Microevolution from shock to adaptation revealed strategies improving ethanol tolerance and production in Thermoanaerobacter

Biotechnology for Biofuels

Volumn 6, Issue 1, 2013, Pages

  Lin, Lu ^a   Ji, Yuetong ^a   Tu, Qichao ^b   Huang, Ranran ^a   Teng, Lin ^a   Zeng, Xiaowei ^a   Song, Houhui ^a   Wang, Kun ^a   Zhou, Qian ^a   Li, Yifei ^a   Cui, Qiu ^a   He, Zhili ^b   Zhou, Jizhong ^b   Xu, Jian ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

Adaptation; Ethanol; Microevolution; Shock; Thermophile

Indexed keywords

ADAPTATION; BIOFUELS AND BIOCHEMICALS; MICROEVOLUTION; PHOSPHOTRANSFERASE SYSTEM; RESISTANCE-NODULATION-CELL DIVISIONS; SHOCK; THERMOPHILE; TRANSCRIPTIONAL NETWORKS;

AMINO ACIDS; BACTERIA; CELL PROLIFERATION; GENES; GENETIC ENGINEERING; INDUSTRIAL APPLICATIONS; PRODUCTIVITY;

ETHANOL;

ADAPTATION; BIOCHEMISTRY; BIOFUEL; BIOTECHNOLOGY; CATABOLISM; ENZYME ACTIVITY; ETHANOL; GENETIC ENGINEERING; MOLECULAR ANALYSIS; SOLVENT; THERMOPHILIC BACTERIUM;

THERMOANAEROBACTER; THERMOANAEROBACTER SP.;

EID: 84880334488     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/1754-6834-6-103     Document Type: Article

References (63)

1. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, Lenski RE, Kim JF, Nature 2009 461 1243 1247 10.1038/nature08480 19838166
2. Wiegel J, Adams MWW, Thermophiles: The Keys to the Molecular Evolution and the Origin of Life Philadelphia: Taylor & Francis e-Library 2003
3. The evolutionary origin of complex features. Lenski RE, Ofria C, Pennock RT, Adami C, Nature 2003 423 139 144 10.1038/nature01568 12736677
4. Mutant alcohol dehydrogenase leads to improved ethanol tolerance in Clostridium thermocellum. Brown SD, Guss AM, Karpinets TV, Parks JM, Smolin N, Yang S, Land ML, Klingeman DM, Bhandiwad A, Rodriguez M Jr, et al. Proc Natl Acad Sci USA 2011 108 13752 13757 10.1073/pnas.1102444108 21825121
5. Evolution combined with genomic study elucidates genetic bases of isobutanol tolerance in Escherichia coli. Minty JJ, Lesnefsky AA, Lin F, Chen Y, Zaroff TA, Veloso AB, Xie B, McConnell CA, Ward RJ, Schwartz DR, et al. Microb Cell Fact 2011 10 18 10.1186/1475-2859-10-18 21435272
6. Evolution, genomic analysis, and reconstruction of isobutanol tolerance in Escherichia coli. Atsumi S, Wu TY, Machado IM, Huang WC, Chen PY, Pellegrini M, Liao JC, Mol Syst Biol 2010 6 449 21179021
7. Genomic analysis of a key innovation in an experimental Escherichia coli population. Blount ZD, Barrick JE, Davidson CJ, Lenski RE, Nature 2012 489 513 518 10.1038/nature11514 22992527
8. 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
9. An integrated network approach identifies the isobutanol response network of Escherichia coli. Brynildsen MP, Liao JC, Mol Syst Biol 2009 5 277 19536200
10. The ethanol stress response and ethanol tolerance of Saccharomyces cerevisiae. Stanley D, Bandara A, Fraser S, Chambers PJ, Stanley GA, J Appl Microbiol 2010 109 13 24 20070446
11. Mechanisms of ethanol tolerance in Saccharomyces cerevisiae. Ma M, Liu ZL, Appl Microbiol Biotechnol 2010 87 829 845 10.1007/s00253-010-2594-3 20464391
12. Overexpression of groESL in Clostridium acetobutylicum results in increased solvent production and tolerance, prolonged metabolism, and changes in the cell's transcriptional program. Tomas CA, Welker NE, Papoutsakis ET, Appl Environ Microbiol 2003 69 4951 4965 10.1128/AEM.69.8.4951-4965.2003 12902291
13. Transcriptional analysis of butanol stress and tolerance in Clostridium acetobutylicum. Tomas CA, Beamish J, Papoutsakis ET, J Bacteriol 2004 186 2006 2018 10.1128/JB.186.7.2006-2018.2004 15028684
14. 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
15. Genome-wide screening for trait conferring genes using DNA microarrays. Gill RT, Wildt S, Yang YT, Ziesman S, Stephanopoulos G, Proc Natl Acad Sci USA 2002 99 7033 7038 10.1073/pnas.102154799 11997466
16. Rapid dissection of a complex phenotype through genomic-scale mapping of fitness altering genes. Warnecke TE, Lynch MD, Karimpour-Fard A, Lipscomb ML, Handke P, Mills T, Ramey CJ, Hoang T, Gill RT, Metab Eng 2010 12 241 250 10.1016/j.ymben.2009.12.002 20060059
17. Harnessing recombination to speed adaptive evolution in Escherichia coli. Winkler J, Kao KC, Metab Eng 2012 14 487 495 10.1016/j.ymben.2012.07.004 22842472
18. Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Kao KC, Sherlock G, Nat Genet 2008 40 1499 1504 10.1038/ng.280 19029899
19. Genomic library screens for genes involved in n-butanol tolerance in Escherichia coli. Reyes LH, Almario MP, Kao KC, PLoS One 2011 6 17678 10.1371/journal.pone.0017678 21408113
20. Engineering genomes in multiplex. Woodruff LB, Gill RT, Curr Opin Biotechnol 2011 22 576 583 10.1016/j.copbio.2011.04.019 21592776
21. Dynamics of genomic-library enrichment and identification of solvent tolerance genes for Clostridium acetobutylicum. Borden JR, Papoutsakis ET, Appl Environ Microbiol 2007 73 3061 3068 10.1128/AEM.02296-06 17337545
22. 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
23. Rapid profiling of a microbial genome using mixtures of barcoded oligonucleotides. Warner JR, Reeder PJ, Karimpour-Fard A, Woodruff LBA, Gill RT, Nat Biotech 2010 28 856 862 10.1038/nbt.1653
24. In thermophiles: general, molecular and applied microbiology New York: John Wiley & Sons, Brock TD, 1986
25. The Thermoanaerobacter glycobiome reveals mechanisms of pentose and hexose co-utilization in bacteria. Lin L, Song H, Tu Q, Qin Y, Zhou A, Liu W, He Z, Zhou J, Xu J, PLoS Genet 2011 7 1002318 10.1371/journal.pgen.1002318 22022280
26. Dissecting and engineering metabolic and regulatory networks of thermophilic bacteria for biofuel production. Lin L, Xu J, Biotechnol Adv 2013 10.1016/j.biotechadv.2013.03.003
27. Thermophilic ethanologenesis: future prospects for second-generation bioethanol production. Taylor MP, Eley KL, Martin S, Tuffin MI, Burton SG, Cowan DA, Trends Biotechnol 2009 27 398 405 10.1016/j.tibtech.2009.03.006 19481826
28. Metabolic engineering of a thermophilic bacterium to produce ethanol at high yield. Shaw AJ, Podkaminer KK, Desai SG, Bardsley JS, Rogers SR, Thorne PG, Hogsett DA, Lynd LR, Proc Natl Acad Sci USA 2008 105 13769 13774 10.1073/pnas.0801266105 18779592
29. Microbial responses to solvent and alcohol stress. Taylor M, Tuffin M, Burton S, Eley K, Cowan D, Biotechnol J 2008 3 1388 1397 10.1002/biot.200800158 18956369
30. Analysis of composition and structure of Clostridium thermocellum membranes from wild-type and ethanol-adapted strains. Timmons MD, Knutson BL, Nokes SE, Strobel HJ, Lynn BC, Appl Microbiol Biotechnol 2009 82 929 939 10.1007/s00253-009-1891-1 19221734
31. Regulatory and metabolic rewiring during laboratory evolution of ethanol tolerance in E. coli. Goodarzi H, Bennett BD, Amini S, Reaves ML, Hottes AK, Rabinowitz JD, Tavazoie S, Mol Syst Biol 2010 6 378 20531407
32. Enzyme mechanism as a kinetic control element for designing synthetic biofuel pathways. Bond-Watts BB, Bellerose RJ, Chang MCY, Nat Chem Biol 2011 7 222 227 10.1038/nchembio.537 21358636
33. Proteome reference map and comparative proteomic analysis between a wild type Clostridium acetobutylicum DSM 1731 and its mutant with enhanced butanol tolerance and butanol yield. Mao S, Luo Y, Zhang T, Li J, Bao G, Zhu Y, Chen Z, Zhang Y, Li Y, Ma Y, J Proteome Res 2010 9 3046 3061 10.1021/pr9012078 20426490
34. Correlation of genomic and physiological traits of thermoanaerobacter species with biofuel yields. Hemme CL, Fields MW, He Q, Deng Y, Lin L, Tu Q, Mouttaki H, Zhou A, Feng X, Zuo Z, et al. Appl Environ Microbiol 2011 77 7998 8008 10.1128/AEM.05677-11 21948836
35. Avoiding dangerous missense: thermophiles display especially low mutation rates. Drake JW, PLoS Genet 2009 5 1000520 10.1371/journal.pgen.1000520 19543367
36. Moat AG, Foster JW, Spector MP, Microbial stress responses New York: Wiley-Liss, Inc 4 Microbial Physiology. 2002
37. Conserving a volatile metabolite: a role for carboxysome-like organelles in Salmonella enterica. Penrod JT, Roth JR, J Bacteriol 2006 188 2865 2874 10.1128/JB.188.8.2865-2874.2006 16585748
38. Arginine catabolism by sourdough lactic acid bacteria: Purification and characterization of the arginine deiminase pathway enzymes from Lactobacillus sanfranciscensis CB1. Angelis MD, Mariotti L, Rossi J, Servili M, Fox PF, Rollan G, Gobbetti M, Appl Environ Microbiol 2002 68 6193 6201 10.1128/AEM.68.12.6193- 6201.2002 12450844
39. The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). Bateman A, Bycroft M, J Mol Biol 2000 299 1113 1119 10.1006/jmbi.2000.3778 10843862
40. Turner PC, Mclennan AG, Bates AD, White MRH, Instant Notes in Molecular Biology Liverpool, UK: University of Liverpool 3 2001
41. Bacterial stress responses: what doesn't kill them can make then stronger. Boor KJ, PLoS Biol 2006 4 23 10.1371/journal.pbio.0040023 16535775
42. Light-limitation on predator-prey interactions: consequences for metabolism and locomotion of deep-sea cephalopods. Seibel BA, Thuesen EV, Childress JJ, Biol Bull 2000 198 284 298 10.2307/1542531 10786948
43. A new TetR family transcriptional regulator required for morphogenesis in Streptomyces coelicolor. Hillerich B, Westpheling J, J Bacteriol 2008 190 61 67 10.1128/JB.01316-07 17965158
44. Engineering microbes for tolerance to next-generation biofuels. Dunlop MJ, Biotechnol Biofuels 2011 4 32 10.1186/1754-6834-4-32 21936941
45. The biochemistry and genetics of capsular polysaccharide production in bacteria. Roberts IS, Annu Rev Microbiol 1996 50 285 315 10.1146/annurev.micro. 50.1.285 8905082
46. Increase of organic solvent tolerance by overexpression of manXYZ in Escherichia coli. Okochi M, Kurimoto M, Shimizu K, Honda H, Appl Microbiol Biotechnol 2007 73 1394 1399 10.1007/s00253-006-0624-y 17053901
47. Bacterial cell shape. Cabeen MT, Jacobs-Wagner C, Nat Rev Microbiol 2005 3 601 610 10.1038/nrmicro1205 16012516
48. FapR, a bacterial transcription factor involved in global regulation of membrane lipid biosynthesis. Schujman GE, Paoletti L, Grossman AD, de Mendoza D, Dev Cell 2003 4 663 672 10.1016/S1534-5807(03)00123-0 12737802
49. 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
50. Sigma M, an ECF RNA polymerase sigma factor of Bacillus subtilis 168, is essential for growth and survival in high concentrations of salt. Horsburgh MJ, Moir A, Mol Microbiol 1999 32 41 50 10.1046/j.1365-2958.1999.01323.x 10216858
51. The aldehyde/alcohol dehydrogenase (AdhE) in relation to the ethanol formation in Thermoanaerobacter ethanolicus JW200. Peng H, Wu G, Shao W, Anaerobe 2008 14 125 127 10.1016/j.anaerobe.2007.09.004 17981479
52. Sigma factor mimicry involved in regulation of general stress response. Vorholt JA, Francez-Charlot A, Frunzke J, Reichen C, Ebneter JZ, Gourion B, Proc Natl Acad Sci USA 2009 106 3467 3472 10.1073/pnas.0810291106 19218445
53. Identification of gene targets eliciting improved alcohol tolerance in Saccharomyces cerevisiae through inverse metabolic engineering. Hong ME, Lee KS, Yu BJ, Sung YJ, Park SM, Koo HM, Kweon DH, Park JC, Jin YS, J Biotechnol 2010 149 52 59 10.1016/j.jbiotec.2010.06.006 20600383
54. Ultrasound-mediated DNA transformation in thermophilic Gram-positive anaerobes. Lin L, Song H, Ji Y, He Z, Pu Y, Zhou J, Xu J, PLoS One 2010 5 9 12582 10.1371/journal.pone.0012582 20838444
55. Ethyl Methanesulfonate Mutagenesis in Extremely Halophilic Archaebacteria-Isolation of Auxotrophic Mutants of Haloferax-Mediterranei and Haloferax-Gibbonsii. Nieto JJ, Fernandezcastillo R, Megias M, Ruizberraquero F, Curr Microbiol 1992 24 41 47 10.1007/BF01570098
56. Functional molecular ecological networks. Zhou J, Deng Y, Luo F, He Z, Tu Q, Zhi X, MBio 2010 1 4 00169 00110 20941329
57. TM4 microarray software suite. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J, Methods Enzymol 2006 411 134 193 16939790
58. Molecular mechanisms of ethanol-induced pathogenesis revealed by RNA-sequencing. Camarena L, Bruno V, Euskirchen G, Poggio S, Snyder M, PLoS Pathog 2010 6 1000834 10.1371/journal.ppat.1000834 20368969
59. SOAP2: an improved ultrafast tool for short read alignment. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J, Bioinformatics 2009 25 1966 1967 10.1093/bioinformatics/btp336 19497933
60. Mapping short DNA sequencing reads and calling variants using mapping quality scores. Li H, Ruan J, Durbin R, Genome Res 2008 18 1851 1858 10.1101/gr.078212.108 18714091
61. The Sequence alignment/map (SAM) format and SAMtools. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Bioinformatics 2009 25 2078 2079 10.1093/bioinformatics/btp352 19505943
62. A framework for variation discovery and genotyping using next-generation DNA sequencing data. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, Angel GD, Rivas MA, Hanna M, et al. Nat Genet 2011 43 491 498 10.1038/ng.806 21478889
63. Modeller: generation and refinement of homology-based protein structure models. Fiser A, Sali A, Methods Enzymol 2003 374 461 491 14696385