A Targetron System for Gene Targeting in Thermophiles and Its Application in Clostridium thermocellum

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Mohr, Georg ^a   Hong, Wei ^b,d   Zhang, Jie ^b,d   Cui, Gu zhen ^b   Yang, Yunfeng ^c   Cui, Qiu ^b   Liu, Ya jun ^b   Lambowitz, Alan M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b QINGDAO INSTITUTE OF BIOENERGY AND BIOPROCESS TECHNOLOGY   (China)

^c TSINGHUA UNIVERSITY   (China)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ALCOHOL; CARBON; LACTATE DEHYDROGENASE; LACTIC ACID; PHOSPHATE ACETYLTRANSFERASE;

ARTICLE; BACTERIUM COLONY; BACTERIUM TRANSFORMATION; BASE PAIRING; BIOFUEL PRODUCTION; CIPA GENE; CLOSTRIDIUM THERMOCELLUM; CYANOBACTERIUM; DNA SEQUENCE; FERMENTATION; GEL MOBILITY SHIFT ASSAY; GENE; GENE CONSTRUCT; GENE DISRUPTION; GENE INTERACTION; GENE TARGETING; HFAT GENE; HIGH TEMPERATURE; HYD GENE; INTRON; LACZ GENE; LDH GENE; MELTING POINT; MESOPHILIC BACTERIUM; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PTA GENE; PYRF GENE; TARGETRON; THERMOPHILE; THERMOSYNECHOCOCCUS ELONGATUS;

BASE PAIRING; BASE SEQUENCE; BINDING SITES; CHROMOSOMES, BACTERIAL; CLOSTRIDIUM THERMOCELLUM; CYANOBACTERIA; ESCHERICHIA COLI; GENE ORDER; GENE TARGETING; GENETIC VECTORS; INTRONS; L-LACTATE DEHYDROGENASE; LAC OPERON; METABOLOME; METABOLOMICS; MUTAGENESIS, INSERTIONAL; NUCLEIC ACID CONFORMATION; PHOSPHATE ACETYLTRANSFERASE; PLASMIDS; RNA, BACTERIAL; RNA, CATALYTIC; TEMPERATURE;

CLOSTRIDIUM THERMOCELLUM; ESCHERICHIA COLI; THERMOSYNECHOCOCCUS ELONGATUS;

EID: 84879973036     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069032     Document Type: Article

References (74)

1. Zaldivar J, Nielsen J, Olsson L, (2001) Fuel ethanol production from lignocellulose: a challenge for metabolic engineering and process integration. Appl Microbiol Biotechnol 56: 17-34 doi:10.1007/s002530100624.
2. Hoffert MI, (2010) Climate change. Farewell to fossil fuels? Science 329: 1292-1294 doi:10.1126/science.1195449.
3. Chang T, Yao S, (2011) Thermophilic, lignocellulolytic bacteria for ethanol production: current state and perspectives. Appl Microbiol Biotechnol 92: 13-27 doi:10.1007/s00253-011-3456-3.
4. Payton MA, (1984) Production of ethanol by thermophilic bacteria. Trends Biotechnol 2: 153-158 doi:10.1016/0167-7799(84)90032-5.
5. Lynd LR, Grethlein HE, Wolkin RH, (1989) Fermentation of cellulosic substrates in batch and continuous culture by Clostridium thermocellum. Appl Environ Microbiol 55: 3131-3139.
6. Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS, (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66: 506-577 doi:10.1128/MMBR.66.3.506-577.2002.
7. Lamed R, Setter E, Bayer EA, (1983) Characterization of a cellulose-binding, cellulase-containing complex in Clostridium thermocellum. J Bacteriol 156: 828-836 doi: 10.1128/AEM.70.2.883-890.2004.
8. Lynd LR, van Zyl WH, McBride JE, Laser M, (2005) Consolidated bioprocessing of cellulosic biomass: an update. Curr Opin Biotechnol 16: 577-583 doi:10.1016/j.copbio.2005.08.009.
9. Tyurin MV, Desai SG, Lynd LR, (2004) Electrotransformation of Clostridium thermocellum. Appl Environ Microbiol 70: 883-890 doi: 10.1128/?AEM.70.2.883-890.2004.
10. Zverlov VV, Klupp M, Krauss J, Schwarz WH, (2008) Mutations in the scaffoldin gene, cipA, of Clostridium thermocellum with impaired cellulosome formation and cellulose hydrolysis: insertions of a new transposable element, IS1447, and implications for cellulase synergism on crystalline cellulose. J Bacteriol 190: 4321-4327 doi:10.1128/JB.00097-08.
11. Olson DG, Tripathi SA, Giannone RJ, Lo J, Caiazza NC, et al. (2010) Deletion of the Cel48S cellulase from Clostridium thermocellum. Proc Natl Acad Sci USA 107: 17727-17732 doi:10.1073/pnas.1003584107.
12. Tripathi SA, Olson DG, Argyros DA, Miller BB, Barrett TF, et al. (2010) Development of pyrF-based genetic system for targeted gene deletion in Clostridium thermocellum and creation of a pta mutant. Appl Environ Microbiol 76: 6591-6599 doi:10.1128/AEM.01484-10.
13. Guo H, Karberg M, Long M, Jones JP III, Sullenger B, et al. (2000) Group II introns designed to insert into therapeutically relevant DNA target sites in human cells. Science 289: 452-457 doi:10.1126/science.289.5478.452.
14. Karberg M, Guo H, Zhong J, Coon RG, Perutka J, et al. (2001) Group II introns as controllable gene targeting vectors for genetic manipulation of bacteria. Nat Biotechnol 19: 1162-1167 doi:10.1038/nbt1201-1162.
15. Perutka J, Wang W, Goerlitz D, Lambowitz AM, (2004) Use of computer-designed group II introns to disrupt Escherichia coli DExH/D-box protein and DNA helicase genes. J Mol Biol 336: 421-439 doi:10.1016/j.jmb.2003.12.009.
16. Lambowitz AM, Zimmerly S, (2011) Group II introns: mobile ribozymes that invade DNA. Cold Spring Harb Perspect Biol 3: a003616 doi:10.1101/cshperspect.a003616.
17. Guo H, Zimmerly S, Perlman PS, Lambowitz AM, (1997) Group II intron endonucleases use both RNA and protein subunits for recognition of specific sequences in double-stranded DNA. EMBO J 16: 6835-6848 doi:10.1093/emboj/16.22.6835.
18. Mohr G, Smith D, Belfort M, Lambowitz AM, (2000) Rules for DNA target-site recognition by a lactococcal group II intron enable retargeting of the intron to specific DNA sequences. Genes Dev 14: 559-573 doi:10.1101/gad.14.5.559.
19. Singh NN, Lambowitz AM, (2001) Interaction of a group II intron ribonucleoprotein endonuclease with its DNA target site investigated by DNA footprinting and modification interference. J Mol Biol 309: 361-386 doi:10.1006/jmbi.2001.4658.
20. Eskes R, Yang J, Lambowitz AM, Perlman PS, (1997) Mobility of yeast mitochondrial group II introns: engineering a new site specificity and retrohoming via full reverse splicing. Cell 88: 865-874 doi:10.1016/S0092-8674(00)81932-7.
21. Smith D, Zhong J, Matsuura M, Lambowitz AM, Belfort M, (2005) Recruitment of host functions suggests a repair pathway for late steps in group II intron retrohoming. Genes Dev 19: 2477-2487 doi:10.1101/gad.1345105.
22. Yao J, Truong DM, Lambowitz AM, (2013) Genetic and biochemical assays reveal a key role for replication restart proteins in group II intron retrohoming. PLoS Genet 9: e1003469 doi:10.1371/journal.pgen.1003469.
23. Yao J, Zhong J, Fang Y, Geisinger E, Novick RP, et al. (2006) Use of targetrons to disrupt essential and nonessential genes in Staphylococcus aureus reveals temperature sensitivity of Ll.LtrB group II intron splicing. RNA 12: 1271-1281 doi:10.1261/rna.68706.
24. Yao J, Lambowitz AM, (2007) Gene targeting in gram-negative bacteria by use of a mobile group II intron ("targetron") expressed from a broad-host-range vector. Appl Environ Microbiol 73: 2735-2743 doi:10.1128/AEM.02829-06.
25. Zhuang F, Karberg M, Perutka J, Lambowitz AM, (2009) EcI5, a group IIB intron with high retrohoming frequency: DNA target site recognition and use in gene targeting. RNA 15: 432-449 doi:10.1261/rna.1378909.
26. García-Rodríguez FM, Barrientos-Durán A, Díaz-Prado V, Fernández-López M, Toro N, (2011) Use of RmInt1, a group IIB intron lacking the intron-encoded protein endonuclease domain, in gene targeting. Appl Environ Microbiol 77: 854-861 doi:10.1128/AEM.02319-10.
27. Frazier CL, San Filippo J, Lambowitz AM, Mills DA, (2003) Genetic manipulation of Lactococcus lactis by using targeted group II introns: generation of stable insertions without selection. Appl Environ Microbiol 69: 1121-1128 doi:10.1128/AEM.69.2.1121-1128.2003.
28. Zhong J, Karberg M, Lambowitz AM, (2003) Targeted and random bacterial gene disruption using a group II intron (targetron) vector containing a retrotransposition-activated selectable marker. Nucleic Acids Res 31: 1656-1664 doi:10.1093/nar/gkg248.
29. Heap JT, Pennington OJ, Cartman ST, Carter GP, Minton NP, (2007) The ClosTron: a universal gene knock-out system for the genus Clostridium. J Microbiol Methods 70: 452-464 doi:10.1016/j.mimet.2007.05.021.
30. Qin PZ, Pyle AM, (1999) Antagonistic substrate binding by a group II intron ribozyme. J Mol Biol 291: 15-27 doi:10.1006/jmbi.1999.2922.
31. Chen Y, McClane BA, Fisher DJ, Rood JI, Gupta P, (2005) Construction of an alpha toxin gene knockout mutant of Clostridium perfringens type A by use of a mobile group II intron. Appl Environ Microbiol 71: 7542-7547 doi:10.1128/AEM.71.11.7542-7547.2005.
32. Corvaglia AR, François P, Hernandez D, Perron K, Linder P, et al. (2010) A type III-like restriction endonuclease functions as a major barrier to horizontal gene transfer in clinical Staphylococcus aureus strains. Proc Natl Acad Sci USA 107: 11954-11958 doi:10.1073/pnas.1000489107.
33. Upadhyay A, Srivastava S, (2011) Phenazine-1-carboxylic acid is a more important contributor to biocontrol Fusarium oxysporum than pyrrolnitrin in Pseudomonas fluorescens strain Psd. Microbiol Res 166: 323-335 doi:10.1016/j.micres.2010.06.001.
34. Malhotra M, Srivastava S, (2008) An ipdC gene knock-out of Azospirillum brasilense strain SM and its implications on indole-3-acetic acid biosynthesis and plant growth promotion. Antonie Van Leeuwenhoek 93: 425-433 doi:10.1007/s10482-007-9207-x.
35. Rodriguez SA, Yu J-J, Davis G, Arulanandam BP, Klose KE, (2008) Targeted inactivation of Francisella tularensis genes by group II introns. Appl Environ Microbiol 74: 2619-2626 doi:10.1128/AEM.02905-07.
36. Alonzo F, Port GC, Cao M, Freitag NE, (2009) The posttranslocation chaperone PrsA2 contributes to multiple facets of Listeria monocytogenes pathogenesis. Infect Immun 77: 2612-2623 doi:10.1128/IAI.00280-09.
37. Zarschler K, Janesch B, Zayni S, Schäffer C, Messner P, (2009) Construction of a gene knockout system for application in Paenibacillus alvei CCM 2051T, exemplified by the S-layer glycan biosynthesis initiation enzyme WsfP. Appl Environ Microbiol 75: 3077-3085 doi:10.1128/AEM.00087-09.
38. Steen JA, Steen JA, Harrison P, Seemann T, Wilkie I, et al. (2010) Fis is essential for capsule production in Pasteurella multocida and regulates expression of other important virulence factors. PLoS Pathog 6: e1000750 doi:10.1371/journal.ppat.1000750.
39. Park JM, Jang Y-S, Kim TY, Lee SY, (2010) Development of a gene knockout system for Ralstonia eutropha H16 based on the broad-host-range vector expressing a mobile group II intron. FEMS Microbiol Rev 309: 193-200 doi:10.1111/j.1574-6968.2010.02041.x.
40. King NP, Beatson SA, Totsika M, Ulett GC, Alm RA, et al. (2011) UafB is a serine-rich repeat adhesin of Staphylococcus saprophyticus that mediates binding to fibronectin, fibrinogen and human uroepithelial cells. Microbiology 157: 1161-1175 doi:10.1099/mic.0.047639-0.
41. Palonen E, Lindström M, Karttunen R, Somervuo P, Korkeala H, (2011) Expression of signal transduction system encoding genes of Yersinia pseudotuberculosis IP32953 at 28°C and 3°C. PLoS ONE 6: e25063 doi:10.1371/journal.pone.0025063.
42. Palonen E, Lindström M, Somervuo P, Johansson P, Björkroth J, et al. (2012) Requirement for RNA helicase CsdA for growth of Yersinia pseudotuberculosis IP32953 at low temperatures. Appl Environ Microbiol 78: 1298-1301 doi:10.1128/AEM.07278-11.
43. Maltz MA, Weiss BL, O'Neill M, Wu Y, Aksoy S, (2012) OmpA-mediated biofilm formation is essential for the commensal bacterium Sodalis glossinidius to colonize the tsetse fly gut. Appl Environ Microbiol 78: 7760-7768 doi:10.1128/AEM.01858-12.
44. Akhtar P, Khan SA, (2012) Two independent replicons can support replication of the anthrax toxin-encoding plasmid pXO1 of Bacillus anthracis. Plasmid 67: 111-117 doi:10.1016/j.plasmid.2011.12.012.
45. Rawsthorne H, Turner KN, Mills DA, (2006) Multicopy integration of heterologous genes, using the lactococcal group II intron targeted to bacterial insertion sequences. Appl Environ Microbiol 72: 6088-6093 doi:10.1128/AEM.02992-05.
46. Zoraghi R, See RH, Gong H, Lian T, Swayze R, et al. (2010) Functional analysis, overexpression, and kinetic characterization of pyruvate kinase from methicillin-resistant Staphylococcus aureus. Biochemistry 49: 7733-7747 doi:10.1021/bi100780t.
47. Carter GP, Awad MM, Hao Y, Thelen T, Bergin IL, et al. (2011) TcsL is an essential virulence factor in Clostridium sordellii ATCC 9714. Infect Immun 79: 1025-1032 doi:10.1128/IAI.00968-10.
48. Jiang Y, Xu C, Dong F, Yang Y, Jiang W, et al. (2009) Disruption of the acetoacetate decarboxylase gene in solvent-producing Clostridium acetobutylicum increases the butanol ratio. Metab Eng 11: 284-291 doi:10.1016/j.ymben.2009.06.002.
49. Jang Y-S, Lee JY, Lee J, Park JH, Im JA, et al. (2012) Enhanced butanol production obtained by reinforcing the direct butanol-forming route in Clostridium acetobutylicum. MBio 3: e00314-12 doi:10.1128/mBio.00314-12.
50. Li Y, Tschaplinski TJ, Engle NL, Hamilton CY, Rodriguez M, et al. (2012) Combined inactivation of the Clostridium cellulolyticum lactate and malate dehydrogenase genes substantially increases ethanol yield from cellulose and switchgrass fermentations. Biotechnol Biofuels 5: 2 doi:10.1186/1754-6834-5-2.
51. Nakamura Y, Kaneko T, Sato S, Ikeuchi M, Katoh H, et al. (2002) Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res 9: 123-130 doi:10.1093/dnares/9.4.123.
52. Ueda K, Yamashita A, Ishikawa J, Shimada M, Watsuji T-O, et al. (2004) Genome sequence of Symbiobacterium thermophilum, an uncultivable bacterium that depends on microbial commensalism. Nucleic Acids Res 32: 4937-4944 doi:10.1093/nar/gkh830.
53. Vellore J, Moretz SE, Lampson BC, (2004) A group II intron-type open reading frame from the thermophile Bacillus (Geobacillus) stearothermophilus encodes a heat-stable reverse transcriptase. Appl Environ Microbiol 70: 7140-7147 doi:10.1128/AEM.70.12.7140-7147.2004.
54. Tourasse NJ, Kolstø A-B, (2008) Survey of group I and group II introns in 29 sequenced genomes of the Bacillus cereus group: insights into their spread and evolution. Nucleic Acids Res 36: 4529-4548 doi:10.1093/nar/gkn372.
55. Mohr G, Ghanem E, Lambowitz AM, (2010) Mechanisms used for genomic proliferation by thermophilic group II introns. PLoS Biol 8: e1000391 doi:10.1371/journal.pbio.1000391.
56. McBee RH, (1954) The characteristics of Clostridium thermocellum. J Bacteriol 67: 505-506.
57. Freier D, Mothershed CP, Wiegel J, (1988) Characterization of Clostridium thermocellum JW20. Appl Environ Microbiol 54: 204-211.
58. Ciruela A, Cross S, Freedman RB, Hazlewood GP, (1997) Sequence and transcriptional analysis of groES and groEL genes from the thermophilic bacterium Clostridium thermocellum. Gene 186: 143-147 doi:10.1016/S0378-1119(96)00814-1.
59. Argyros DA, Tripathi SA, Barrett TF, Rogers SR, Feinberg LF, et al. (2011) High ethanol titers from cellulose by using metabolically engineered thermophilic, anaerobic microbes. Appl Environ Microbiol 77: 8288-8294 doi:10.1128/AEM.00646-11.
60. Berger E, Crampton MC, Nxumalo NP, Louw ME, (2011) Extracellular secretion of a recombinant therapeutic peptide by Bacillus halodurans utilizing a modified flagellin type III secretion system. Microb Cell Fact 10: 62 doi:10.1186/1475-2859-10-62.
61. Frey M, (2002) Hydrogenases: hydrogen-activating enzymes. Chembiochem 3: 153-160.
62. Plante I, Cousineau B, (2006) Restriction for gene insertion within the Lactococcus lactis Ll.LtrB group II intron. RNA 12: 1980-1992 doi:10.1261/rna.193306.
63. Yamaoka T, Satoh K, Katoh S, (1978) Photosynthetic activities of a thermophilic blue-green alga. Plant Cell Physiol 19: 943-954.
64. Mohr S, Ghanem E, Smith W, Sheeter D, Qin Y, et al. (2013) Thermostable group II intron reverse transcriptase fusion proteins and their use in cDNA synthesis and next-generation RNA sequencing. RNA, in press. doi:10.1261/rna.039743.113.
65. Haki GD, Rakshit SK, (2003) Developments in industrially important thermostable enzymes: a review. Bioresour Technol 89: 17-34 doi:10.1016/S0960-8524(03)00033-6.
66. Turner P, Mamo G, Karlsson EN, (2007) Potential and utilization of thermophiles and thermostable enzymes in biorefining. Microb Cell Fact 6: 9 doi:10.1186/1475-2859-6-9.
67. Mai V, Lorenz W, Wiegel J, (1997) Transformation of Thermoanaerobacterium sp. strain JW/SL-YS485 with plasmid pIKM1 conferring kanamycin resistance. FEMS Microbiol Rev 148: 163-167 doi:10.1111/j.1574-6968.1997.tb10283.x.
68. Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR, (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61-68 doi:10.1016/0378-1119(89)90359-4.
69. Ausubel FM, Brent R, Kingston R, Moore DD, Seidman JG, et al. (2002) Short protocols in molecular biology. 5th ed. Hoboken, NJ: John Wiley & Sons, Inc.
70. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
71. Cui Q, Lewis IA, Hegeman AD, Anderson ME, Li J, et al. (2008) Metabolite identification via the Madison Metabolomics Consortium Database. Nat Biotechnol 26: 162-164 doi:10.1038/nbt0208-162.
72. Malik HS, Burke WD, Eickbush TH, (1999) The age and evolution of non-LTR retrotransposable elements. Mol Biol Evol 16: 793-805.
73. Blocker FJH, Mohr G, Conlan LH, Qi L, Belfort M, et al. (2005) Domain structure and three-dimensional model of a group II intron-encoded reverse transcriptase. RNA 11: 14-28 doi:10.1261/rna.7181105.
74. Crooks GE, Hon G, Chandonia J-M, Brenner SE, (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190 doi:10.1101/gr.849004.