1932

Abstract

has become a widely used microbial cell factory for the production of recombinant proteins, especially those associated with foods and food processing. Recent advances in genetic manipulation and proteomic analysis have been used to greatly improve protein production in . This review begins with a discussion of genome-editing technologies and application of the CRISPR–Cas9 system to . A summary of the characteristics of crucial legacy strains is followed by suggestions regarding the choice of origin strain for genetic manipulation. Finally, the review analyzes the genes and operons of that are important for the production of secretory proteins and provides suggestions and examples of how they can be altered to improve protein production. This review is intended to promote the engineering of this valuable microbial cell factory for better recombinant protein production.

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2020-03-25
2024-06-24
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Literature Cited

  1. Akopian D, Shen K, Zhang X, Shan SO 2013. Signal recognition particle: an essential protein-targeting machine. Annu. Rev. Biochem. 82:693–721
    [Google Scholar]
  2. Altenbuchner J. 2016. Editing of the Bacillus subtilis genome by the CRISPR-Cas9 system. Appl. Environ. Microbiol. 82:5421–27
    [Google Scholar]
  3. Baker D, Sohl JL, Agard DA 1992. A protein-folding reaction under kinetic control. Nature 356:263–65
    [Google Scholar]
  4. Belitsky BR, Sonenshein AL. 1998. Role and regulation of Bacillus subtilis glutamate dehydrogenase genes. J. Bacteriol. 180:6298–305
    [Google Scholar]
  5. Berks BC, Palmer T, Sargent F 2003. The Tat protein translocation pathway and its role in microbial physiology. Adv. Microb. Physiol. 47:187–254
    [Google Scholar]
  6. Bisicchia P, Noone D, Lioliou E, Howell A, Quigley S et al. 2007. The essential YycFG two-component system controls cell wall metabolism in Bacillus subtilis. Mol. Microbiol 65:180–200
    [Google Scholar]
  7. Blackman SA, Smith TJ, Foster SJ 1998. The role of autolysins during vegetative growth of Bacillus subtilis 168. Microbiology 144:73–82
    [Google Scholar]
  8. Bolhuis A, Matzen A, Hyyrylainen HL, Kontinen VP, Meima R et al. 1999a. Signal peptide peptidase- and ClpP-like proteins of Bacillus subtilis required for efficient translocation and processing of secretory proteins. J. Biol. Chem. 274:24585–92
    [Google Scholar]
  9. Bolhuis A, Venema G, Quax WJ, Bron S, van Dijl JM 1999b. Functional analysis of paralogous thiol-disulfide oxidoreductases in Bacillus subtilis. J. Biol. Chem 274:24531–38
    [Google Scholar]
  10. Brockmeier U, Caspers M, Freudl R, Jockwer A, Noll T, Eggert T 2006. Systematic screening of all signal peptides from Bacillus subtilis: a powerful strategy in optimizing heterologous protein secretion in Gram-positive bacteria. J. Mol. Biol. 362:393–402
    [Google Scholar]
  11. Burkholder PR, Giles NH Jr 1947. Induced biochemical mutations in Bacillus subtilis. Am. J. . Bot 34:345–48
    [Google Scholar]
  12. Cai D, Wang H, He P, Zhu C, Wang Q et al. 2017. A novel strategy to improve protein secretion via overexpression of the SppA signal peptide peptidase in Bacillus licheniformis. Microb. Cell Fact 16:70
    [Google Scholar]
  13. Cai D, Wei X, Qiu Y, Chen Y, Chen J et al. 2016. High-level expression of nattokinase in Bacillus licheniformis by manipulating signal peptide and signal peptidase. J. Appl. Microbiol. 121:704–12
    [Google Scholar]
  14. Caspers M, Brockmeier U, Degering C, Eggert T, Freudl R 2010. Improvement of Sec-dependent secretion of a heterologous model protein in Bacillus subtilis by saturation mutagenesis of the N-domain of the AmyE signal peptide. Appl. Microbiol. Biotechnol. 86:1877–85
    [Google Scholar]
  15. Chambert R, Benyahia F, Petit-Glatron MF 1990. Secretion of Bacillus subtilis levansucrase. Fe(III) could act as a cofactor in an efficient coupling of the folding and translocation processes. Biochem. J. 265:375–82
    [Google Scholar]
  16. Chen J, Fu G, Gai Y, Zheng P, Zhang D, Wen J 2015. Combinatorial Sec pathway analysis for improved heterologous protein secretion in Bacillus subtilis: identification of bottlenecks by systematic gene overexpression. Microb. Cell Fact. 14:92
    [Google Scholar]
  17. Chen R, Guttenplan SB, Blair KM, Kearns DB 2009. Role of the σD-dependent autolysins in Bacillus subtilis population heterogeneity. J. Bacteriol. 191:5775–84
    [Google Scholar]
  18. Conn HJ. 1930. The identity of Bacillus subtilis. J. Infect. Dis 46:341–50
    [Google Scholar]
  19. Craynest M, Jorgensen S, Sarvas M, Kontinen VP 2003. Enhanced secretion of heterologous cyclodextrin glycosyltransferase by a mutant of Bacillus licheniformis defective in the D-alanylation of teichoic acids. Lett. Appl. Microbiol. 37:75–80
    [Google Scholar]
  20. Darmon E, Dorenbos R, Meens J, Freudl R, Antelmann H et al. 2006. A disulfide bond-containing alkaline phosphatase triggers a BdbC-dependent secretion stress response in Bacillus subtilis. Appl. Environ. . Microbiol 72:6876–85
    [Google Scholar]
  21. Degering C, Eggert T, Puls M, Bongaerts J, Evers S et al. 2010. Optimization of protease secretion in Bacillus subtilis and Bacillus licheniformis by screening of homologous and heterologous signal peptides. Appl. Environ. Microbiol. 76:6370–76
    [Google Scholar]
  22. Deuerling E, Paeslack B, Schumann W 1995. The ftsH gene of Bacillus subtilis is transiently induced after osmotic and temperature upshift. J. Bacteriol. 177:4105–12
    [Google Scholar]
  23. Diao L, Dong Q, Xu Z, Yang S, Zhou J, Freudl R 2012. Functional implementation of the posttranslational SecB–SecA protein-targeting pathway in Bacillus subtilis. Appl. Environ. Microbiol 78:651–59
    [Google Scholar]
  24. Ellis RJ, van der Vies SM 1991. Molecular chaperones. Annu. Rev. Biochem. 60:321–47
    [Google Scholar]
  25. Freudl R. 2018. Signal peptides for recombinant protein secretion in bacterial expression systems. Microb. Cell Fact. 17:52
    [Google Scholar]
  26. Fu G, Liu J, Li J, Zhu B, Zhang D 2018. Systematic screening of optimal signal peptides for secretory production of heterologous proteins in Bacillus subtilis. J. Agric. Food Chem 66:13141–51
    [Google Scholar]
  27. Gallagher T, Gilliland G, Wang L, Bryan P 1995. The prosegment-subtilisin BPN′ complex: crystal structure of a specific “foldase. .” Structure 3:907–14
    [Google Scholar]
  28. Georgopoulos C. 1992. The emergence of the chaperone machines. Trends Biochem. Sci. 17:295–99
    [Google Scholar]
  29. Goosens VJ, De-San-Eustaquio-Campillo A, Carballido-Lopez R, van Dijl JM 2015. A Tat ménage à trois: the role of Bacillus subtilis TatAc in twin-arginine protein translocation. Biochim. Biophys. Acta 1853:2745–53
    [Google Scholar]
  30. Haldenwang WG. 1995. The sigma factors of Bacillus subtilis. Microbiol. Rev 59:1–30
    [Google Scholar]
  31. Harwood CR, Cranenburgh R. 2008. Bacillus protein secretion: an unfolding story. Trends Microbiol 16:73–79
    [Google Scholar]
  32. Hashimoto M, Ooiwa S, Sekiguchi J 2012. Synthetic lethality of the lytE cwlO genotype in Bacillus subtilis is caused by lack of d,l-endopeptidase activity at the lateral cell wall. J. Bacteriol. 194:796–803
    [Google Scholar]
  33. Hirano H, Gootenberg JS, Horii T, Abudayyeh OO, Kimura M et al. 2016. Structure and engineering of Francisella novicida Cas9. Cell 164:950–61
    [Google Scholar]
  34. Homuth G, Masuda S, Mogk A, Kobayashi Y, Schumann W 1997. The dnaK operon of Bacillus subtilis is heptacistronic. J. Bacteriol 179:1153–64
    [Google Scholar]
  35. Hu JH, Miller SM, Geurts MH, Tang W, Chen L et al. 2018. Evolved Cas9 variants with broad PAM compatibility and high DNA specificity. Nature 556:57–63
    [Google Scholar]
  36. Hyyrylainen HL, Bolhuis A, Darmon E, Muukkonen L, Koski P et al. 2001. A novel two-component regulatory system in Bacillus subtilis for the survival of severe secretion stress. Mol. Microbiol. 41:1159–72
    [Google Scholar]
  37. Hyyrylainen HL, Marciniak BC, Dahncke K, Pietiainen M, Courtin P et al. 2010. Penicillin-binding protein folding is dependent on the PrsA peptidyl-prolyl cis-trans isomerase in Bacillus subtilis. Mol. . Microbiol 77:108–27
    [Google Scholar]
  38. Hyyrylainen HL, Pietiainen M, Lunden T, Ekman A, Gardemeister M et al. 2007. The density of negative charge in the cell wall influences two-component signal transduction in Bacillus subtilis. . Microbiology 153:2126–36
    [Google Scholar]
  39. Hyyrylainen HL, Sarvas M, Kontinen VP 2005. Transcriptome analysis of the secretion stress response of Bacillus subtilis. Appl. Microbiol. Biotechnol 67:389–96
    [Google Scholar]
  40. Hyyrylainen HL, Vitikainen M, Thwaite J, Wu H, Sarvas M et al. 2000. d-Alanine substitution of teichoic acids as a modulator of protein folding and stability at the cytoplasmic membrane/cell wall interface of Bacillus subtilis. J. Biol. Chem 275:26696–703
    [Google Scholar]
  41. Iwasaki H, Shimada A, Ito E 1986. Comparative studies of lipoteichoic acids from several Bacillus strains. J. Bacteriol. 167:508–16
    [Google Scholar]
  42. Jia Y, Liu H, Bao W, Weng M, Chen W et al. 2010. Functional analysis of propeptide as an intramolecular chaperone for in vivo folding of subtilisin nattokinase. FEBS Lett 584:4789–96
    [Google Scholar]
  43. Jiang Y, Qian F, Yang J, Liu Y, Dong F et al. 2017. CRISPR-Cpf1 assisted genome editing of Corynebacterium glutamicum. Nat. Commun 8:15179
    [Google Scholar]
  44. Kabisch J, Thurmer A, Hubel T, Popper L, Daniel R, Schweder T 2013. Characterization and optimization of Bacillus subtilis ATCC 6051 as an expression host. J. Biotechnol. 163:97–104
    [Google Scholar]
  45. Kakeshita H, Kageyama Y, Ara K, Ozaki K, Nakamura K 2010. Enhanced extracellular production of heterologous proteins in Bacillus subtilis by deleting the C-terminal region of the SecA secretory machinery. Mol. Biotechnol. 46:250–57
    [Google Scholar]
  46. Konkol MA, Blair KM, Kearns DB 2013. Plasmid-encoded ComI inhibits competence in the ancestral 3610 strain of Bacillus subtilis. J. Bacteriol 195:4085–93
    [Google Scholar]
  47. Kontinen VP, Saris P, Sarvas M 1991. A gene (prsA) of Bacillus subtilis involved in a novel, late stage of protein export. Mol. Microbiol. 5:1273–83
    [Google Scholar]
  48. Kontinen VP, Sarvas M. 1993. The PrsA lipoprotein is essential for protein secretion in Bacillus subtilis and sets a limit for high-level secretion. Mol. Microbiol. 8:727–37
    [Google Scholar]
  49. Kouwen TR, Dubois JY, Freudl R, Quax WJ, van Dijl JM 2008. Modulation of thiol-disulfide oxidoreductases for increased production of disulfide-bond-containing proteins in Bacillus subtilis. Appl. Environ. . Microbiol 74:7536–45
    [Google Scholar]
  50. Kouwen TR, van der Goot A, Dorenbos R, Winter T, Antelmann H et al. 2007. Thiol-disulphide oxidoreductase modules in the low-GC Gram-positive bacteria. Mol. Microbiol. 64:984–99
    [Google Scholar]
  51. Kouwen TR, van Dijl JM 2009a. Applications of thiol-disulfide oxidoreductases for optimized in vivo production of functionally active proteins in Bacillus. Appl. Microbiol. Biotechnol 85:45–52
    [Google Scholar]
  52. Kouwen TR, van Dijl JM 2009b. Interchangeable modules in bacterial thiol-disulfide exchange pathways. Trends Microbiol 17:6–12
    [Google Scholar]
  53. Krishnappa L, Dreisbach A, Otto A, Goosens VJ, Cranenburgh RM et al. 2013. Extracytoplasmic proteases determining the cleavage and release of secreted proteins, lipoproteins, and membrane proteins in Bacillus subtilis. J. Proteome Res 12:4101–10
    [Google Scholar]
  54. Krishnappa L, Monteferrante CG, Neef J, Dreisbach A, van Dijl JM 2014. Degradation of extracytoplasmic catalysts for protein folding in Bacillus subtilis. Appl. Environ. Microbiol 80:1463–68
    [Google Scholar]
  55. Kruger E, Volker U, Hecker M 1994. Stress induction of clpC in Bacillus subtilis and its involvement in stress tolerance. J. Bacteriol. 176:3360–67
    [Google Scholar]
  56. Lazarevic V, Margot P, Soldo B, Karamata D 1992. Sequencing and analysis of the Bacillus subtilis lytRABC divergon: a regulatory unit encompassing the structural genes of the N-acetylmuramoyl-l-alanine amidase and its modifier. J. Gen. Microbiol. 138:1949–61
    [Google Scholar]
  57. Lee SJ, Kim DM, Bae KH, Byun SM, Chung JH 2000. Enhancement of secretion and extracellular stability of staphylokinase in Bacillus subtilis by wprA gene disruption. Appl. Environ. Microbiol. 66:476–80
    [Google Scholar]
  58. Li W, Zhou X, Lu P 2004. Bottlenecks in the expression and secretion of heterologous proteins in Bacillus subtilis. Res. Microbiol 155:605–10
    [Google Scholar]
  59. Linde D, Volkmer-Engert R, Schreiber S, Muller JP 2003. Interaction of the Bacillus subtilis chaperone CsaA with the secretory protein YvaY. FEMS Microbiol. Lett. 226:93–100
    [Google Scholar]
  60. Lindholm A, Ellmen U, Tolonen-Martikainen M, Palva A 2006. Heterologous protein secretion in Lactococcus lactis is enhanced by the Bacillus subtilis chaperone-like protein PrsA. Appl. Microbiol. Biotechnol. 73:904–14
    [Google Scholar]
  61. Liu JM, Xin XJ, Li CX, Xu JH, Bao J 2012. Cloning of thermostable cellulase genes of Clostridium thermocellum and their secretive expression in Bacillus subtilis. Appl. Biochem. Biotech 166:652–62
    [Google Scholar]
  62. Liu X, Wang H, Wang B, Pan L 2018. Efficient production of extracellular pullulanase in Bacillus subtilis ATCC6051 using the host strain construction and promoter optimization expression system. Microb. Cell Fact. 17:163
    [Google Scholar]
  63. Lu Z, Yang S, Yuan X, Shi Y, Ouyang L et al. 2019. CRISPR-assisted multi-dimensional regulation for fine-tuning gene expression in Bacillus subtilis. . Nucleic Acids Res 47:e40
    [Google Scholar]
  64. Ma RJ, Wang YH, Liu L, Bai LL, Ban R 2018. Production enhancement of the extracellular lipase LipA in Bacillus subtilis: effects of expression system and Sec pathway components. Protein Expr. Purif. 142:81–87
    [Google Scholar]
  65. Malten M, Nahrstedt H, Meinhardt F, Jahn D 2005. Coexpression of the type I signal peptidase gene sipM increases recombinant protein production and export in Bacillus megaterium MS941. Biotechnol. Bioeng. 91:616–21
    [Google Scholar]
  66. Margot P, Pagni M, Karamata D 1999. Bacillus subtilis 168 gene lytF encodes a gamma-d-glutamate-meso-diaminopimelate muropeptidase expressed by the alternative vegetative sigma factor, sigmaD. Microbiology 145:57–65
    [Google Scholar]
  67. Meima R, Eschevins C, Fillinger S, Bolhuis A, Hamoen LW et al. 2002. The bdbDC operon of Bacillus subtilis encodes thiol-disulfide oxidoreductases required for competence development. J. Biol. Chem. 277:6994–7001
    [Google Scholar]
  68. Meng D, Dai M, Xu BL, Zhao ZS, Liang X et al. 2016. Maturation of fibrinolytic bacillopeptidase F involves both hetero- and autocatalytic processes. Appl. Environ. Microbiol. 82:318–27
    [Google Scholar]
  69. Mogk A, Homuth G, Scholz C, Kim L, Schmid FX, Schumann W 1997. The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis. . EMBO J 16:4579–90
    [Google Scholar]
  70. Mulder KC, Bandola J, Schumann W 2013. Construction of an artificial secYEG operon allowing high level secretion of α-amylase. Protein Expr. Purif. 89:92–96
    [Google Scholar]
  71. Muller JP, Bron S, Venema G, van Dijl JM 2000a. Chaperone-like activities of the CsaA protein of Bacillus subtilis. . Microbiology 146:77–88
    [Google Scholar]
  72. Muller JP, Ozegowski J, Vettermann S, Swaving J, Van Wely KH, Driessen AJ 2000b. Interaction of Bacillus subtilis CsaA with SecA and precursor proteins. Biochem. J. 348:367–73
    [Google Scholar]
  73. Murashima K, Chen CL, Kosugi A, Tamaru Y, Doi RH, Wong SL 2002. Heterologous production of Clostridium cellulovorans engB, using protease-deficient Bacillus subtilis, and preparation of active recombinant cellulosomes. J. Bacteriol. 184:76–81
    [Google Scholar]
  74. Peters JM, Colavin A, Shi H, Czarny TL, Larson MH et al. 2016. A comprehensive, CRISPR-based functional analysis of essential genes in bacteria. Cell 165:1493–506
    [Google Scholar]
  75. Petitglatron MF, Grajcar L, Munz A, Chambert R 1993. The contribution of the cell wall to a transmembrane calcium gradient could play a key role in Bacillus subtilis protein secretion. Mol. Microbiol. 9:1097–106
    [Google Scholar]
  76. Pohl S, Bhavsar G, Hulme J, Bloor AE, Misirli G et al. 2013. Proteomic analysis of Bacillus subtilis strains engineered for improved production of heterologous proteins. Proteomics 13:3298–308
    [Google Scholar]
  77. Pohl S, Harwood CR. 2010. Heterologous protein secretion by Bacillus species from the cradle to the grave. Adv. Appl. Microbiol. 73:1–25
    [Google Scholar]
  78. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S et al. 2013. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154:1380–89
    [Google Scholar]
  79. Rashid MH, Kuroda A, Sekiguchi J 1993. Bacillus subtilis mutant deficient in the major autolytic amidase and glucosaminidase is impaired in motility. FEMS Microbiol. Lett. 112:135–40
    [Google Scholar]
  80. Rey MW, Ramaiya P, Nelson BA, Brody-Karpin SD, Zaretsky EJ et al. 2004. Complete genome sequence of the industrial bacterium Bacillus licheniformis and comparisons with closely related Bacillus species. Genome Biol 5:R77
    [Google Scholar]
  81. Ritz D, Beckwith J. 2001. Roles of thiol-redox pathways in bacteria. Annu. Rev. Microbiol. 55:21–48
    [Google Scholar]
  82. Sarvas M, Harwood CR, Bron S, van Dijl JM 2004. Post-translocational folding of secretory proteins in Gram-positive bacteria. Biochim. Biophys. Acta 1694:311–27
    [Google Scholar]
  83. Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P 2008. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol. Rev. 32:234–58
    [Google Scholar]
  84. Schulz A, Schumann W. 1996. hrcA, the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J. Bacteriol. 178:1088–93
    [Google Scholar]
  85. Schulz A, Schwab S, Homuth G, Versteeg S, Schumann W 1997. The htpG gene of Bacillus subtilis belongs to class III heat shock genes and is under negative control. J. Bacteriol. 179:3103–9
    [Google Scholar]
  86. Smith TJ, Blackman SA, Foster SJ 1996. Peptidoglycan hydrolases of Bacillus subtilis 168. Microb. Drug Resist. 2:113–18
    [Google Scholar]
  87. Smith TJ, Blackman SA, Foster SJ 2000. Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 146:249–62
    [Google Scholar]
  88. So Y, Park SY, Park EH, Park SH, Kim EJ et al. 2017. A highly efficient CRISPR-Cas9-mediated large genomic deletion in Bacillus subtilis. Front. Microbiol 8:1167
    [Google Scholar]
  89. Song W, Nie Y, Mu XQ, Xu Y 2016. Enhancement of extracellular expression of Bacillus naganoensis pullulanase from recombinant Bacillus subtilis: effects of promoter and host. Protein Expr. Purif. 124:23–31
    [Google Scholar]
  90. Song Y, Fu G, Dong H, Li J, Du Y, Zhang D 2017. High-efficiency secretion of β-mannanase in Bacillus subtilis through protein synthesis and secretion optimization. J. Agric. Food Chem. 65:2540–48
    [Google Scholar]
  91. Stephenson K, Bron S, Harwood CR 2010. Cellular lysis in Bacillus subtilis; the affect of multiple extracellular protease deficiencies. Lett. Appl. Microbiol. 29:141–45
    [Google Scholar]
  92. Takase K, Mizuno H, Yamane K 1988. NH2-terminal processing of Bacillus subtilis α-amylase. J. Biol. Chem. 263:11548–53
    [Google Scholar]
  93. Tan JT, Bardwell JC. 2004. Key players involved in bacterial disulfide-bond formation. ChemBioChem 5:1479–87
    [Google Scholar]
  94. Terpe K. 2006. Overview of bacterial expression systems for heterologous protein production: from molecular and biochemical fundamentals to commercial systems. Appl. Microbiol. Biotechnol. 72:211–22
    [Google Scholar]
  95. Thwaite JE, Baillie LW, Carter NM, Stephenson K, Rees M et al. 2002. Optimization of the cell wall microenvironment allows increased production of recombinant Bacillus anthracis protective antigen from B. subtilis. Appl. Environ. Microbiol 68:227–34
    [Google Scholar]
  96. Tjalsma H, Antelmann H, Jongbloed JDH, Braun PG, Darmon E et al. 2004. Proteomics of protein secretion by Bacillus subtilis: separating the “secrets” of the secretome. Microbiol. Mol. Biol. Rev. 68:207–33
    [Google Scholar]
  97. Tjalsma H, Bolhuis A, Van Roosmalen ML, Wiegert T, Schumann W et al. 1998. Functional analysis of the secretory precursor processing machinery of Bacillus subtilis: identification of a eubacterial homolog of archaeal and eukaryotic signal peptidases. Genes Dev 12:2318–31
    [Google Scholar]
  98. Tjalsma H, van Dijl JM 2005. Proteomics-based consensus prediction of protein retention in a bacterial membrane. Proteomics 5:4472–82
    [Google Scholar]
  99. Van Wely KH, Swaving J, Klein M, Freudl R, Driessen AJ 2000. The carboxyl terminus of the Bacillus subtilis SecA is dispensable for protein secretion and viability. Microbiology 146:2573–81
    [Google Scholar]
  100. Vitikainen M, Hyyrylainen HL, Kivimaki A, Kontinen VP, Sarvas M 2005. Secretion of heterologous proteins in Bacillus subtilis can be improved by engineering cell components affecting post-translocational protein folding and degradation. J. Appl. Microbiol. 99:363–75
    [Google Scholar]
  101. Vitikainen M, Lappalainen I, Seppala R, Antelmann H, Boer H et al. 2004. Structure-function analysis of PrsA reveals roles for the parvulin-like and flanking N- and C-terminal domains in protein folding and secretion in Bacillus subtilis. J. Biol. Chem 279:19302–14
    [Google Scholar]
  102. Vollmer W, Joris B, Charlier P, Foster S 2010. Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev. 32:259–86
    [Google Scholar]
  103. Wahome PG, Setlow P. 2008. Growth, osmotic downshock resistance and differentiation of Bacillus subtilis strains lacking mechanosensitive channels. Arch. Microbiol. 189:49–58
    [Google Scholar]
  104. Wang L, Ruan B, Ruvinov S, Bryan PN 1998. Engineering the independent folding of the subtilisin BPN′ pro-domain: correlation of pro-domain stability with the rate of subtilisin folding. Biochemistry 37:3165–71
    [Google Scholar]
  105. Wang Y, Chen Z, Zhao R, Jin T, Zhang X, Chen X 2014. Deleting multiple lytic genes enhances biomass yield and production of recombinant proteins by Bacillus subtilis. Microb. . Cell Fact 13:129
    [Google Scholar]
  106. Westbrook AW, Moo-Young M, Chou CP 2016. Development of a CRISPR-Cas9 tool kit for comprehensive engineering of Bacillus subtilis. Appl. Environ. Microbiol 82:4876–95
    [Google Scholar]
  107. Westers H, Westers L, Darmon E, van Dijl JM, Quax WJ, Zanen G 2006a. The CssRS two-component regulatory system controls a general secretion stress response in Bacillus subtilis. . FEBS J 273:3816–27
    [Google Scholar]
  108. Westers L, Dijkstra DS, Westers H, van Dijl JM, Quax WJ 2006b. Secretion of functional human interleukin-3 from Bacillus subtilis. J. Biotechnol 123:211–24
    [Google Scholar]
  109. Westers L, Westers H, Quax WJ 2004. Bacillus subtilis as cell factory for pharmaceutical proteins: a biotechnological approach to optimize the host organism. Biochim. Biophys. Acta 1694:299–310
    [Google Scholar]
  110. Williams RC, Rees ML, Jacobs MF, Pragai Z, Thwaite JE et al. 2003. Production of Bacillus anthracis protective antigen is dependent on the extracellular chaperone, PrsA. J. Biol. Chem. 278:18056–62
    [Google Scholar]
  111. Wu SC, Ye R, Wu XC, Ng SC, Wong SL 1998. Enhanced secretory production of a single-chain antibody fragment from Bacillus subtilis by coproduction of molecular chaperones. J. Bacteriol. 180:2830–35
    [Google Scholar]
  112. Wu SC, Yeung JC, Duan Y, Ye R, Szarka SJ et al. 2002. Functional production and characterization of a fibrin-specific single-chain antibody fragment from Bacillus subtilis: effects of molecular chaperones and a wall-bound protease on antibody fragment production. Appl. Environ. Microbiol. 68:3261–69
    [Google Scholar]
  113. Wu XC, Lee W, Tran L, Wong SL 1991. Engineering a Bacillus subtilis expression-secretion system with a strain deficient in six extracellular proteases. J. Bacteriol. 173:4952–58
    [Google Scholar]
  114. Yabuta Y, Takagi H, Inouye M, Shinde U 2001. Folding pathway mediated by an intramolecular chaperone: propeptide release modulates activation precision of pro-subtilisin. J. Biol. Chem. 276:44427–34
    [Google Scholar]
  115. Yamamoto H, Kurosawa S, Sekiguchi J 2003. Localization of the vegetative cell wall hydrolases LytC, LytE, and LytF on the Bacillus subtilis cell surface and stability of these enzymes to cell wall–bound or extracellular proteases. J. Bacteriol. 185:6666–77
    [Google Scholar]
  116. Yan X, Yu HJ, Hong Q, Li SP 2008. Cre/lox system and PCR-based genome engineering in Bacillus subtilis. Appl. Environ. Microbiol 74:5556–62
    [Google Scholar]
  117. Yao D, Su L, Li N, Wu J 2019. Enhanced extracellular expression of Bacillus stearothermophilus α-amylase in Bacillus subtilis through signal peptide optimization, chaperone overexpression and α-amylase mutant selection. Microb. Cell Fact. 18:69
    [Google Scholar]
  118. Ye R, Kim JH, Kim BG, Szarka S, Sihota E, Wong SL 1999. High-level secretory production of intact, biologically active staphylokinase from Bacillus subtilis. Biotechnol. Bioeng 62:87–96
    [Google Scholar]
  119. Yuan G, Wong SL. 1995. Isolation and characterization of Bacillus subtilis groE regulatory mutants: evidence for orf39 in the dnaK operon as a repressor gene in regulating the expression of both groE and dnaK. J. Bacteriol 177:6462–68
    [Google Scholar]
  120. Zeigler DR, Prágai Z, Rodriguez S, Chevreux B, Muffler A et al. 2008. The origins of 168, W23, and other Bacillus subtilis legacy strains. J. Bacteriol. 190:6983–95
    [Google Scholar]
  121. Zhang K, Duan X, Wu J 2016. Multigene disruption in undomesticated Bacillus subtilis ATCC 6051a using the CRISPR/Cas9 system. Sci. Rep. 6:27943
    [Google Scholar]
  122. Zhang K, Su L, Wu J 2018. Enhanced extracellular pullulanase production in Bacillus subtilis using protease-deficient strains and optimal feeding. Appl. Microbiol. Biotechnol. 102:5089–103
    [Google Scholar]
  123. Zhang W, Yang M, Yang Y, Zhan J, Zhou Y, Zhao X 2016. Optimal secretion of alkali-tolerant xylanase in Bacillus subtilis by signal peptide screening. Appl. Microbiol. Biotechnol. 100:8745–56
    [Google Scholar]
  124. Zhao L, Ye J, Fu J, Chen GQ 2018. Engineering peptidoglycan degradation related genes of Bacillus subtilis for better fermentation processes. Bioresour. Technol. 248:238–47
    [Google Scholar]
  125. Zuber U, Schumann W. 1994. CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J. Bacteriol 176:1359–63
    [Google Scholar]
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