Butanol tolerance regulated by a two-component response regulator Slr1037 in photosynthetic Synechocystis sp. PCC 6803

Biotechnology for Biofuels

Volumn 7, Issue 1, 2014, Pages

  Chen, Lei ^a,b,c   Wu, Lina ^a,b,c   Wang, Jiangxin ^a,b,c   Zhang, Weiwen ^a,b,c  

^a TIANJIN UNIVERSITY   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^c Collaborative Innovation Center of Chemical Science and Engineering   (China)

Author keywords

Butanol; Proteomics; Response regulator; Synechocystis; Tolerance

Indexed keywords

AMINO ACIDS; BUTENES; CARBON DIOXIDE; FITS AND TOLERANCES; GENE ENCODING; MOLECULAR BIOLOGY; PROTEINS; SIGNAL TRANSDUCTION;

METHIONINE SULFOXIDE REDUCTASE; PROTEOMICS; RESPONSE REGULATORS; REVERSE TRANSCRIPTION PCR; SYNECHOCYSTIS; SYNECHOCYSTIS SP. PCC 6803; TRANSCRIPTIONAL ENGINEERINGS; TWO-COMPONENT SIGNAL TRANSDUCTION SYSTEMS;

PLANTS (BOTANY);

ALCOHOL; CARBON DIOXIDE; CYANOBACTERIUM; PHOTOSYNTHESIS; POLYMERASE CHAIN REACTION; PROTEIN; PROTEOMICS; TOXICITY;

CYANOBACTERIA; SYNECHOCYSTIS; SYNECHOCYSTIS SP. PCC 6803;

EID: 84902550995     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/1754-6834-7-89     Document Type: Article

References (66)

1. Biobutanol: an attractive biofuel. Durre P, Biotechnol J 2007 2 1525 1534 10.1002/biot.200700168 17924389
2. Solventogenic enzymes of Clostridium acetobutylicum: catalytic properties, genetic organization, and transcriptional regulation. Durre P, Fischer RJ, Kuhn A, Lorenz K, Schreiber W, Sturzenhofecker B, Ullmann S, Winzer K, Sauer U, FEMS Microbiol Rev 1995 17 251 262 10.1016/0168-6445(95)00006-X 7576767
3. Fermentative butanol production by Clostridia. Lee SY, Park JH, Jang SH, Nielsen LK, Kim J, Jung KS, Biotechnol Bioeng 2008 101 209 228 10.1002/bit.22003 18727018
4. Problems with the microbial production of butanol. Zheng YN, Li LZ, Xian M, Ma YJ, Yang JM, Xu X, He DZ, J Ind Microbiol Biotechnol 2009 36 1127 1138 10.1007/s10295-009-0609-9 19562394
5. Fermentative production of butanol-the industrial perspective. Green EM, Curr Opin Biotechnol 2011 22 337 343 10.1016/j.copbio.2011.02.004 21367598
6. Metabolic engineering of Escherichia coli for 1-butanol production. Atsumi S, Cann AF, Connor MR, Shen CR, Smith KM, Brynildsen MP, Chou KJ, Hanai T, Liao JC, Metab Eng 2008 10 305 311 10.1016/j.ymben.2007.08.003 17942358
7. Expression of Clostridium acetobutylicum butanol synthetic genes in Escherichia coli. Inui M, Suda M, Kimura S, Yasuda K, Suzuki H, Toda H, Yamamoto S, Okino S, Suzuki N, Yukawa H, Appl Microbiol Biotechnol 2008 77 1305 1316 10.1007/s00253-007-1257-5 18060402
8. Metabolic engineering of Escherichia coli for 1-butanol and 1-propanol production via the keto-acid pathways. Shen CR, Liao JC, Metab Eng 2008 10 312 320 10.1016/j.ymben.2008.08.001 18775501
9. Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels. Atsumi S, Hanai T, Liao JC, Nature 2008 451 86 89 10.1038/nature06450 18172501
10. Reconstructing the clostridial n-butanol metabolic pathway in Lactobacillus brevis. Berezina OV, Zakharova NV, Brandt A, Yarotsky SV, Schwarz WH, Zverlov VV, Appl Microbiol Biotechnol 2010 87 635 646 10.1007/s00253-010- 2480-z 20195860
11. Cyanobacterial biofuel production. Machado IM, Atsumi S, J Biotechnol 2012 162 50 56 10.1016/j.jbiotec.2012.03.005 22446641
12. Metabolic engineering of cyanobacteria for 1-butanol production from carbon dioxide. Lan EI, Liao JC, Metab Eng 2011 13 353 363 10.1016/j.ymben.2011. 04.004 21569861
13. ATP drives direct photosynthetic production of 1-butanol in cyanobacteria. Lan EI, Liao JC, Proc Natl Acad Sci U S A 2012 109 6018 6023 10.1073/pnas.1200074109 22474341
14. A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: from biofuels and chemicals, to biocatalysis and bioremediation. Nicolaou SA, Gaida SM, Papoutsakis ET, Metab Eng 2010 12 307 331 10.1016/j.ymben.2010.03.004 20346409
15. Engineering microbes for tolerance to next-generation biofuels. Dunlop MJ, Biotechnol Biofuels 2011 4 32 10.1186/1754-6834-4-32 21936941
16. An integrated network approach identifies the isobutanol response network of Escherichia coli. Brynildsen MP, Liao JC, Mol Syst Biol 2009 5 277 19536200
17. Functional genomic study of exogenous n-butanol stress in Escherichia coli. Rutherford BJ, Dahl RH, Price RE, Szmidt HL, Benke PI, Mukhopadhyay A, Keasling JD, Appl Environ Microbiol 2010 76 1935 1945 10.1128/AEM.02323-09 20118358
18. Engineering yeast transcription machinery for improved ethanol tolerance and production. Alper H, Moxley J, Nevoigt E, Fink GR, Stephanopoulos G, Science 2006 314 1565 1568 10.1126/science.1131969 17158319
19. Transcriptional analysis of spo0A overexpression in Clostridium acetobutylicum and its effect on the cell's response to butanol stress. Alsaker KV, Spitzer TR, Papoutsakis ET, J Bacteriol 2004 186 1959 1971 10.1128/JB.186.7.1959-1971.2004 15028679
20. Laboratory-evolved mutants of an exogenous global regulator, IrrE from Deinococcus radiodurans, enhance stress tolerances of Escherichia coli. Chen T, Wang J, Yang R, Li J, Lin M, Lin Z, PLoS One 2011 6 16228 10.1371/journal.pone. 0016228 21267412
21. Engineering global transcription factor cyclic AMP receptor protein of Escherichia coli for improved 1-butanol tolerance. Zhang H, Chong H, Ching CB, Song H, Jiang R, Appl Microbiol Biotechnol 2012 94 1107 1117 10.1007/s00253-012-4012-5 22466954
22. Evolution of two-component signal transduction systems. Capra EJ, Laub MT, Annu Rev Microbiol 2012 66 325 347 10.1146/annurev-micro-092611-150039 22746333
23. The role of two-component regulation systems in the physiology of the bacterial cell. Bekker M, de Teixeira MM, Hellingwerf KJ, Sci Prog 2006 89 213 242 10.3184/003685006783238308 17338439
24. Proteomic analysis reveals resistance mechanism against biofuel hexane in Synechocystis sp. PCC 6803. Liu J, Chen L, Wang J, Qiao J, Zhang W, Biotechnol Biofuels 2012 5 68 10.1186/1754-6834-5-68 22958739
25. RNA-seq based identification and mutant validation of gene targets related to ethanol resistance in cyanobacterial Synechocystis sp. PCC 6803. Wang J, Chen L, Huang S, Liu J, Ren X, Tian X, Qiao J, Zhang W, Biotechnol Biofuels 2012 5 89 10.1186/1754-6834-5-89 23259593
26. Quantitative proteomics reveals dynamic responses of Synechocystis sp. PCC 6803 to next-generation biofuel butanol. Tian X, Chen L, Wang J, Qiao J, Zhang W, J Proteomics 2013 78 326 345 23079071
27. Quantitative iTRAQ LC-MS/MS proteomics reveals metabolic responses to biofuel ethanol in cyanobacterial Synechocystis sp. PCC 6803. Qiao J, Wang J, Chen L, Tian X, Huang S, Ren X, Zhang W, J Proteome Res 2012 11 5286 5300 10.1021/pr300504w 23062023
28. Systematic characterization of hypothetical proteins in Synechocystis sp. PCC 6803 reveals proteins functionally relevant to stress responses. Qiao J, Shao M, Chen L, Wang J, Wu G, Tian X, Liu J, Huang S, Zhang W, Gene 2013 512 6 15 10.1016/j.gene.2012.10.004 23063937
29. Integrated OMICS guided engineering of biofuel butanol-tolerance in photosynthetic Synechocystis sp. PCC 6803. Zhu H, Ren X, Wang J, Song Z, Shi M, Qiao J, Tian X, Liu J, Chen L, Zhang W, Biotechnol Biofuels 2013 6 106 10.1186/1754-6834-6-106 23883549
30. Engineering bacterial signals and sensors. Salis H, Tamsir A, Voigt C, Contrib Microbiol 2009 16 194 225 19494587
31. Cyanobacterial two-component proteins: structure, diversity, distribution, and evolution. Ashby MK, Houmard J, Microbiol Mol Biol Rev 2006 70 472 509 10.1128/MMBR.00046-05 16760311
32. Identical Hik-Rre systems are involved in perception and transduction of salt signals and hyperosmotic signals but regulate the expression of individual genes to different extents in Synechocystis. Shoumskaya MA, Paithoonrangsarid K, Kanesaki Y, Los DA, Zinchenko VV, Tanticharoen M, Suzuki I, Murata N, J Biol Chem 2005 280 21531 21538 10.1074/jbc.M412174200 15805106
33. A large-scale protein protein interaction analysis in Synechocystis sp. PCC6803. Sato S, Shimoda Y, Muraki A, Kohara M, Nakamura Y, Tabata S, DNA Res 2007 14 207 216 10.1093/dnares/dsm021 18000013
34. Photophysical diversity of two novel cyanobacteriochromes with phycocyanobilin chromophores: photochemistry and dark reversion kinetics. Chen Y, Zhang J, Luo J, Tu JM, Zeng XL, Xie J, Zhou M, Zhao JQ, Scheer H, Zhao KH, FEBS J 2012 279 40 54 10.1111/j.1742-4658.2011.08397.x 22008418
35. Structural analysis of four large plasmids harboring in a unicellular cyanobacterium, Synechocystis sp. PCC 6803. Kaneko T, Nakamura Y, Sasamoto S, Watanabe A, Kohara M, Matsumoto M, Shimpo S, Yamada M, Tabata S, DNA Res 2003 10 221 228 10.1093/dnares/10.5.221 14686584
36. Inactivation of the open reading frame slr0399 in Synechocystissp. PCC 6803 functionally complements mutations near the Q(A) niche of photosystem II. A possible role of Slr0399 as a chaperone for quinone binding. Ermakova-Gerdes S, Vermaas W, J Biol Chem 1999 274 30540 30549 10.1074/jbc.274.43.30540 10521436
37. Attachment of noncognate chromophores to CpcA of Synechocystis sp. PCC 6803 and Synechococcus sp. PCC 7002 by heterologous expression in Escherichia coli. Alvey RM, Biswas A, Schluchter WM, Bryant DA, Biochemistry 2011 50 4890 4902 10.1021/bi200307s 21553904
38. Expression and regulation of the crucial plant-like ferredoxin of cyanobacteria. Mazouni K, Domain F, Chauvat F, Cassier-Chauvat C, Mol Microbiol 2003 49 1019 1029 10.1046/j.1365-2958.2003.03609.x 12890025
39. Role of histidine-86 in the catalytic mechanism of ferredoxin:thioredoxin reductase. Walters EM, Garcia-Serres R, Naik SG, Bourquin F, Glauser DA, Schurmann P, Huynh BH, Johnson MK, Biochemistry 2009 48 1016 1024 10.1021/bi802074p 19132843
40. Photosynthetic regulation of the cyanobacterium Synechocystis sp. PCC 6803 thioredoxin system and functional analysis of TrxB (Trx x) and TrxQ (Trx y) thioredoxins. Perez-Perez ME, Martin-Figueroa E, Florencio FJ, Mol Plant 2009 2 270 283 19825613
41. The role of cytochrome c-550 as studied through reverse genetics and mutant characterization in Synechocystis sp. PCC 6803. Shen JR, Vermaas W, Inoue Y, J Biol Chem 1995 270 6901 6907 10.1074/jbc.270.12.6901 7896839
42. Transcript profiling reveals new insights into the acclimation of the mesophilic fresh-water cyanobacterium Synechococcus elongatus PCC 7942 to iron starvation. Nodop A, Pietsch D, Hocker R, Becker A, Pistorius EK, Forchhammer K, Michel KP, Plant Physiol 2008 147 747 763 10.1104/pp.107.114058 18424627
43. Proteomic analysis of Pseudomonas putida reveals an organic solvent tolerance-related gene mmsB. Ni Y, Song L, Qian X, Sun Z, PLoS One 2013 8 55858 10.1371/journal.pone.0055858 23409067
44. N-terminus deletion affecting the preparation of soluble cyanobacterial glutaredoxin in Escherichia coli. Li M, Yang Q, Gao Y, Wu Q, Biochemistry (Mosc) 2007 72 313 319 10.1134/S0006297907030091 17447885
45. The glutathione/glutaredoxin system is essential for arsenate reduction in Synechocystis sp. strain PCC 6803. Lopez-Maury L, Sanchez-Riego AM, Reyes JC, Florencio FJ, J Bacteriol 2009 191 3534 3543 10.1128/JB.01798-08 19304854
46. A cyanobacterial hemoglobin with unusual ligand binding kinetics and stability properties. Thorsteinsson MV, Bevan DR, Potts M, Dou Y, Eich RF, Hargrove MS, Gibson QH, Olson JS, Biochemistry 1999 38 2117 2126 10.1021/bi9819172 10026295
47. Molecular biology of cyanobacterial salt acclimation. Hagemann M, FEMS Microbiol Rev 2011 35 87 123 10.1111/j.1574-6976.2010.00234.x 20618868
48. RpaB, another response regulator operating circadian clock-dependent transcriptional regulation in Synechococcus elongatus PCC 7942. Hanaoka M, Takai N, Hosokawa N, Fujiwara M, Akimoto Y, Kobori N, Iwasaki H, Kondo T, Tanaka K, J Biol Chem 2012 287 26321 26327 10.1074/jbc.M111.338251 22665493
49. Paradigm for industrial strain improvement identifies sodium acetate tolerance loci in Zymomonas mobilis and Saccharomyces cerevisiae. Yang S, Land ML, Klingeman DM, Pelletier DA, Lu TY, Martin SL, Guo HB, Smith JC, Brown SD, Proc Natl Acad Sci U S A 2010 107 10395 10400 10.1073/pnas.0914506107 20484677
50. The hglK gene is required for localization of heterocyst-specific glycolipids in the cyanobacterium Anabaena sp. strain PCC 7120. Black K, Buikema WJ, Haselkorn R, J Bacteriol 1995 177 6440 6448 7592418
51. Fra proteins influencing filament integrity, diazotrophy and localization of septal protein SepJ in the heterocyst-forming cyanobacterium Anabaena sp. Merino-Puerto V, Mariscal V, Mullineaux CW, Herrero A, Flores E, Mol Microbiol 2010 75 1159 1170 10.1111/j.1365-2958.2009.07031.x 20487302
52. Tolerance and stress response to ethanol in the yeast Saccharomyces cerevisiae. Ding J, Huang X, Zhang L, Zhao N, Yang D, Zhang K, Appl Microbiol Biotechnol 2009 85 253 263 10.1007/s00253-009-2223-1 19756577
53. 2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, Kaplan A, Ogawa T, Proc Natl Acad Sci U S A 2001 98 11789 11794 10.1073/pnas.191258298 11562454
54. A noncanonical WD-repeat protein from the cyanobacterium Synechocystis PCC6803: structural and functional study. Hisbergues M, Gaitatzes CG, Joset F, Bedu S, Smith TF, Protein Sci 2001 10 293 300 10.1110/ps.22701 11266615
55. Gene expression patterns of sulfur starvation in Synechocystis sp. PCC 6803. Zhang Z, Pendse ND, Phillips KN, Cotner JB, Khodursky A, BMC Genomics 2008 9 344 10.1186/1471-2164-9-344 18644144
56. The quantitative proteomic response of Synechocystis sp. PCC6803 to phosphate acclimation. Fuszard MA, Ow SY, Gan CS, Noirel J, Ternan NG, McMullan G, Biggs CA, Reardon KF, Wright PC, Aquat Biosyst 2013 9 5 10.1186/2046-9063-9-5 23442353
57. Disruption of a Synechocystis sp. PCC 6803 gene with partial similarity to phytochrome genes alters growth under changing light qualities. Wilde A, Churin Y, Schubert H, Borner T, FEBS Lett 1997 406 89 92 10.1016/S0014-5793(97) 00248-2 9109392
58. Characterization of single and double inactivation strains reveals new physiological roles for group 2 sigma factors in the cyanobacterium Synechocystis sp. PCC 6803. Pollari M, Gunnelius L, Tuominen I, Ruotsalainen V, Tyystjarvi E, Salminen T, Tyystjarvi T, Plant Physiol 2008 147 1994 2005 10.1104/pp.108.122713 18539776
59. Detecting subtle sequence signals: a Gibbs sampling strategy for multiple alignment. Lawrence CE, Altschul SF, Boguski MS, Liu JS, Neuwald AF, Wootton JC, Science 1993 262 208 214 10.1126/science.8211139 8211139
60. Gibbs Recursive Sampler: finding transcription factor binding sites. Thompson W, Rouchka EC, Lawrence CE, Nucleic Acids Res 2003 31 3580 3585 10.1093/nar/gkg608 12824370
61. Regulatory sequence analysis tools. van Helden J, Nucleic Acids Res 2003 31 3593 3596 10.1093/nar/gkg567 12824373
62. WebLogo: a sequence logo generator. Crooks GE, Hon G, Chandonia JM, Brenner SE, Genome Res 2004 14 1188 1190 10.1101/gr.849004 15173120
63. Bacterial glutathione S-transferases: what are they good for? Vuilleumier S, J Bacteriol 1997 179 1431 1441 9045797
64. Glutathione in Synechocystis 6803: a closer look into the physiology of a gshB mutant. Cameron JC, Pakrasi HB, Plant Signal Behav 2011 6 89 92 10.4161/psb.6.1.14145 21301218
65. Optimization of fusion PCR for in vitro construction of gene knockout fragments. Wang HL, Postier BL, Burnap RL, Biotechniques 2002 33 26 30 12139251
66. Protein phosphatase PphA from Synechocystis sp. PCC 6803: the physiological framework of PII-P dephosphorylation. Kloft N, Rasch G, Forchhammer K, Microbiology 2005 151 1275 1283 10.1099/mic.0.27771-0 15817794