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Applied Microbiology and Biotechnology

, Volume 97, Issue 14, pp 6113–6127 | Cite as

Developing Bacillus spp. as a cell factory for production of microbial enzymes and industrially important biochemicals in the context of systems and synthetic biology

  • Long Liu
  • Yanfeng Liu
  • Hyun-dong Shin
  • Rachel R. Chen
  • Nam Sun Wang
  • Jianghua Li
  • Guocheng DuEmail author
  • Jian ChenEmail author
Mini-Review

Abstract

Increasing concerns over limited petroleum resources and associated environmental problems are motivating the development of efficient cell factories to produce chemicals, fuels, and materials from renewable resources in an environmentally sustainable economical manner. Bacillus spp., the best characterized Gram-positive bacteria, possesses unique advantages as a host for producing microbial enzymes and industrially important biochemicals. With appropriate modifications to heterologous protein expression and metabolic engineering, Bacillus species are favorable industrial candidates for efficiently converting renewable resources to microbial enzymes, fine chemicals, bulk chemicals, and fuels. Here, we summarize the recent advances in developing Bacillus spp. as a cell factory. We review the available genetic tools, engineering strategies, genome sequence, genome-scale structure models, proteome, and secretion pathways, and we list successful examples of enzymes and industrially important biochemicals produced by Bacillus spp. Furthermore, we highlight the limitations and challenges in developing Bacillus spp. as a robust and efficient production host, and we discuss in the context of systems and synthetic biology the emerging opportunities and future research prospects in developing Bacillus spp. as a microbial cell factory.

Keywords

Bacillus species Microbial cell factory Systems metabolic engineering Genome-scale modeling Systems biology Synthetic biology 

Notes

Acknowledgments

This project was financially supported by the Enterprise-university-research prospective program, Jiangsu Province (BY2012054), 111 Project (111-2-06), 863 Program (2012AA022202), and 973 Program (2012CB720806, 2013CB733602).

References

  1. Abdel-Mawgoud AM, Aboulwafa MM, Hassouna NA-H (2008) Optimization of surfactin production by Bacillus subtilis isolate BS5. Appl Biochem Biotechnol 150:305–325Google Scholar
  2. Anderson T, Miller J, Fierobe H, Clubb R (2013) Recombinant Bacillus subtilis that grows on untreated plant biomass. Appl Environ Microbiol 79:867–876Google Scholar
  3. Ajikumar PK, Xiao WH, Tyo KEJ, Wang Y, Simeon F, Leonard E, Mucha O, Phon TH, Pfeifer B, Stephanopoulos G (2010) Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli. Science 330:70–74Google Scholar
  4. Alper H, Stephanopoulos G (2007) Global transcription machinery engineering: a new approach for improving cellular phenotype. Metab Eng 9:258–267Google Scholar
  5. Amani H, Mehrnia MR, Sarrafzadeh MH, Haghighi M, Soudi MR (2010) Scale up and application of biosurfactant from Bacillus subtilis in enhanced oil recovery. Appl Biochem Biotechnol 162:510–523Google Scholar
  6. Bajaj IB, Singhal RS (2009) Sequential optimization approach for enhanced production of poly(gamma-glutamic acid) from newly isolated Bacillus subtilis. Food Technol Biotechnol 47:313–322Google Scholar
  7. Banik RM, Singh P, Pandey SK, Jagannadham MV (2010) Purification and characterization of highly thermostable alkaline phosphatase produced from B. licheniformis MTCC 1483. J Biotechnol 150:S350–S351Google Scholar
  8. Barbe V, Cruveiller S, Kunst F, Lenoble P, Meurice G, Sekowska A, Vallenet D, Wang T, Moszer I, Médigue C (2009) From a consortium sequence to a unified sequence: the Bacillus subtilis 168 reference genome a decade later. Microbiology 155:1758–1775Google Scholar
  9. Biswas R, Yamaoka M, Nakayama H, Kondo T, Yoshida K, Bisaria VS, Kondo A (2012) Enhanced production of 2,3-butanediol by engineered Bacillus subtilis. Appl Microbiol Biotechnol 94:651–658Google Scholar
  10. Brans A, Filée P, Chevigné A, Claessens A, Joris B (2004) New integrative method to generate Bacillus subtilis recombinant strains free of selection markers. Appl Environ Microb 70:7241Google Scholar
  11. Buescher JM, Liebermeister W, Jules M, Uhr M, Muntel J, Botella E, Hessling B, Kleijn RJ, Le Chat L, Lecointe F, Mäder U, Nicolas P, Piersma S, Ruegheimer F, Becher D, Bessieres P, Bidnenko E, Denham EL, Dervyn E, Devine KM, Doherty G, Drulhe S, Felicori L, Fogg MJ, Goelzer A, Hansen A, Harwood CR, Hecker M, Hubner S, Hultschig C, Jarmer H, Klipp E, Leduc A, Lewis P, Molina F, Noirot P, Peres S, Pigeonneau N, Pohl S, Rasmussen S, Rinn B, Schaffer M, Schnidder J, Schwikowski B, van Dijl JM, Veiga P, Walsh S, Wilkinson AJ, Stelling J, Aymerich S, Sauer U (2012) Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism. Science 335:1099–1103Google Scholar
  12. Cavalcante Barros FF, Ponezi AN, Pastore GM (2008) Production of biosurfactant by Bacillus subtilis LB5a on a pilot scale using cassava wastewater as substrate. J Ind Microbiol Biotechnol 35:1071–1078Google Scholar
  13. Chang WT, Chen ML, Wang SL (2010) An antifungal chitinase produced by Bacillus subtilis using chitin waste as a carbon source. World J Microbiol Biotechnol 26:945–950Google Scholar
  14. Chen J, Shi F, Zhang B, Zhu F, Cao W, Xu Z, Xu G, Cen P (2010a) Effects of cultivation conditions on the production of gamma-PGA with Bacillus subtilis ZJU-7. Appl Biochem Biotechnol 160:370–377Google Scholar
  15. Chen N, Xing CG, Xie XX, Xu QY (2009) Optimization of technical conditions of producing ribavirin by Bacillus subtilis. Ann Microbiol 59:525–530Google Scholar
  16. Chen PT, Chiang CJ, Chao YP (2007a) Strategy to approach stable production of recombinant nattokinase in Bacillus subtilis. Biotechnol Progr 23:808–813Google Scholar
  17. Chen PT, Shaw JF, Chao YP, Ho THD, Yu SM (2010b) Construction of chromosomally located T7 expression system for production of heterologous secreted proteins in Bacillus subtilis. J Agr Food Chem 58:5392–5399Google Scholar
  18. Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, Morgenstern B, Voss B, Hess WR, Reva O (2007b) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007–1014Google Scholar
  19. Cho YH, Song JY, Kim KM, Kim MK, Lee IY, Kim SB, Kim HS, Han NS, Lee BH, Kim BS (2010) Production of nattokinase by batch and fed-batch culture of Bacillus subtilis. New Biotechnol 27:341–346Google Scholar
  20. Chtioui O, Dimitrov K, Gancel F, Nikov I (2010) Biosurfactants production by immobilized cells of Bacillus subtilis ATCC 21332 and their recovery by pertraction. Process Biochem 45:1795–1799Google Scholar
  21. Coutte F, Leclere V, Bechet M, Guez JS, Lecouturier D, Chollet-Imbert M, Dhulster P, Jacques P (2010) Effect of pps disruption and constitutive expression of srfA on surfactin productivity, spreading and antagonistic properties of Bacillus subtilis 168 derivatives. J Appl Microbiol 109:480–491Google Scholar
  22. Das K, Mukherjee AK (2007) Comparison of lipopeptide biosurfactants production by Bacillus subtilis strains in submerged and solid state fermentation systems using a cheap carbon source: some industrial applications of biosurfactants. Process Biochem 42:1191–1199Google Scholar
  23. de Faria AF, Teodoro-Martinez DS, de Oliveira BGN, Vaz BG, Silva IS, Garcia JS, Totola MR, Eberlin MN, Grossman M, Alves OL, Durrant LR (2011) Production and structural characterization of surfactin (C-14/Leu(7)) produced by Bacillus subtilis isolate LSFM-05 grown on raw glycerol from the biodiesel industry. Process Biochem 46:1951–1957Google Scholar
  24. de Jong B, Siewers V, Nielsen J (2011) Systems biology of yeast: enabling technology for development of cell factories for production of advanced biofuels. Curr Opion Biotechnol 23:1–7Google Scholar
  25. Deepak V, Kalishwaralal K, Ramkumarpandian S, Babu SV, Senthilkumar SR, Sangiliyandi G (2008) Optimization of media composition for nattokinase production by Bacillus subtilis using response surface methodology. Bioresource Technol 99:8170–8174Google Scholar
  26. 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 Microb 78:651–659Google Scholar
  27. Duan YX, Chen T, Chen X, Zhao XM (2010) Overexpression of glucose-6-phosphate dehydrogenase enhances riboflavin production in Bacillus subtilis. Appl Microbiol Biotechnol 85:1907–1914Google Scholar
  28. Dueber JE, Wu GC, Malmirchegini GR, Moon TS, Petzold CJ, Ullal AV, Prather KL, Keasling JD (2009) Synthetic protein scaffolds provide modular control over metabolic flux. Nat Biotechnol 27:753–759Google Scholar
  29. Dunlop MJ, Dossani ZY, Szmidt HL, Chu HC, Lee TS, Keasling JD, Hadi MZ, Mukhopadhyay A (2011) Engineering microbial biofuel tolerance and export using efflux pumps. Mol Syst Biol 7:487Google Scholar
  30. Fabret C, Dusko Ehrlich S, Noirot P (2002) A new mutation delivery system for genome-scale approaches in Bacillus subtilis. Mol Microbiol 46:25–36Google Scholar
  31. Fang T, Chen X, Li N, Song H, Bai J, Xiong J, Ying H (2010) Optimization of medium components for d-ribose production by transketolase-deficient Bacillus subtilis NJT-1507. Korean J Chem Eng 27:1725–1729Google Scholar
  32. Fu LL, Xu ZR, Shuai JB, Hu CX, Dai W, Li WF (2008) High-level secretion of a chimeric thermostable lichenase from Bacillus subtilis by screening of site-mutated signal peptides with structural alterations. Curr Microbiol 56:287–292Google Scholar
  33. Fu LL, Xu ZR, Li WF, Shuai JB, Lu P, Hu CX (2007) Protein secretion pathways in Bacillus subtilis: implication for optimization of heterologous protein secretion. Biotechnol Adv 25:1–12Google Scholar
  34. Gerosa L, Sauer U (2011) Regulation and control of metabolic fluxes in microbes. Curr Opin Biotechnol 22:566–575Google Scholar
  35. Goosens VJ, Otto A, Glasner C, Monteferrante CC, van der Ploeg R, Hecker M, Becher D, van Dijl JM (2013) Novel twin-arginine translocation pathway-dependent phenotypes of Bacillus subtilis unveiled by quantitative proteomics. J Proteome Res 12:796–807Google Scholar
  36. Gong G, Zheng Z, Chen H, Yuan C, Wang P, Yao L, Yu Z (2009) Enhanced production of surfactin by Bacillus subtilis E8 mutant obtained by ion beam implantation. Food Technol Biotechnol 47:27–31Google Scholar
  37. Hahne H, Mäder U, Otto A, Bonn F, Steil L, Bremer E, Hecker M, Becher D (2010) A comprehensive proteomics and transcriptomics analysis of Bacillus subtilis salt stress adaptation. J Bacteriol 192:870–882Google Scholar
  38. Henry CS, Zinner JF, Cohoon MP, Stevens RL (2009) iBsu1103: a new genome-scale metabolic model of Bacillus subtilis based on SEED annotations. Genome Biol 10:R69Google Scholar
  39. Heravi KM, Wenzel M, Altenbuchner J (2011) Regulation of mtl operon promoter of Bacillus subtilis: requirements of its use in expression vectors. Microb Cell Fact 10:83Google Scholar
  40. Hmidet N, Ali NEH, Zouari-Fakhfakh N, Haddar A, Nasri M, Sellemi-Kamoun A (2010) Chicken feathers: a complex substrate for the co-production of alpha-amylase and proteases by B. licheniformis NH1. J Ind Microbiol Biotechnol 37:983–990Google Scholar
  41. Hong SW, Chu IH, Chung KS (2011) Purification and biochemical characterization of thermostable phytase from newly isolated Bacillus subtilis CF92. J Korean Soc Appl Bi 54:89–94Google Scholar
  42. Huang J, Du Y, Xu G, Zhang H, Zhu F, Huang L, Xu Z (2011) High yield and cost-effective production of poly(gamma-glutamic acid) with Bacillus subtilis. Eng Life Sci 11:291–297Google Scholar
  43. İleri N, Çalik P (2006) Effects of pH strategy on endo– and exo–metabolome profiles and sodium potassium hydrogen ports of β–lactamase–producing Bacillus licheniformis. Biotechnol Progr 22:411–419Google Scholar
  44. Jeong JH, Kim JN, Wee YJ, Ryu HW (2010) The statistically optimized production of poly(gamma-glutamic acid) by batch fermentation of a newly isolated Bacillus subtilis RKY3. Bioresour Technol 101:4533–4539Google Scholar
  45. Jung J, Yu KO, Ramzi AB, Choe SH, Kim SW, Han SO (2012) Improvement of surfactin production in Bacillus subtilis using synthetic wastewater by overexpression of specific extracellular signaling peptides, comX and phrC. Biotechnol Bioeng 109:2349–2356Google Scholar
  46. Kakeshtia 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 46:250–257Google Scholar
  47. Keasling JD (2010) Manufacturing molecules through metabolic engineering. Science 330:1355–1358Google Scholar
  48. Kim IK, Roldão A, Siewers V, Nielsen J (2012) A systems-level approach for metabolic engineering of yeast cell factories. FEMS Yeast Res 12:228–248Google Scholar
  49. Kimura K, Tran LSP, Do TH, Itoh Y (2009) Expression of the pgsB encoding the poly-gamma-dl-glutamate synthetase of Bacillus subtilis (natto). Biosci Biotechnol Biochem 73:1149–1155Google Scholar
  50. Konsoula Z, Liakopoulou-Kyriakides M (2006) Thermostable alpha-amylase production by Bacillus subtilis entrapped in calcium alginate gel capsules. Enzyme Microb Technol 39:690–696Google Scholar
  51. Kunst F, Ogasawara N, Moszer I, Albertini A, Alloni G, Azevedo V, Bertero M, Bessieres P, Bolotin A, Borchert S, Borriss R, Boursier L, Brans A, Braun M, Brignell SC, Bron S, Brouillet S, Bruschi CV, Caldwell B, Capuano V, Carter NM, Choi SK, Codani JJ, Connerton IF, Cummings NJ, Daniel RA, Denizot F, Devine KM, Dusterhoft A, Ehrlich SD, Emmerson PT, Entian KD, Errington J, Fabret C, Ferrari E, Foulger D, Fritz C, Fujita M, Fujita Y, Fuma S, Galizzi A, Galleron N, Ghim SY, Glaser P, Goffeau A, Golightly EJ, Grandi G, Guiseppi G, Guy BJ, Haga K, Haiech J, Harwood CR, Henaut A, Hilbert H, Holsappel S, Hosono S, Hullo MF, Itaya M, Jones L, Joris B, Karamata D, Kasahara Y, Klaerr-Blanchard M, Klein C, Kobayashi Y, Koetter P, Koningstein G, Krogh S, Kumano M, KuritaK LA, Lardinois S, Lauber J, Lazarevic V, Lee M, Levine A, Liu H, Masuda S, Mauel C, Medigue C, Medina N, Mellado RP, Mizuno M, Moestl D, Nakai S, Noback M, Noone D, O’Reilly M, Ogawa K, Ogiwara A, Oudega B, Park SH, ParroV PTM, Portetelle D, Porwollik S, Prescott AM, Presecan E, Pujic P, Purnelle B, Rapoport G, Rey M, Reynolds S, Rieger M, Rivolta C, Rocha E, Roche B, Rose M, Sadaie Y, Sato T, Scanlan E, Schleich S, Schroeter R, Scoffone F, Sekiguchi J, Sekowska A, Seror SJ, Serror P, Shin BS, Soldo B, Sorokin A, Tacconi E, Takagi T, Takahashi H, Takemaru K, Takeuchi M, Tamakoshi A, Tanaka T, Terpstra P, Tognoni A, Tosato V, Uchiyama S, Vandenbol M, Vannier F, Vassarotti A, Viari A, Wambutt R, Wedler E, Wedler H, Weitzenegger T, Winters P, Wipat A, Yamamoto H, Yamane K, Yasumoto K, Yata K, Yoshida K, Yoshikawa HF, Zumstein E, Yoshikawa H, Danchin A (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249–256Google Scholar
  52. Kurosawa K, Hosaka T, Tamehiro N, Inaoka T, Ochi K (2006) Improvement of alpha-amylase production by modulation of ribosomal component protein S12 in Bacillus subtilis 168. Appl Environ Microb 72:71–77Google Scholar
  53. Kwon EY, Kim KM, Kim MK, Lee IY, Kim BS (2011) Production of nattokinase by high cell density fed-batch culture of Bacillus subtilis. Bioproc Biosyst Eng 34:789–793Google Scholar
  54. Lammers CR, Flórez LA, Schmeisky AG, Roppel SF, Mäder U, Hamoen L, Stülke J (2010) Connecting parts with processes: SubtiWiki and SubtiPathways integrate gene and pathway annotation for Bacillus subtilis. Microbiology 156:849–859Google Scholar
  55. Lee BH, Kim BK, Lee YJ, Chung CH, Lee JW (2010a) Industrial scale of optimization for the production of carboxymethylcellulase from rice bran by a marine bacterium, Bacillus subtilis subsp subtilis A-53. Enzyme Microb Technol 46:38–42Google Scholar
  56. Lee DG, Jang MK, Lee OH, Kim NY, Ju SA, Lee SH (2008) Over-production of a glycoside hydrolase family 50 beta-agarase from Agarivorans sp JA-1 in Bacillus subtilis and the whitening effect of its product. Biotechnol Lett 30:911–918Google Scholar
  57. Lee SJ, Pan JG, Park SH, Choi SK (2010b) Development of a stationary phase-specific autoinducible expression system in Bacillus subtilis. J Biotechnol 149:16–20Google Scholar
  58. Li H, Zhang G, Deng A, Chen N, Wen T (2011a) De novo engineering and metabolic flux analysis of inosine biosynthesis in Bacillus subtilis. Biotechnol Lett 33:1575–1580Google Scholar
  59. Li S, Wen J, Jia X (2011b) Engineering Bacillus subtilis for isobutanol production by heterologous Ehrlich pathway construction and the biosynthetic 2-ketoisovalerate precursor pathway overexpression. Appl Microbiol Biotechnol 91:577–589Google Scholar
  60. Liu JF, Yang J, Yang SZ, Ye RQ, Mu BZ (2012) Effects of different amino acids in culture media on surfactin variants produced by Bacillus subtilis TD7. Appl Biochem Biotechnol 166:2091–2100Google Scholar
  61. Liu S, Endo K, Ara K, Ozaki K, Ogasawara N (2008a) Introduction of marker-free deletions in Bacillus subtilis using the AraR repressor and the ara promoter. Microbiology 154:2562–2570Google Scholar
  62. Liu YH, Lu FP, Li Y, Yin XB, Wang Y, Gao C (2008b) Characterisation of mutagenised acid-resistant alpha-amylase expressed in Bacillus subtilis WB600. Appl Microbiol Biotechnol 78:85–94Google Scholar
  63. Lu Y, Lin Q, Wang J, Wu Y, Bao W, Lv F, Lu Z (2010) Overexpression and characterization in Bacillus subtilis of a positionally nonspecific lipase from Proteus vulgaris. J Ind Microbiol Biotechnol 37:919–925Google Scholar
  64. Mäder U, Schmeisky AG, Florez LA, Stülke J (2012) SubtiWiki—a comprehensive community resource for the model organism Bacillus subtilis. Nucleic Acids Res 40:D1278–D1287Google Scholar
  65. Manabe K, Kageyama Y, Morimoto T, Ozawa T, Sawada K, Endo K, Tohata M, Ara K, Ozaki K, Ogasawara N (2011) Combined effect of improved cell yield and increased specific productivity enhances recombinant enzyme production in genome-reduced Bacillus subtilis strain MGB874. Appl Environ Microbiol 77:8370–8381Google Scholar
  66. Manabe K, Kageyama Y, Tohata M, Ara K, Ozaki K, Ogasawara N (2012) High external pH enables more efficient secretion of alkaline alpha-amylase AmyK38 by Bacillus subtilis. Microb Cell Fact 11:74Google Scholar
  67. Ming YM, Wei ZW, Lin CY, Sheng GY (2010) Development of a Bacillus subtilis expression system using the improved Pglv promoter. Microb Cell Fact 9:55Google Scholar
  68. Morimoto T, Kadoya R, Endo K, Tohata M, Sawada K, Liu S, Ozawa T, Kodama T, Kakeshita H, Kageyama Y, Manabe K, Kanaya S, Ara K, Ozaki K, Ogasawara N (2008) Enhanced recombinant protein productivity by genome reduction in Bacillus subtilis. DNA Res 15:73–81Google Scholar
  69. Moszer I, Glaser P, Danchin A (1995) SubtiList: a relational database for the Bacillus subtilis genome. Microbiology 141:261–268Google Scholar
  70. Mulder KCL, Bandola J, Schumann W (2013) Construction of an artificial secYEG operon allowing high level secretion of alpha-amylase, Protein Expr Purif  http://dx.doi.org/10.1016/j.pep.2013.02.008
  71. Na D, Yoo SM, ChungH PH, Park JH, Lee SY (2013) Metabolic engineering of Escherichia coli using synthetic small regulatory RNAs. Nat Biotechnol 30:170–174Google Scholar
  72. Nicolas P, Mäder U, Dervyn E, Rochat T, Leduc A, Pigeonneau N, Bidnenko E, Marchadier E, Hoebeke M, Aymerich S, Becher D, Bisicchia P, Botella E, Delumeau O, Doherty G, Denham EL, Fogg MJ, Fromion V, Goelzer A, Hansen A, Härtig E, Harwood CR, Homuth G, Jarmer H, Jules M, Klipp E, Le Chat L, Lecointe F, Lewis P, Liebermeister W, March A, Mars RAT, Priyanka N, Noone D, Pohl S, Rinn B, Rügheimer F, Sappa PK, Samson F, Schaffer M, Schwikowski B, Steil L, Stülke J, Wiegert T, Devine KM, Wilkinson AJ, van Dijl JM, Hecker M, Völker U, Bessières P, Noirot P (2012) Condition dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335:1103–1106Google Scholar
  73. Ochi K (2007) From microbial differentiation to ribosome engineering. Biosci Biotechnol Biochem 71:1373–1386Google Scholar
  74. Oh C, De Zoysa M, Kang DH, Lee Y, Whang I, Nikapitiya C, Heo SJ, Yoon KT, Affan A, Lee J (2011) Isolation, purification, and enzymatic characterization of extracellular chitosanase from marine bacterium Bacillus subtilis CH2. J Microbiol Biotechnol 21:1021–1025Google Scholar
  75. Oh YK, Palsson BO, Park SM, Schilling CH, Mahadevan R (2007) Genome-scale reconstruction of metabolic network in Bacillus subtilis based on high-throughput phenotyping and gene essentiality data. J Biol Chem 282:28791–28799Google Scholar
  76. Ozcan BD, Ozcan N (2008) Expression of thermostable alpha-amylase gene from Bacillus stearothermophilus in various Bacillus subtilis strains. Ann Microbiol 58:265–268Google Scholar
  77. Perkins J, Wyss M, Sauer U, Hohmann HP (2009) Metabolic engineering of B. subtilis. In: CD Smolke, J Nielsen (eds) Metabolic pathway engineering handbook. CRC, Boca Raton.Google Scholar
  78. Phan TTP, Nguyen HD, Schumann W (2012) Development of a strong intracellular expression system for Bacillus subtilis by optimizing promoter elements. J Biotechnol 157:167–172Google Scholar
  79. Ponte Rocha MV, Gomes Barreto RV, Melo VMM, Barros Goncalves LR (2009) Evaluation of cashew apple juice for surfactin production by Bacillus subtilis LAMI008. Appl Biochem Biotechnol 155:366–378Google Scholar
  80. Rajagopalan G, Krishnan C (2008a) Alpha-amylase production from catabolite derepressed Bacillus subtilis KCC103 utilizing sugarcane bagasse hydrolysate. Bioresource Technol 99:3044–3050Google Scholar
  81. Rajagopalan G, Krishnan C (2008b) Optimization of agro-residual medium for alpha-amylase production from a hyper-producing Bacillus subtilis KCC103 in submerged fermentation. J Chem Technol Biotechnol 84:618–625Google Scholar
  82. Romero-Garcia S, Hernández-Bustos C, Merino E, Gosset G, Martinez A (2009) Homolactic fermentation from glucose and cellobiose using Bacillus subtilis. Microb Cell Fact 8:23Google Scholar
  83. Romero S, Merino E, Bolívar F, Gosset G, Martinez A (2007) Metabolic engineering of Bacillus subtilis for ethanol production: lactate dehydrogenase plays a key role in fermentative metabolism. Appl Environ Microb 73:5190–5198Google Scholar
  84. Rückert C, Blom J, Chen X, Reva O, Borriss R (2011) Genome sequence of B. amyloliquefaciens type strain DSM7(T) reveals differences to plant-associated B. amyloliquefaciens FZB42. J Biotechnol 155:78–85Google Scholar
  85. Saimmai A, Rukadee O, Sobhon V, Maneerat S (2012) Biosurfactant production by Bacillus subtilis TD4 and Pseudomonas aeruginosa SU7 grown on crude glycerol obtained from biodiesel production plant as sole carbon source. J Sci Ind Res 71:396–406Google Scholar
  86. Sanghi A, Garg N, Sharma J, Kuhar K, Kuhad RC, Gupta VK (2008) Optimization of xylanase production using inexpensive agro-residues by alkalophilic Bacillus subtilis ASH in solid-state fermentation. World J Microbi Biotechnol 24:633–640Google Scholar
  87. Sathish T, Prakasham RS (2010) Enrichment of glutaminase production by Bacillus subtilis RSP-GLU in submerged cultivation based on neural network-genetic algorithm approach. J Chem Technol Biotechnol 85:50–58Google Scholar
  88. Schallmey M, Singh A, Ward OP (2004) Developments in the use of Bacillus species for industrial production. Can J Microbiol 50:1–17Google Scholar
  89. Schumann W (2007) Production of recombinant proteins in Bacillus subtilis. Adv Appl Microbiol 62:137–189Google Scholar
  90. Shi F, Xu ZN, Cen PL (2006) Efficient production of poly-gamma-glutamic acid by Bacillus subtilis ZJU-7. Appl Biochem Biotechnol 133:271–281Google Scholar
  91. Shi S, Chen T, Zhang Z, Chen X, Zhao X (2009a) Transcriptome analysis guided metabolic engineering of Bacillus subtilis for riboflavin production. Metab Eng 11:243–252Google Scholar
  92. Shi S, Shen Z, Chen X, Chen T, Zhao X (2009b) Increased production of riboflavin by metabolic engineering of the purine pathway in Bacillus subtilis. Biochem Eng J 46:28–33Google Scholar
  93. Shi X, Feng M, Zhao Y, Guo X, Zhou P (2008) Overexpression, purification and characterization of a recombinant secretary catalase from Bacillus subtilis. Biotechnol Lett 30:181–186Google Scholar
  94. Sierro N, Makita Y, de Hoon M, Nakai K (2008) DBTBS: a database of transcriptional regulation in Bacillus subtilis containing upstream intergenic conservation information. Nucleic Acids Res 36:D93–D96Google Scholar
  95. Soni SK, Goyal N, Gupta JK, Soni R (2012) Enhanced production of alpha-amylase from Bacillus subtilis subsp. spizizenii in solid state fermentation by response surface methodology and its evaluation in the hydrolysis of raw potato starch. Starch-Starke 64:64–77Google Scholar
  96. Su Y, Li X, Liu Q, Hou Z, Zhu X, Guo X, Ling P (2010) Improved poly-gamma-glutamic acid production by chromosomal integration of the Vitreoscilla hemoglobin gene (vgb) in Bacillus subtilis. Bioresource Technol 101:4733–4736Google Scholar
  97. Tanaka K, Henry CS, Zinner JF, Jolivet E, Cohoon MP, Xia F, Bidnenko V, Ehrlich SD, Stevens RL, Noirot P (2013) Building the repertoire of dispensable chromosome regions in Bacillus subtilis entails major refinement of cognate large-scale metabolic model. Nucleic Acids Res 41:687–699Google Scholar
  98. Tanyildizi MS, Oezer D, Elibol M (2007) Production of bacterial alpha-amylase by B. amyloliquefaciens under solid substrate fermentation. Biochem Eng J 37:294–297Google Scholar
  99. Tjalsma H, Antelmann H, Jongbloed JDH, Braun PG, Darmon E, Dorenbos R, Dubois JYF, Westers H, Zanen G, Quax WJ, Kuipers OP, Bron S, Hecker M, van Dijl JM (2004) Proteomics of protein secretion by Bacillus subtilis: separating the “secrets” of the secretome. Microbiol Mol Biol R 68:207–233Google Scholar
  100. Tyo KEJ, Ajikumar PK, Stephanopoulos G (2009) Stabilized gene duplication enables long-term selection-free heterologous pathway expression. Nat Biotechnol 27:760–765Google Scholar
  101. van Dijl JM, Hecker M (2013) Bacillus subtilis: from soil bacterium to super-secreting cell factory. Microb Cell Fact 12:3Google Scholar
  102. Veith B, Herzberg C, Steckel S, Feesche J, Maurer KH, Ehrenreich P, Bäumer S, Henne A, Liesegang H, Merkl R (2004) The complete genome sequence of Bacillus licheniformis DSM13, an organism with great industrial potential. J Mol Microb Biotechnol 7:204–211Google Scholar
  103. Voigt B, Schweder T, Sibbald M, Albrecht D, Ehrenreich A, Bernhardt J, Feesche J, Maurer KH, Gottschalk G, van Dijl JM, Hecker M (2006) The extracellular proteome of Bacillus licheniformis grown in different media and under different nutrient starvation conditions. Proteomics 6:268–281Google Scholar
  104. Wang Y, Weng J, Waseem R, Yin X, Zhang R, Shen Q (2012) Bacillus subtilis genome editing using ssDNA with short homology regions. Nucleic Acids Res 40:e91Google Scholar
  105. Wang Z, Chen T, Ma X, Shen Z, Zhao X (2011) Enhancement of riboflavin production with Bacillus subtilis by expression and site-directed mutagenesis of zwf and gnd gene from Corynebacterium glutamicum. Bioresource Technol 102:3934–3940Google Scholar
  106. Wenzel M, Mueller A, Siemann-Herzberg M, Altenbuchner J (2011) Self-inducible Bacillus subtilis expression system for reliable and inexpensive protein production by high-cell-density fermentation. Appl Environ Microb 77:6419–6425Google Scholar
  107. Westers H, Dorenbos R, van Dijl JM, Kabel J, Flanagan T, Devine KM, Jude F, Séror SJ, Beekman AC, Darmon E, Eschevins C, de Jong A, Bron S, Kuipers OP, Albertini AM, Antelmann H, Hecker M, Zamboni N, Sauer U, Bruand C, Ehrlich DS, Alonso JC, Salas M, Quax WJ (2003) Genome engineering reveals large dispensable regions in Bacillus subtilis. Mol Biol Evol 20:2076–2090Google Scholar
  108. Widner B, Thomas M, Sternberg D, Lammon D, Behr R, Sloma A (2000) Development of marker-free strains of Bacillus subtilis capable of secreting high levels of industrial enzymes. J Ind Microbiol Biotechnol 25:204–212Google Scholar
  109. Wolff S, Antelmann H, Albrecht D, Becher D, Bernhardt J, Bron S, Buettner K, van Dijl JM, Eymann C, Otto A, Tam LT, Hecker M (2007) Towards the entire proteome of the model bacterium Bacillus subtilis by gel-based and gel-free approaches. J Chromatogr B 849:129–140Google Scholar
  110. Wu QL, Chen T, Gan Y, Chen X, Zhao XM (2007) Optimization of riboflavin production by recombinant Bacillus subtilis RH44 using statistical designs. Appl Microbiol Biotechnol 76:783–794Google Scholar
  111. Wu Q, Xu H, Shi N, Yao J, Li S, Ouyang P (2008) Improvement of poly(gamma-glutamic acid) biosynthesis and redistribution of metabolic flux with the presence of different additives in Bacillus subtilis CGMCC 0833. Appl Microbiol Biotechnol 79:527–535Google Scholar
  112. Xu C, Liu L, Zhang Z, Jin D, Qiu J, Chen M (2013) Genome-scale metabolic model in guiding metabolic engineering of microbial improvement. Appl Microbiol Biotechnol 97:519–539Google Scholar
  113. Xue J, Ahring BK (2011) Enhancing isoprene production by genetic modification of the 1-deoxy-d-xylulose-5-phosphate pathway in Bacillus subtilis. Appl Environ Microb 77:2399–2405Google Scholar
  114. Yan X, Yu HJ, Hong Q, Li SP (2008) Cre/lox system and PCR-based genome engineering in Bacillus subtilis. Appl Environ Microb 74:5556–5562Google Scholar
  115. Yang M, Zhang W, Ji S, Cao P, Chen Y, Zhao X (2013) Generation of an artificial double promoter for protein expression in Bacillus subtilis through a promoter trap system. PloS One 8:e56321Google Scholar
  116. You C, Zhang XZ, Zhang YHP (2012) Simple cloning via direct transformation of PCR Product (DNA multimer) to Escherichia coli and Bacillus subtilis. Appl Environ Microb 78:1593–1595Google Scholar
  117. Yue Y, Lian J, Tian P, Tan T (2009) Cloning of amidase gene from Rhodococcus erythropolis and expression by distinct promoters in Bacillus subtilis. J Mol Catal B-Enzym 56:89–95Google Scholar
  118. Zakataeva NP, Nikitina OV, Gronskiy SV, Romanenkov DV, Livshits VA (2010) A simple method to introduce marker-free genetic modifications into the chromosome of naturally nontransformable Bacillus amyloliquefaciens strains. Appl Microbiol Biotechnol 85:1201–1209Google Scholar
  119. Zamboni N, Fendt SM, Rühl M, Sauer U (2009) 13C-based metabolic flux analysis. Nat Protoc 4:878–892Google Scholar
  120. Zhang C, Zhang X, Yao Z, Lu Y, Lu F, Lu Z (2011a) A new method for multiple gene inactivations in Bacillus subtilis 168, producing a strain free of selectable markers. Can J Microbiol 57:427–436Google Scholar
  121. Zhang D, Feng X, Zhou Z, Zhang Y, Xu H (2012a) Economical production of poly(gamma-glutamic acid) using untreated cane molasses and monosodium glutamate waste liquor by Bacillus subtilis NX-2. Bioresource Technol 114:583–588Google Scholar
  122. Zhang H, Zhu J, Zhu X, Cai J, Zhang A, Hong Y, Huang J, Huang L, Xu Z (2012b) High-level exogenous glutamic acid-independent production of poly-(gamma-glutamic acid) with organic acid addition in a new isolated Bacillus subtilis C10. Bioresource Technol 116:241–246Google Scholar
  123. Zhang XZ, Sathitsuksanoh N, Zhu Z, Zhang YHP (2011b) One-step production of lactate from cellulose as the sole carbon source without any other organic nutrient by recombinant cellulolytic Bacillus subtilis. Metab Eng 13:364–372Google Scholar
  124. Zhang XZ, Yan X, Cui ZL, Hong Q, Li SP (2006) mazF, a novel counter-selectable marker for unmarked chromosomal manipulation in Bacillus subtilis. Nucleic Acids Res 34:e71–e71Google Scholar
  125. Zhang XZ, Zhang YHP (2010) One-step production of biocommodities from lignocellulosic biomass by recombinant cellulolytic Bacillus subtilis: opportunities and challenges. Eng Life Sci 10:398–406Google Scholar
  126. Zhang XZ, Zhang YHP (2011) Simple, fast and high-efficiency transformation system for directed evolution of cellulase in Bacillus subtilis. Microb Biotechnol 4:98–105Google Scholar
  127. Zhao Q, Ding R, Kang Y, Chen J (2008) Expression of pectate lyase A from Aspergillus nidulans in Bacillus subtilis. World J Microb Biotechol 24:2607–2612Google Scholar
  128. Zhou K, Zou R, Zhang C, Stephanopoulos G, Too HP (2013) Optimization of amorphadiene synthesis in Bacillus subtilis via transcriptional, translational and media modulation. Biotechnol Bioeng. doi: 10.1002/bit.24900 Google Scholar
  129. Zhu FM, Ji SY, Zhang WW, Li W, Cao BY, Yang MM (2008) Development and application of a novel signal peptide probe vector with PGA as reporter in Bacillus subtilis WB700: twenty-four tat pathway signal peptides from Bacillus subtilis were monitored. Mol Biotechnol 39:225–230Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Long Liu
    • 1
    • 2
  • Yanfeng Liu
    • 1
    • 2
  • Hyun-dong Shin
    • 3
  • Rachel R. Chen
    • 3
  • Nam Sun Wang
    • 4
  • Jianghua Li
    • 1
    • 2
  • Guocheng Du
    • 1
    • 2
    Email author
  • Jian Chen
    • 5
    Email author
  1. 1.Key Laboratory of Carbohydrate Chemistry and Biotechnology, Ministry of EducationJiangnan UniversityWuxiChina
  2. 2.Key Laboratory of Industrial Biotechnology, Ministry of EducationJiangnan UniversityWuxiChina
  3. 3.School of Chemical and Biomolecular EngineeringGeorgia Institute of TechnologyAtlantaUSA
  4. 4.Department of Chemical and Biomolecular EngineeringUniversity of MarylandCollege ParkUSA
  5. 5.National Engineering of Laboratory for Cereal Fermentation TechnologyJiangnan UniversityWuxiChina

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