevis PC16 and biotransformation. Bioresour. Technol. 247: 940-946.   DOI
21 Dai X, Liu M, Pan K, Yang J. 2018. Surface display of OmpC of Salmonella serovar Pullorum on Bacillus subtilis spores. PLoS One 13: e0191627.   DOI
22 Rostami A, Hinc K, Goshadrou F, Shali A, Bayat M, Hassanzadeh M, et al. 2017. Display of B. pumilus chitinase on the surface of B. subtilis spore as a potential biopesticide. Pestic Biochem. Physiol. 140: 17-23.   DOI
23 Duc le H, Hong HA, Atkins HS, Flick-Smith HC, Durrani Z, Rijpkema S, et al. 2007. Immunization against anthrax using Bacillus subtilis spores expressing the anthrax protective antigen. Vaccine 25: 346-355.   DOI
24 Yuan Y, Feng F, Chen L, Yao Q, Chen K. 2013. Surface display of Acetobacter pasteurianus AdhA on Bacillus subtilis spores to enhance ethanol tolerance for liquor industrial potential. Eur. Food Res. Technol. 238: 285-293.   DOI
25 Negri A, Potocki W, Iwanicki A, Obuchowski M, Hinc K. 2013. Expression and display of Clostridium difficile protein FliD on the surface of Bacillus subtilis spores. J. Med. Microbiol. 62: 1379-1385.   DOI
26 He W, Jiang B, Mu W, Zhang T. 2016. Production of d-allulose with d-psicose 3-epimerase expressed and displayed on the surface of Bacillus subtilis spores. J. Agric. Food Chem. 64: 7201-7207.   DOI
27 Li G, Tang Q, Chen H, Yao Q, Ning D, Chen K. 2011. Display of Bombyx mori nucleopolyhedrovirus GP64 on the Bacillus subtilis spore coat. Curr. Microbiol. 62: 1368-1373.   DOI
28 Tavassoli S, Hinc K, Iwanicki A, Obuchowski M, Ahmadian G. 2013. Investigation of spore coat display of Bacillus subtilis $\beta$-galactosidase for developing of whole cell biocatalyst. Arch. Microbiol. 195: 197-202.   DOI
29 Lian C, Zhou Y, Feng F, Chen L, Tang Q, Yao Q, et al. 2014. Surface display of human growth hormone on Bacillus subtilis spores for oral administration. Curr. Microbiol. 68: 463-471.   DOI
30 Zhou Z, Gong S, Li XM, Yang Y, Guan R, Zhou S, et al. 2015. Expression of Helicobacter pylori urease B on the surface of Bacillus subtilis spores. J. Med. Microbiol. 64: 104-110.   DOI
31 Gao C, Xu X, Zhang X, Che B, Ma C, Qiu J, et al. 2011. Chemoenzymatic synthesis of N-acetyl-D-neuraminic acid from N-acetyl-D-glucosamine by using the spore surface-displayed N-acetyl-D-neuraminic acid aldolase. Appl. Environ. Microbiol. 77: 7080-7083.   DOI
32 Li L, Hu X, Wu Z, Xiong S, Zhou Z, Wang X, et al. 2009. Immunogenicity of self-adjuvanticity oral vaccine candidate based on use of Bacillus subtilis spore displaying Schistosoma japonicum 26 KDa GST protein. Parasitol Res. 105: 1643-1651.   DOI
33 Wang N, Chang C, Yao Q, Li G, Qin L, Chen L, et al. 2011. Display of Bombyx mori alcohol dehydrogenases on the Bacillus subtilis spore surface to enhance enzymatic activity under adverse conditions. PLoS One 6: e21454.   DOI
34 Mao L, Jiang S, Li G, He Y, Chen L, Yao Q, et al. 2012. Surface display of human serum albumin on Bacillus subtilis spores for oral administration. Curr. Microbiol. 64: 545-551.   DOI
35 Zhou Z, Xia H, Hu X, Huang Y, Li Y, Li L, et al. 2008. Oral administration of a Bacillus subtilis spore-based vaccine expressing Clonorchis sinensis tegumental protein 22.3 kDa confers protection against Clonorchis sinensis. Vaccine 26: 1817-1825.   DOI
36 Feng F, Hu P, Chen L, Tang Q, Lian C, Yao Q, et al. 2013. Display of human proinsulin on the Bacillus subtilis spore surface for oral administration. Curr. Microbiol. 67: 1-8.   DOI
37 Cao Y-G, Li Z-H, Yue Y-Y, Song N-N, Peng L, Wang L-X, et al. 2013. Construction and evaluation of a novel Bacillus subtilis spores-based enterovirus 71 vaccine. J. Appl. Biomed. 11: 105-113.   DOI
38 Zhao G, Miao Y, Guo Y, Qiu H, Sun S, Kou Z, et al. 2014. Development of a heat-stable and orally delivered recombinant M2e-expressing B. subtilis spore-based influenza vaccine. Hum. Vaccin Immunother. 10: 3649-3658.   DOI
39 Hosseini-Abari A, Kim BG, Lee SH, Emtiazi G, Kim W, Kim JH. 2016. Surface display of bacterial tyrosinase on spores of Bacillus subtilis using CotE as an anchor protein. J. Basic Microbiol. 56: 1331-1337..   DOI
40 Hwang BY, Pan JG, Kim BG, Kim JH. 2013. Functional display of active tetrameric beta-galactosidase using Bacillus subtilis spore display system. J. Nanosci. Nanotechnol. 13: 2313-2319.   DOI
41 Iwanicki A, Piatek I, Stasilojc M, Grela A, Lega T, Obuchowski M, et al. 2014. A system of vectors for Bacillus subtilis spore surface display. Microbial. Cell Fact. 13: 30.   DOI
42 GP S. 1985. Filamentous fusion phage novel expression vectors that display cloned antigens on the virion surface. Science 228: 1315-1317.   DOI
43 Qu Y, Wang J, Zhang Z, Shi S, Li D, Shen W, et al. 2014. Catalytic transformation of HODAs using an efficient meta-cleavage product hydrolase-spore surface display system. J. Mol. Catal. 102: 204-210.   DOI
44 Chen H, Chen Z, Ni Z, Tian R, Zhang T, Jia J, et al. 2016. Display of Thermotoga maritima MSB8 nitrilase on the spore surface of Bacillus subtilis using out coat protein CotG as the fusion partner. J. Mol. Catal. 123: 73-80.   DOI
45 Potot S, Serra CR, Henriques AO, Schyns G. 2010. Display of recombinant proteins on Bacillus subtilis spores, using a coat-associated enzyme as the carrier. Appl. Environ. Microbiol. 76: 5926-5933.   DOI
46 Lindborg M, Magnusson CG, Zargari A, Schmidt M, Scheynius A, Crameri R, et al. 1999. Selective cloning of allergens from the skin colonizing yeast Malassezia furfur by phage surface display technology. J. Invest. Dermatol. 113: 156-161.   DOI
47 Wang H, Yang R, Hua X, Zhang W, Zhao W. 2016. Production using the CotX-mediated spore-displayed beta-galactosidase as a biocatalyst. J. Microbiol. Biotechnol. 26: 1267-1277.   DOI
48 Hinc K, Iwanicki A, Obuchowski M. 2013. New stable anchor protein and peptide linker suitable for successful spore surface display in B. subtilis. Microb. Cell Fact. 12: 22.   DOI
49 Gupta N, Farinas ET. 2010. Directed evolution of CotA laccase for increased substrate specificity using Bacillus subtilis spores. Protein Eng. Des. Sel. 23: 679-682.   DOI
50 Gwak S, Almirall JR. 2015. Rapid screening of 35 new psychoactive substances by ion mobility spectrometry (IMS) and direct analysis in real time (DART) coupled to quadrupole time-of-flight mass spectrometry (QTOF-MS). Drug Test. Anal. 7: 884-893.   DOI
51 Wang H, Yang R, Hua X, Zhao W, Zhang W. 2015. Functional display of active $\beta$-galactosidase on Bacillus subtilis spores using crust proteins as carriers. Food Sci. Biotechnol. 24: 1755-1759.   DOI
52 Huang Z, Li G, Zhang C, Xing XH. 2016. A study on the effects of linker flexibility on acid phosphatase PhoC-GFP fusion protein using a novel linker library. Enzyme Microb. Technol. 83: 1-6.   DOI
53 Potocki W, Negri A, Peszynska-Sularz G, Hinc K, Obuchowski M, Iwanicki A. 2017. The combination of recombinant and non-recombinant Bacillus subtilis spore display technology for presentation of antigen and adjuvant on single spore. Microb. Cell Fact. 16: 151.   DOI
54 Zhang Z, Liu J, Fan J, Wang Z, Li L. 2018. Detection of catechol using an electrochemical biosensor based on engineered Escherichia coli cells that surface-display laccase. Anal. Chim. Acta 1009: 65-72.   DOI
55 Xu X, Gao C, Zhang X, Che B, Ma C, Qiu J, et al. 2011. Production of N-acetyl-D-neuraminic acid by use of an efficient spore surface display system. Appl. Environ. Microbiol. 77: 3197-3201.   DOI
56 Liu Y, Li S, Xu H, Wu L, Xu Z, Liu J, et al. 2014. Efficient production of D-tagatose using a food-grade surface display system. J. Agric. Food Chem. 62: 6756-6762.   DOI
57 Wittmann A, Suess B. 2012. Engineered riboswitches: Expanding researchers' toolbox with synthetic RNA regulators. FEBS Lett. 586: 2076-2083.   DOI
58 Auer TO, Duroure K, De Cian A, Concordet JP, Del Bene F. 2014. Highly efficient CRISPR/Cas9-mediated knock-in in zebrafish by homology-independent DNA repair. Genome Res. 24: 142-153.   DOI
59 Duc LH, Hong HA, Fairweather N, Ricca E, Cutting SM. 2003. Bacterial Spores as Vaccine Vehicles. Infect. Immun. 71: 2810-2818.   DOI
60 Fantino JR, Barras F, Denizot F. 2009. Sposensor: a whole-bacterial biosensor that uses immobilized Bacillus subtilis spores and a one-step incubation/detection process. J. Mol. Microbiol. Biotechnol. 17: 90-95.   DOI
61 Hoang TH, Hong HA, Clark GC, Titball RW, Cutting SM. 2008. Recombinant Bacillus subtilis expressing the Clostridium perfringens alpha toxoid is a candidate orally delivered vaccine against necrotic enteritis. Infect. Immun. 76: 5257-5265.   DOI
62 Hinc K, Isticato R, Dembek M, Karczewska J, Iwanicki A, Peszynska-Sularz G, et al. 2010. Expression and display of UreA of Helicobacter acinonychis on the surface of Bacillus subtilis spores. Microb. Cell Fact. 9: 2.   DOI
63 Sun H, Lin Z, Zhao L, Chen T, Shang M, Jiang H, et al. 2018. Bacillus subtilis spore with surface display of paramyosin from Clonorchis sinensis potentializes a promising oral vaccine candidate. Parasit. Vectors. 11: 156.   DOI
64 Uyen NQ, Hong HA, Cutting SM. 2007. Enhanced immunisation and expression strategies using bacterial spores as heat-stable vaccine delivery vehicles. Vaccine 25: 356-365.   DOI
65 Ciabattini A, Parigi R, Isticato R, Oggioni MR, Pozzi G. 2004. Oral priming of mice by recombinant spores of Bacillus subtilis. Vaccine 22: 4139-4143.   DOI
66 Nguyen AT, Pham CK, Pham HT, Pham HL, Nguyen AH, Dang LT, et al. 2014. Bacillus subtilis spores expressing the VP28 antigen: a potential oral treatment to protect Litopenaeus vannamei against white spot syndrome. FEMS Microbiol Lett. 358: 202-208.   DOI
67 Wang X, Chen W, Tian Y, Mao Q, Lv X, Shang M, et al. 2014. Surface display of Clonorchis sinensis enolase on Bacillus subtilis spores potentializes an oral vaccine candidate. Vaccine 32: 1338-1345.   DOI
68 Li W, Xu H, Xiao T, Cong L, Love MI, Zhang F, et al. 2014. MAGeCK enables robust identification of essential genes from genome-scale CRISPR/Cas9 knockout screens. Genome Biol. 15: 554.   DOI
69 ET B, KD W. 1997. Yeast surface display for screening combinatorial polypeptide libraries. Nature Biotechnol. 15: 553-557.   DOI
70 Hu S, Kong J, Sun Z, Han L, Kong W, Yang P. 2011. Heterologous protein display on the cell surface of lactic acid bacteria mediated by the s-layer protein. Microb. Cell Fact. 10: 86-86.   DOI
71 Tavares Batista M, Souza RD, Paccez JD, Luiz WB, Ferreira EL, Cavalcante RC, et al. 2014. Gut adhesive Bacillus subtilis spores as a platform for mucosal delivery of antigens. Infect. Immun. 82: 1414-1423.   DOI
72 Permpoonpattana P, Hong HA, Phetcharaburanin J, Huang JM, Cook J, Fairweather NF, et al. 2011. Immunization with Bacillus spores expressing toxin A peptide repeats protects against infection with Clostridium difficile strains producing toxins A and B. Infect. Immun. 79: 2295-2302.   DOI