Bacillus subtilis: From soil bacterium to super-secreting cell factory

Microbial Cell Factories

Volumn 12, Issue 1, 2013, Pages

  van Dijl, Jan Maarten ^a   Hecker, Michael ^b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Bacillus subtilis; Cell factory; Protein secretion; Proteomics; Synthetic biology; Systems biology

Indexed keywords

BACTERIAL PROTEIN;

BACILLUS SUBTILIS; BACTERIAL CELL WALL; EDITORIAL; ESCHERICHIA COLI; FUNCTIONAL GENOMICS; NONHUMAN; PROTEIN SECRETION; PROTEOMICS; SOIL MICROFLORA; SYNTHETIC BIOLOGY;

BACILLUS SUBTILIS; BIOTECHNOLOGY; PROTEOME; RECOMBINANT PROTEINS; SOIL MICROBIOLOGY;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); POSIBACTERIA;

EID: 84872143710     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-12-3     Document Type: Editorial

References (67)

1. Earl AM, Losick R, Kolter R. Ecology and genomics of Bacillus subtilis. Trends Microbiol 2008, 16:269-275. 10.1016/j.tim.2008.03.004, 2819312, 18467096.
2. Harwood CR. Bacillus subtilis and its relatives: molecular biological and industrial workhorses. Trends Biotechnol 1992, 10:247-256.
3. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, et al. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 1997, 390:249-256. 10.1038/36786, 9384377.
4. Barbe V, Cruveiller S, Kunst F, Lenoble P, Meurice G, Sekowska A, et al. From a consortium sequence to a unified sequence: the Bacillus subtilis 168 reference genome a decade later. Microbiology 2009, 155:1758-1775. 10.1099/mic.0.027839-0, 2885750, 19383706.
5. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, Arnaud M, et al. Essential Bacillus subtilis genes. Proc Natl Acad Sci USA 2003, 100:4678-4683. 10.1073/pnas.0730515100, 153615, 12682299.
6. Nicolas P, Mäder U, Dervyn E, Rochat T, Leduc A, Pigeonneau N, et al. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 2012, 335:1103-1106. 10.1126/science.1206848, 22383849.
7. Büscher JM, Liebermeister W, Jules M, Uhr M, Muntel J, Botella E, et al. Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism. Science 2012, 335:1099-1103. 10.1126/science.1206871, 22383848.
8. Otto A, Bernhardt J, Meyer H, Schaffer M, Herbst FA, Siebourg J, et al. Systems-wide temporal proteomic profiling in glucose-starved Bacillus subtilis. Nat Commun 2010, 1:137. 10.1038/ncomms1137, 3105300, 21266987.
9. Becher D, Büttner K, Moche M, Hessling B, Hecker M. From the genome sequence to the protein inventory of Bacillus subtilis. Proteomics 2011, 11:2971-2980. 10.1002/pmic.201100090, 21710564.
10. Maass S, Sievers S, Zühlke D, Kuzinski J, Sappa PK, Muntel J, et al. Efficient, global-scale quantification of absolute protein amounts by integration of targeted mass spectrometry and two-dimensional gel-based proteomics. Anal Chem 2011, 83:2677-2684. 10.1021/ac1031836, 21395229.
11. Tjalsma H, Bolhuis A, Jongbloed JD, Bron S, van Dijl JM. Signal peptide-dependent protein transport in Bacillus subtilis: a genome-based survey of the secretome. Microbiol Mol Biol Rev 2000, 64:515-547. 10.1128/MMBR.64.3.515-547.2000, 99003, 10974125.
12. Antelmann H, Tjalsma H, Voigt B, Ohlmeier S, Bron S, van Dijl JM, et al. A proteomic view on genome-based signal peptide predictions. Genome Res 2001, 11:1484-1502. 10.1101/gr.182801, 11544192.
13. Tjalsma H, Antelmann H, Jongbloed JD, Braun PG, Darmon E, Dorenbos R, et al. Proteomics of protein secretion by Bacillus subtilis: separating the 'secrets' of the secretome. Microbiol Mol Biol Rev 2004, 68:207-233. 10.1128/MMBR.68.2.207-233.2004, 419921, 15187182.
14. Jongbloed JDH, Martin U, Antelmann H, Hecker M, Tjalsma H, Venema G, et al. TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway. J Biol Chem 2000, 275:41350-41357. 10.1074/jbc.M004887200, 11007775.
15. Wolff S, Antelmann H, Albrecht D, Becher D, Bernhardt J, Bron S, et al. Towards the entire proteome of the model bacterium Bacillus subtilis by gel-based and gel-free approaches. J Chromatogr B Analyt Technol Biomed Life Sci 2007, 849:129-140. 10.1016/j.jchromb.2006.09.029, 17055787.
16. Antelmann H, Darmon E, Noone D, Veening JW, Westers H, Bron S, et al. The extracellular proteome of Bacillus subtilis under secretion stress conditions. Mol Microbiol 2003, 49:143-156. 10.1046/j.1365-2958.2003.03565.x, 12823817.
17. Darmon E, Dorenbos R, Meens J, Freudl R, Antelmann H, Hecker M, et al. A disulfide bond-containing alkaline phosphatase triggers a BdbC-dependent secretion stress response in Bacillus subtilis. Appl Environ Microbiol 2006, 72:6876-6885. 10.1128/AEM.01176-06, 1636209, 17088376.
18. Tjalsma H, van Dijl JM. Proteomics-based consensus prediction of protein retention in a bacterial membrane. Proteomics 2005, 5:4472-4482. 10.1002/pmic.200402080, 16220534.
19. Brockmeier U, Caspers M, Freudl R, Jockwer A, Noll T, Eggert T. Systematic screening of all signal peptides from Bacillus subtilis: a powerful strategy in optimizing heterologous protein secretion in Gram-positive bacteria. J Mol Biol 2006, 362:393-402. 10.1016/j.jmb.2006.07.034, 16930615.
20. Dalbey RE, Wang P, van Dijl JM. Membrane proteases in the bacterial protein secretion and quality control pathway. Microbiol Mol Biol Rev 2012, 76:311-330. 10.1128/MMBR.05019-11, 22688815.
21. van Roosmalen ML, Geukens N, Jongbloed JDH, Tjalsma H, Dubois J-YF, Bron S, et al. Type I signal peptidases of Gram-positive bacteria. Biochim Biophys Acta 2004, 1694:279-297. 10.1016/j.bbamcr.2004.05.006, 15546672.
22. Saito A, Hizukuri Y, Matsuo E, Chiba S, Mori H, Nishimura O, et al. Post-liberation cleavage of signal peptides is catalyzed by the site-2 protease (S2P) in bacteria. Proc Natl Acad Sci USA 2011, 108:13740-13745. 10.1073/pnas.1108376108, 3158159, 21810987.
23. Yuan J, Zweers JC, van Dijl JM, Dalbey RE. Protein transport across and into cell membranes in bacteria and archaea. Cell Mol Life Sci 2010, 67:179-199. 10.1007/s00018-009-0160-x, 19823765.
24. Sarvas M, Harwood CR, Bron S, van Dijl JM. Post-translocational folding of secretory proteins in Gram-positive bacteria. Biochim Biophys Acta 2004, 1694:311-327.
25. Jongbloed JDH, Van Der Ploeg R, van Dijl JM. Bifunctional TatA subunits in minimal Tat protein translocases. Trends Microbiol 2006, 14:2-4. 10.1016/j.tim.2005.11.001, 16303306.
26. Fröbel J, Rose P, Lausberg F, Blümmel AS, Freudl R, Müller M. Transmembrane insertion of twin-arginine signal peptides is driven by TatC and regulated by TatB. Nat Commun 2012, 3:1311. 3538955, 23250441.
27. Rollauer SE, Tarry MJ, Graham JE, Jääskeläinen M, Jäger F, Johnson S, et al. Structure of the TatC core of the twin-arginine protein transport system. Nature 2012, 492:210-214. 10.1038/nature11683, 23201679.
28. Van Der Ploeg R, Mäder U, Homuth G, Schaffer M, Denham EL, Monteferrante CG, et al. Environmental salinity determines the specificity and need for Tat-dependent secretion of the YwbN protein in Bacillus subtilis. PLoS One 2011, 6:e18140. 10.1371/journal.pone.0018140, 3068169, 21479178.
29. Van Der Ploeg R, Barnett JP, Vasisht N, Goosens VJ, Poether DC, Robinson C, et al. Salt-sensitivity of Minimal Twin-arginine Translocases. J Biol Chem 2011, 286:43759-43770. 10.1074/jbc.M111.243824, 3243503, 22041895.
30. Monteferrante CG, MacKichan C, Marchadier E, Prejean M-V, Carballido-López R, Van Dijl JM. Mapping the twin-arginine protein translocation network of Bacillus subtilis. Proteomics 2012, in press.
31. van Dijl JM, Braun PG, Robinson C, Quax WJ, Antelmann H, Hecker M, et al. Functional genomic analysis of the Bacillus subtilis Tat pathway for protein secretion. J Biotechnol 2002, 98:243-254. 10.1016/S0168-1656(02)00135-9, 12141990.
32. Van Der Ploeg R, Monteferrante CG, Piersma S, Barnett JP, Kouwen TRHM, Robinson C, et al. High salinity growth conditions promote Tat-independent secretion of Tat substrates in Bacillus subtilis. Appl Environ Microbiol 2012, 78:7733-7744. 10.1128/AEM.02093-12, 22923407.
33. Barnett JP, Eijlander RT, Kuipers OP, Robinson C. A minimal Tat system from a gram-positive organism: a bifunctional TatA subunit participates in discrete TatAC and TatA complexes. J Biol Chem 2008, 283:2534-2542.
34. Barnett JP, Van Der Ploeg R, Eijlander RT, Nenninger A, Mendel S, Rozeboom R, et al. The Twin-Arginine Translocation (Tat) systems from Bacillus subtilis display a conserved mode of complex organisation and similar substrate recognition requirements. FEBS J 2009, 276:232-243. 10.1111/j.1742-4658.2008.06776.x, 19049517.
35. Jongbloed JDH, Antelmann H, Hecker M, Nijland R, Bron S, Airaksinen U, et al. Selective contribution of the twin-arginine translocation pathway to protein secretion in Bacillus subtilis. J Biol Chem 2002, 277:44068-44078. 10.1074/jbc.M203191200, 12218047.
36. Smith H, de Jong A, Bron S, Venema G. Characterization of signal-sequence-coding regions selected from the Bacillus subtilis chromosome. Gene 1988, 70:351-61. 10.1016/0378-1119(88)90207-7, 3145906.
37. Caspers M, Brockmeier U, Degering C, Eggert T, Freudl R. 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 2010, 86:1877-1885. 10.1007/s00253-009-2405-x, 20077115.
38. Goosens VJ, Otto A, Glasner C, Monteferrante CG, Van der Ploeg R, Hecker M. Novel twin-arginine translocation pathway-dependent phenotypes of Bacillus subtilis unveiled by quantitative proteomics. J Proteome Res in press.
39. Zweers JC, Barák I, Becher D, Driessen AJM, Hecker M, Kontinen VP, et al. Towards the development of Bacillus subtilis as a cell factory for membrane proteins and protein complexes. Microb Cell Fact 2008, 7:10. 10.1186/1475-2859-7-10, 2323362, 18394159.
40. Kakeshita H, Kageyama Y, Ara K, Ozaki K, Nakamura K. Enhanced extracellular production of heterologous proteins in Bacillus subtilis by deleting the C-terminal region of the SecA secretory machinery. Mol Biotechnol 2010, 46:250-257. 10.1007/s12033-010-9295-0, 20574771.
41. Diao L, Dong Q, Xu Z, Yang S, Zhou J, Freudl R. Functional implementation of the posttranslational SecB-SecA protein-targeting pathway in Bacillus subtilis. Appl Environ Microbiol 2012, 78:651-659. 10.1128/AEM.07209-11, 3264108, 22113913.
42. Kouwen TRHM, van Dijl JM. Applications of thiol-disulfide oxidoreductases for optimized in vivo production of functionally active proteins in Bacillus. Appl Microbiol Biotechnol 2009, 85:45-52. 10.1007/s00253-009-2212-4, 2765640, 19727703.
43. Kouwen TRHM, van Dijl JM. Interchangeable modules in bacterial thiol-disulfide exchange pathways. Trends Microbiol 2009, 17:6-12. 10.1016/j.tim.2008.10.003, 19059781.
44. Kouwen TRHM, Dubois JYF, Freudl R, Quax WJ, van Dijl JM. Modulation of thiol-disulfide oxidoreductases for increased production of disulfide bond-containing proteins in Bacillus. Appl Environ Microbiol 2008, 74:7536-7545. 10.1128/AEM.00894-08, 2607156, 18952880.
45. Wu XC, Lee W, Tran L, Wong SL. Engineering a Bacillus subtilis expression-secretion system with a strain deficient in six extracellular proteases. J Bacteriol 1991, 173:4952-4958. 208183, 1907264.
46. Wu SC, Yeung JC, Duan Y, Ye R, Szarka SJ, Habibi HR, et al. 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 2002, 68:3261-3269. 10.1128/AEM.68.7.3261-3269.2002, 126797, 12089002.
47. Westers H, Braun PG, Westers L, Antelmann H, Hecker M, Jongbloed JDH, et al. Genes involved in SkfA killing factor production protect a Bacillus subtilis lipase against proteolysis. Appl Environ Microbiol 2005, 71:1899-1908. 10.1128/AEM.71.4.1899-1908.2005, 1082511, 15812018.
48. Westers L, Dijkstra DS, Westers H, van Dijl JM, Quax WJ. Secretion of functional human interleukin-3 from Bacillus subtilis. J Biotechnol 2006, 123:211-224. 10.1016/j.jbiotec.2005.11.007, 16359746.
49. Antelmann H, Yamamoto H, Sekiguchi J, Hecker M. Stabilization of cell wall proteins in Bacillus subtilis: a proteomic approach. Proteomics 2002, 2:591-602. 10.1002/1615-9861(200205)2:5<591::AID-PROT591>3.0.CO;2-8, 11987133.
50. Westers L, Westers H, Zanen G, Antelmann H, Hecker M, Noone D, et al. Genetic or chemical protease inhibition causes significant changes in the Bacillus subtilis exoproteome. Proteomics 2008, 8:2704-2713. 10.1002/pmic.200800009, 18546160.
51. Yang H, Liu L, Li J, Du G, Chen J. Heterologous expression, biochemical characterization, and overproduction of alkaline α-amylase from Bacillus alcalophilus in Bacillus subtilis. Microb Cell Fact 2011, 10:77. 10.1186/1475-2859-10-77, 3204233, 21978209.
52. Krishnappa L, Monteferrante CG, van Dijl JM. Degradation of the twin-arginine translocation substrate YwbN by extracytoplasmic proteases of Bacillus subtilis. Appl Environ Microbiol 2012, 78:7801-7804. 10.1128/AEM.02023-12, 22923395.
53. Goelzer A, Bekkal Brikci F, Martin-Verstraete I, Noirot P, Bessières P, Aymerich S, et al. Reconstruction and analysis of the genetic and metabolic regulatory networks of the central metabolism of Bacillus subtilis. BMC Syst Biol 2008, 2:20. 10.1186/1752-0509-2-20, 2311275, 18302748.
54. Goelzer A, Fromion V. Bacterial growth rate reflects a bottleneck in resource allocation. Biochim Biophys Acta 2011, 1810:978-88. 10.1016/j.bbagen.2011.05.014, 21689729.
55. Goelzer A, Fromion V, Scorletti G. Cell design in bacteria as a convex optimization problem. Automatica 2011, 47:1210-1218.
56. Bansal AK. Bioinformatics in microbial biotechnology-a mini review. Microb Cell Fact 2005, 4:19. 10.1186/1475-2859-4-19, 1182391, 15985162.
57. Papagianni M. Recent advances in engineering the central carbon metabolism of industrially important bacteria. Microb Cell Fact 2012, 11:50. 10.1186/1475-2859-11-50, 3461431, 22545791.
58. Li S, Huang D, Li Y, Wen J, Jia X. Rational improvement of the engineered isobutanol-producing Bacillus subtilis by elementary mode analysis. Microb Cell Fact 2012, 11:101. 10.1186/1475-2859-11-101, 3475101, 22862776.
59. Westers H, Dorenbos R, van Dijl JM, Kabel J, Flanagan T, Devine KM. Genome engineering reveals large dispensable regions in Bacillus subtilis. Mol Biol Evol 2003, 20:2076-2090. 10.1093/molbev/msg219, 12949151.
60. Morimoto T, Kadoya R, Endo K, Tohata M, Sawada K, Liu S. Enhanced recombinant protein productivity by genome reduction in Bacillus subtilis. DNA Res 2008, 15:73-81. 10.1093/dnares/dsn002, 2650625, 18334513.
61. Manabe K, Kageyama Y, Morimoto T, Ozawa T, Sawada K, Endo K. Combined effect of improved cell yield and increased specific productivity enhances recombinant enzyme production in genome-reduced Bacillus subtilis strain MGB874. Appl Environ Microbiol 2011, 77:8370-81. 10.1128/AEM.06136-11, 3233064, 21965396.
62. Manabe K, Kageyama Y, Tohata M, Ara K, Ozaki K, Ogasawara N. High external pH enables more efficient secretion of alkaline α-amylase AmyK38 by Bacillus subtilis. Microb Cell Fact 2012, 11:74. 10.1186/1475-2859-11-74, 3424145, 22681752.
63. Tanaka K, Henry CS, Zinner JF, Jolivet E, Cohoon MP, Xia F. Building the repertoire of dispensable chromosome regions in Bacillus subtilis entails major refinement of cognate large-scale metabolic model. Nucleic Acids Res 2013, 41:687-699. 10.1093/nar/gks963, 23109554.
64. le Tam T, Antelmann H, Eymann C, Albrecht D, Bernhardt J, Hecker M. Proteome signatures for stress and starvation in Bacillus subtilis as revealed by a 2-D gel image color coding approach. Proteomics 2006, 6:4565-85. 10.1002/pmic.200600100, 16847875.
65. Kabisch J, Thürmer A, Hübel T, Popper L, Daniel R, Schweder T. Characterization and optimization of Bacillus subtilis ATCC 6051 as an expression host. J Biotechnol 2012, in press.
66. Marciniak BC, Trip H, Van-der Veek PJ, Kuipers OP. Comparative transcriptional analysis of Bacillus subtilis cells overproducing either secreted proteins, lipoproteins or membrane proteins. Microb Cell Fact 2012, 11:66. 10.1186/1475-2859-11-66, 3514339, 22624725.
67. Toymentseva AA, Schrecke K, Sharipova MR, Mascher T. The LIKE system, a novel protein expression toolbox for Bacillus subtilis based on the liaI promoter. Microb Cell Fact 2012, 11:143. 10.1186/1475-2859-11-143, 23110498.