The contribution of cellulosomal scaffoldins to cellulose hydrolysis by Clostridium thermocellum analyzed by using thermotargetrons

Biotechnology for Biofuels

Volumn 7, Issue 1, 2014, Pages

  Hong, Wei ^a,b   Zhang, Jie ^a,b   Feng, Yingang ^a   Mohr, Georg ^c   Lambowitz, Alan M ^c   Cui, Gu Zhen ^a   Liu, Ya Jun ^a   Cui, Qiu ^a  

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

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Biofuels; Cellulosic ethanol; Cellulosome cell synergy; Consolidated bioprocessing; Thermophile

Indexed keywords

BIOFUELS; CELL MEMBRANES; CELLULOSE; CELLULOSIC ETHANOL; CLOSTRIDIUM; CYTOLOGY; GENETIC ENGINEERING; HYDROLYSIS; SUBSTRATES;

CARBOHYDRATE BINDING MODULES; CELLULOSE DEGRADATION; CELLULOSOME-CELL SYNERGY; CLOSTRIDIUM THERMOCELLUM; CONSOLIDATED BIO-PROCESSING; MACROMOLECULAR COMPLEXES; THERMOPHILE; THERMOPHILIC ANAEROBIC BACTERIA;

MOLECULAR BIOLOGY;

BIODEGRADATION; BIOFUEL; CELLULOSE; ETHANOL; GENETIC ENGINEERING; HYDROLYSIS; THERMOPHILIC BACTERIUM;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM THERMOCELLUM;

EID: 84902131944     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/1754-6834-7-80     Document Type: Article

References (63)

1. Cellulosomes-structure and ultrastructure. Bayer EA, Shimon LJ, Shoham Y, Lamed R, J Struct Biol 1998 124 221 234 10.1006/jsbi.1998.4065 10049808
2. Cellulase, clostridia, and ethanol. Demain AL, Newcomb M, Wu JH, Microbiol Mol Biol Rev 2005 69 124 154 10.1128/MMBR.69.1.124-154.2005 15755956
3. From cellulosomes to cellulosomics. Bayer EA, Lamed R, White BA, Flint HJ, Chem Rec 2008 8 364 377 10.1002/tcr.20160 19107866
4. High ethanol titers from cellulose using metabolically engineered thermophilic, anaerobic microbes. Argyros DA, Tripathi SA, Barrett TF, Rogers SR, Feinberg LF, Olson DG, Foden JM, Miller BB, Lynd LR, Hogsett DA, Caiazza NC, Appl Environ Microbiol 2011 77 8288 8294 10.1128/AEM.00646-11 21965408
5. The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Bayer EA, Belaich JP, Shoham Y, Lamed R, Annu Rev Microbiol 2004 58 521 554 10.1146/annurev.micro.57.030502.091022 15487947
6. Functional subgenomics of Clostridium thermocellum cellulosomal genes: identification of the major catalytic components in the extracellular complex and detection of three new enzymes. Zverlov VV, Kellermann J, Schwarz WH, Proteomics 2005 5 3646 3653 10.1002/pmic.200401199 16127726
7. Separation and characterization of the complexes constituting the cellulolytic enzyme system of Clostridium thermocellum. Hon-nami K, Coughlan M, Hon-nami H, Ljungdahl L, Arch Microbiol 1986 145 13 19 10.1007/BF00413021
8. Global gene expression patterns in Clostridium thermocellum as determined by microarray analysis of chemostat cultures on cellulose or cellobiose. Riederer A, Takasuka TE, Makino S, Stevenson DM, Bukhman YV, Elsen NL, Fox BG, Appl Environ Microbiol 2011 77 1243 1253 10.1128/AEM.02008-10 21169455
9. Characterization of a cellulose-binding, cellulase-containing complex in Clostridium thermocellum. Lamed R, Setter E, Bayer EA, J Bacteriol 1983 156 828 836 6195146
10. The cellulosome of Clostridium thermocellum. Beguin P, Alzari PM, Biochem Soc Trans 1998 26 178 185 9649744
11. Complete genome sequence of the cellulolytic thermophile Clostridium thermocellum DSM1313. Feinberg L, Foden J, Barrett T, Davenport KW, Bruce D, Detter C, Tapia R, Han C, Lapidus A, Lucas S, Cheng JF, Pitluck S, Woyke T, Ivanova N, Mikhailova N, Land M, Hauser L, Argyros DA, Goodwin L, Hogsett D, Caiazza N, J Bacteriol 2011 193 2906 2907 10.1128/JB.00322-11 21460082
12. Interaction of the duplicated segment carried by Clostridium thermocellum cellulases with cellulosome components. Tokatlidis K, Salamitou S, Beguin P, Dhurjati P, Aubert JP, FEBS Lett 1991 291 185 188 10.1016/0014-5793(91)81279-H 1936262
13. Cellulase-xylanase synergy in designer cellulosomes for enhanced degradation of a complex cellulosic substrate. Morais S, Barak Y, Caspi J, Hadar Y, Lamed R, Shoham Y, Wilson DB, Bayer EA, mBio 2010 1 00285 21157512
14. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ, Biochem J 2004 382 769 781 10.1042/BJ20040892 15214846
15. Enzyme-microbe synergy during cellulose hydrolysis by Clostridium thermocellum. Lu Y, Zhang YH, Lynd LR, Proc Natl Acad Sci U S A 2006 103 16165 16169 10.1073/pnas.0605381103 17060624
16. 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. Zverlov VV, Klupp M, Krauss J, Schwarz WH, J Bacteriol 2008 190 4321 4327 10.1128/JB.00097-08 18408027
17. Role of the CipA scaffoldin protein in cellulose solubilization, as determined by targeted gene deletion and complementation in Clostridium thermocellum. Olson DG, Giannone RJ, Hettich RL, Lynd LR, J Bacteriol 2013 195 733 739 10.1128/JB.02014-12 23204466
18. Exchange of type II dockerin-containing subunits of the Clostridium thermocellum cellulosome as revealed by SNAP-tags. Waller BH, Olson DG, Currie DH, Guss AM, Lynd LR, FEMS Microbiol Lett 2013 338 46 53 10.1111/1574-6968.12029 23082914
19. Group II introns designed to insert into therapeutically relevant DNA target sites in human cells. Guo H, Karberg M, Long M, Jones JP III, Sullenger B, Lambowitz AM, Science 2000 289 452 457 10.1126/science.289.5478.452 10903206
20. Group II introns as controllable gene targeting vectors for genetic manipulation of bacteria. Karberg M, Guo H, Zhong J, Coon R, Perutka J, Lambowitz AM, Nat Biotech 2001 19 1162 1167 10.1038/nbt1201-1162
21. Use of computer-designed group II introns to disrupt Escherichia coli DExH/D-box protein and DNA helicase genes. Perutka J, Wang W, Goerlitz D, Lambowitz AM, J Mol Biol 2004 336 421 439 10.1016/j.jmb.2003.12.009 14757055
22. Construction of an alpha toxin gene knockout mutant of Clostridium perfringens type A by use of a mobile group II intron. Chen Y, McClane BA, Fisher DJ, Rood JI, Gupta P, Appl Environ Microbiol 2005 71 7542 7547 10.1128/AEM.71.11.7542-7547.2005 16269799
23. Biotechnological applications of mobile group II introns and their reverse transcriptases: gene targeting, RNA-seq, and non-coding RNA analysis. Enyeart PJ, Mohr G, Ellington AD, Lambowitz AM, Mob DNA 2014 5 2 10.1186/1759-8753-5-2 24410776
24. The ClosTron: mutagenesis in Clostridium refined and streamlined. Heap JT, Kuehne SA, Ehsaan M, Cartman ST, Cooksley CM, Scott JC, Minton NP, J Microbiol Methods 2010 80 49 55 10.1016/j.mimet.2009.10.018 19891996
25. A targetron system for gene targeting in thermophiles and its application in Clostridium thermocellum. Mohr G, Hong W, Zhang J, Cui G-Z, Yang Y, Cui Q, Liu Y-J, Lambowitz AM, PLoS One 2013 8 69032 10.1371/journal.pone.0069032 23874856
26. Mechanisms used for genomic proliferation by thermophilic group II introns. Mohr G, Ghanem E, Lambowitz AM, PLoS Biol 2010 8 1000391 10.1371/journal.pbio.1000391 20543989
27. Global view of the Clostridium thermocellum cellulosome revealed by quantitative proteomic analysis. Gold ND, Martin VJ, J Bacteriol 2007 189 6787 6795 10.1128/JB.00882-07 17644599
28. Affinity digestion for the near-total recovery of purified cellulosome from Clostridium thermocellum. Morag E, Bayer EA, Lamed R, Enzyme Microb Technol 1992 14 289 292 10.1016/0141-0229(92)90153-F
29. Development of a multi-point quantitation method to simultaneously measure enzymatic and structural components of the Clostridium thermocellum cellulosome protein complex. Dykstra AB, Brice LS, Rodriguez M, Raman B, Izquierdo J, Cook KD, Lynd LR, Hettich RL, J Proteome Res 2013 13 692 701 24274857
30. Impact of pretreated Switchgrass and biomass carbohydrates on Clostridium thermocellum ATCC 27405 cellulosome composition: a quantitative proteomic analysis. Raman B, Pan C, Hurst GB, Rodriguez M Jr, McKeown CK, Lankford PK, Samatova NF, Mielenz JR, PLoS One 2009 4 5271 10.1371/journal.pone.0005271 19384422
31. Determination of structural carbohydrates and lignin in biomass. Sluiter A, Hames B, Ruiz R, Scarlata C, Sluiter J, Templeton D, Crocker D, NREL Lab Anal Proced 2008 http://www.nrel.gov/docs/gen/fy13/42618.pdf
32. A flexible growth function for empirical use. Richards FJ, J Exp Bot 1959 10 290 300 10.1093/jxb/10.2.290
33. Cellulosomes: highly efficient nanomachines designed to deconstruct plant cell wall complex carbohydrates. Fontes CM, Gilbert HJ, Annu Rev Biochem 2010 79 655 681 10.1146/annurev-biochem-091208-085603 20373916
34. Organization and distribution of the cellulosome in Clostridium thermocellum. Bayer EA, Setter E, Lamed R, J Bacteriol 1985 163 552 559 4019409
35. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Miller GL, Anal Chem 1959 31 426 428 10.1021/ac60147a030
36. Contribution of a xylan-binding module to the degradation of a complex cellulosic substrate by designer cellulosomes. Morais S, Barak Y, Caspi J, Hadar Y, Lamed R, Shoham Y, Wilson DB, Bayer EA, Appl Environ Microbiol 2010 76 3787 3796 10.1128/AEM.00266-10 20400556
37. Characterization and affinity applications of cellulose-binding domains. Tomme P, Boraston A, McLean B, Kormos J, Creagh AL, Sturch K, Gilkes NR, Haynes CA, Warren RA, Kilburn DG, J Chromatogr B 1998 715 283 296 10.1016/S0378- 4347(98)00053-X
38. A synthetic biology approach for evaluating the functional contribution of designer cellulosome components to deconstruction of cellulosic substrates. Vazana Y, Barak Y, Unger T, Peleg Y, Shamshoum M, Ben-Yehezkel T, Mazor Y, Shapiro E, Lamed R, Bayer EA, Biotechnol Biofuels 2013 6 182 10.1186/1754-6834-6-182 24341331
39. Insights into cellulosome assembly and dynamics: from dissection to reconstruction of the supramolecular enzyme complex. Smith SP, Bayer EA, Curr Opin Struct Biol 2013 23 686 694 10.1016/j.sbi.2013.09.002 24080387
40. Novel Clostridium thermocellum type I cohesin-dockerin complexes reveal a single binding mode. Bras JL, Alves VD, Carvalho AL, Najmudin S, Prates JA, Ferreira LM, Bolam DN, Romao MJ, Gilbert HJ, Fontes CM, J Biol Chem 2012 287 44394 44405 10.1074/jbc.M112.407700 23118225
41. A new type of cohesin domain that specifically binds the dockerin domain of the Clostridium thermocellum cellulosome-integrating protein CipA. Leibovitz E, Beguin P, J Bacteriol 1996 178 3077 3084 8655483
42. Mechanism of bacterial cell-surface attachment revealed by the structure of cellulosomal type II cohesin-dockerin complex. Adams JJ, Pal G, Jia Z, Smith SP, Proc Natl Acad Sci U S A 2006 103 305 310 10.1073/pnas.0507109103 16384918
43. Cellulose utilization by Clostridium thermocellum: bioenergetics and hydrolysis product assimilation. Zhang YH, Lynd LR, Proc Natl Acad Sci U S A 2005 102 7321 7325 10.1073/pnas.0408734102 15883376
44. Adherence of Clostridium thermocellum to cellulose. Bayer EA, Kenig R, Lamed R, J Bacteriol 1983 156 818 6630152
45. Specialized cell surface structures in cellulolytic bacteria. Lamed R, Naimark J, Morgenstern E, Bayer E, J Bacteriol 1987 169 3792 3800 3301817
46. Functional insights into the role of novel type I cohesin and dockerin domains from Clostridium thermocellum. Pinheiro BA, Gilbert HJ, Sakka K, Sakka K, Fernandes VO, Prates JA, Alves VD, Bolam DN, Ferreira LM, Fontes CM, Biochem J 2009 424 375 384 10.1042/BJ20091152 19758121
47. Clostridium thermocellum cellulosomal genes are regulated by extracytoplasmic polysaccharides via alternative sigma factors. Nataf Y, Bahari L, Kahel-Raifer H, Borovok I, Lamed R, Bayer EA, Sonenshein AL, Shoham Y, Proc Natl Acad Sci U S A 2010 107 18646 18651 10.1073/pnas.1012175107 20937888
48. Are cellulosome scaffolding protein CipC and CBM3-containing protein HycP, involved in adherence of Clostridium cellulolyticum to cellulose? Chaves-Olarte E, Ferdinand P-H, Borne R, Trotter V, Pagès S, Tardif C, Fierobe H-P, Perret S, PLoS One 2013 8 69360 10.1371/journal.pone.0069360 23935995
49. Development of pyrF-based genetic system for targeted gene deletion in Clostridium thermocellum and creation of a pta mutant. Tripathi SA, Olson DG, Argyros DA, Miller BB, Barrett TF, Murphy DM, McCool JD, Warner AK, Rajgarhia VB, Lynd LR, Hogsett DA, Caiazza NC, Appl Environ Microbiol 2010 76 6591 6599 10.1128/AEM.01484-10 20693441
50. Deletion of the Cel48S cellulase from Clostridium thermocellum. Olson DG, Tripathi SA, Giannone RJ, Lo J, Caiazza NC, Hogsett DA, Hettich RL, Guss AM, Dubrovsky G, Lynd LR, Proc Natl Acad Sci U S A 2010 107 17727 17732 10.1073/pnas.1003584107 20837514
51. Genetic manipulation of Lactococcus lactis by using targeted group II introns: generation of stable insertions without selection. Frazier CL, San Filippo J, Lambowitz AM, Mills DA, Appl Environ Microbiol 2003 69 1121 1128 10.1128/AEM.69.2.1121-1128.2003 12571038
52. Generalized bacterial genome editing using mobile group II introns and Cre-lox. Enyeart PJ, Chirieleison SM, Dao MN, Perutka J, Quandt EM, Yao J, Whitt JT, Keatinge-Clay AT, Lambowitz AM, Ellington AD, Mol Syst Biol 2013 9 685 24002656
53. Deconstruction of lignocellulose into soluble sugars by native and designer cellulosomes. Morais S, Morag E, Barak Y, Goldman D, Hadar Y, Lamed R, Shoham Y, Wilson DB, Bayer EA, mBio 2012 3 00508 e00512 23232718
54. Targeted gene engineering in Clostridium cellulolyticum H10 without methylation. Cui GZ, Hong W, Zhang J, Li WL, Feng Y, Liu YJ, Cui Q, J Microbiol Methods 2012 89 201 208 10.1016/j.mimet.2012.02.015 22450138
55. Dcm methylation is detrimental to plasmid transformation in Clostridium thermocellum. Guss AM, Olson DG, Caiazza NC, Lynd LR, Biotechnol Biofuels 2012 5 30 10.1186/1754-6834-5-30 22559230
56. Clostridium perfringens enterotoxin carboxy-terminal fragment is a novel tumor-homing peptide for human ovarian cancer. Cocco E, Casagrande F, Bellone S, Richter CE, Bellone M, Todeschini P, Holmberg JC, Fu HH, Montagna MK, Mor G, Schwartz PE, Arin-Silasi D, Azoudi M, Rutherford TJ, Abu-Khalaf M, Pecorelli S, Santin AD, BMC Cancer 2010 10 349 10.1186/1471-2407-10-349 20598131
57. Corynebacterium glutamicum contains 3-deoxy-D-arabino-heptulosonate 7-phosphate synthases that display novel biochemical features. Liu YJ, Li PP, Zhao KX, Wang BJ, Jiang CY, Drake HL, Liu SJ, Appl Environ Microbiol 2008 74 5497 5503 10.1128/AEM.00262-08 18621870
58. Harlow E, Lane D, Using Antibodies: A Laboratory Manual New York: Cold Spring Harbor Laboratory Press 1999
59. Proteomics approach to study the mechanism of action of grape seed proanthocyanidin extracts on arterial remodeling in diabetic rats. Li X-L, Li B-Y, Gao H-Q, Cheng M, Xu L, Li X-H, Zhang W-D, Hu J-W, Int J Mol Med 2010 25 237 20043133
60. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Bradford MM, Anal Biochem 1976 72 248 254 10.1016/0003-2697(76)90527-3 942051
61. Fermentation of cellulosic substrates in batch and continuous culture by Clostridium thermocellum. Lynd LR, Grethlein HE, Wolkin RH, Appl Environ Microb 1989 55 3131 3139
62. Improving activity of minicellulosomes by integration of intra-and intermolecular synergies. Xu Q, Ding S-Y, Brunecky R, Bomble YJ, Himmel ME, Baker JO, Biotechnol Biofuels 2013 6 126 10.1186/1754-6834-6-126 23987588
63. Multilayer adhesion to filter paper of two mesophilic, cellulolytic clostridia. Gelhaye E, Claude B, Cailliez C, Burle S, Petitdemange H, Curr Microbiol 1992 25 307 311 10.1007/BF01577226