Cofactor specificity of the bifunctional alcohol and aldehyde dehydrogenase (AdhE) in wild-type and mutant Clostridium thermocellum and thermoanaerobacterium saccharolyticum

Journal of Bacteriology

Volumn 197, Issue 15, 2015, Pages 2610-2619

  Zheng, Tianyong ^a,f   Olson, Daniel G ^b,f   Tian, Liang ^b,f   Bomble, Yannick J ^c,f   Himmel, Michael E ^c,f   Lo, Jonathan ^a,f   Hon, Shuen ^b,f   Joe Shaw, A ^d   Van Dijken, Johannes P ^e   Lynd, Lee R ^a,b,f  

^a Dartmouth College   (United States)

^b DARTMOUTH COLLEGE   (United States)

^c NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

^d Novogy Inc   (United States)

^e DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^f BioEnergy Science Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; ALCOHOL DEHYDROGENASE; ALDEHYDE DEHYDROGENASE; BACTERIAL ENZYME; CELLOBIOSE; CELLULOSE; HEMICELLULOSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; BACTERIAL PROTEIN; COENZYME;

AFFINITY CHROMATOGRAPHY; ALCOHOL PRODUCTION; ARTICLE; BACTERIAL GENE; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIUM MUTANT; BIOENGINEERING; CATALYTIC EFFICIENCY; CLOSTRIDIUM THERMOCELLUM; CONTROLLED STUDY; DENSITOMETRY; DNA MODIFICATION; ENZYME ACTIVITY; ESCHERICHIA COLI; FERMENTATION; KINETIC PARAMETERS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; THERMOANAEROBACTERIUM; THERMOANAEROBACTERIUM SACCHAROLYTICUM; WILD TYPE; AMINO ACID SEQUENCE; COENZYME; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY;

CLOSTRIDIUM THERMOCELLUM; ESCHERICHIA COLI; THERMOANAEROBACTERIUM SACCHAROLYTICUM;

ALCOHOL DEHYDROGENASE; ALDEHYDE DEHYDROGENASE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CLOSTRIDIUM THERMOCELLUM; COENZYMES; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MOLECULAR SEQUENCE DATA; THERMOANAEROBACTERIUM;

EID: 84936991306     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00232-15     Document Type: Article

References (51)

1. Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS. 2002. Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506 -577. http://dx.doi.org/10.1128/MMBR.66.3.506-577.2002.
2. Blumer-Schuette SE, Brown SD, Sander KB, Bayer EA, Kataeva I, Zurawski JV, Conway JM, Adams MWW, Kelly RM. 2014. Thermophilic lignocellulose deconstruction. FEMS Microbiol Rev 38:393-448. http://dx.doi.org/10.1111/1574-6976.12044.
3. Mai V, Lorenz WW, Wiegel J. 1997. Transformation of Thermoanaerobacterium sp. strain JW/SL-YS485 with plasmid pIKM1 conferring kanamycin resistance. FEMS Microbiol Lett 148:163-167. http://dx.doi.org/10.1111/j.1574-6968.1997.tb10283.x.
4. Shaw AJ, Covalla SF, Miller BB, Firliet BT, Hogsett DA, Herring CD. 2012. Urease expression in a Thermoanaerobacterium saccharolyticum ethanologen allows high titer ethanol production. Metab Eng 14:528-532. http://dx.doi.org/10.1016/j.ymben.2012.06.004.
5. Shao XJ, Raman B, Zhu MJ, Mielenz JR, Brown SD, Guss AM, Lynd LR. 2011. Mutant selection and phenotypic and genetic characterization of ethanol-tolerant strains of Clostridium thermocellum. Appl Microbiol Biotechnol 92:641-652. http://dx.doi.org/10.1007/s00253-011-3492-z.
6. Williams TI, Combs JC, Lynn BC, Strobel HJ. 2007. Proteomic profile changes in membranes of ethanol-tolerant Clostridium thermocellum. Appl Microbiol Biotechnol 74:422-432. http://dx.doi.org/10.1007/s00253-006-0689-7.
7. Rani KS, Swamy M, Sunitha D, Haritha D, Seenayya G. 1996. Improved ethanol tolerance and production in strains of Clostridium thermocellum. World J Microbiol Biotechnol 12:57-60.
8. Sato K, Tomita M, Yonermura S, Goto S, Sekine K, Okuma E, Takagi Y, Hon-nami K, Saiki T. 1993. Characterization of and ethanol hyper production by Clostridium thermocellum I-1-B. Biosci Biotechnol Biochem 57:2116-2121.
9. Argyros DA, Tripathi SA, Barrett TF, Rogers SR, Feinberg LF, Olson DG, Foden JM, Miller BB, Lynd LR, Hogsett DA, Caiazza NC. 2011. High ethanol titers from cellulose by using metabolically engineered thermophilic, anaerobic microbes. Appl Environ Microbiol 77:8288-8294. http://dx.doi.org/10.1128/AEM.00646-11.
10. Shaw AJ, Podkaminer KK, Desai SG, Bardsley JS, Rogers SR, Thorne PG, Hogsett DA, Lynd LR. 2008. Metabolic engineering of a thermophilic bacterium to produce ethanol at high yield. Proc Natl Acad Sci U S A 105:13769 -13774. http://dx.doi.org/10.1073/pnas.0801266105.
11. König S. 1998. Subunit structure, function and organisation of pyruvate decarboxylases from various organisms. Biochim Biophys Acta 1385:271-286. http://dx.doi.org/10.1016/S0167-4838(98)00074-0.
12. Extance J, Crennell SJ, Eley K, Cripps R, Hough DW, Danson MJ. 2013. Structure of a bifunctional alcohol dehydrogenase involved in bioethanol generation in Geobacillus thermoglucosidasius. Acta Crystallogr Sect D Biol Crystallogr 69(Pt 10):2104-2115. http://dx.doi.org/10.1107/S0907444913020349.
13. Membrillo-Hernandez J, Echave P, Cabiscol E, Tamarit J, Ros J, Lin ECC. 2000. Evolution of the adhE gene product of Escherichia coli from a functional reductase to a dehydrogenase. J Biol Chem 275:33869-33875. http://dx.doi.org/10.1074/jbc.M005464200.
14. Yao S. 2008. PhD thesis. Technical University of Denmark, Kongens Lyngby, Denmark.
15. Peng H, Wu G, Shao W. 2008. The aldehyde/alcohol dehydrogenase (AdhE) in relation to the ethanol formation in Thermoanaerobacter ethanolicus JW200. Anaerobe 14:125-127. http://dx.doi.org/10.1016/j .anaerobe.2007.09.004.
16. Bhandiwad A, Shaw AJ, Guss A, Guseva A, Bahl H, Lynd LR. 2014. Metabolic engineering of Thermoanaerobacterium saccharolyticum for n-butanol production. Metab Eng 21:17-25. http://dx.doi.org/10.1016/j .ymben.2013.10.012.
17. Pineda E, Encalada R, Olivos-García A, Néquiz M, Moreno-Sánchez R, Saavedra E. 2013. The bifunctional aldehyde-alcohol dehydrogenase controls ethanol and acetate production in Entamoeba histolytica under aerobic conditions. FEBS Lett 587:178-184. http://dx.doi.org/10.1016/j.febslet.2012.11.020.
18. Boxma B, Voncken F, Jannink S, van Alen T, Akhmanova A, van Weelden SWH, van Hellemond JJ, Ricard G, Huynen M, Tielens AGM, Hackstein JHP. 2004. The anaerobic chytridiomycete fungus Piromyces sp. E2 produces ethanol via pyruvate:formate lyase and an alcohol dehydrogenase E. Mol Microbiol 51:1389-1399. http://dx.doi.org/10.1046/j .1365-2958.2003.03912.x.
19. Atteia A, van Lis R, Mendoza-Hernández G, Henze K, Martin W, Riveros-Rosas H, González-Halphen D. 2003. Bifunctional aldehyde/alcohol dehydrogenase (ADHE) in chlorophyte algal mitochondria. Plant Mol Biol 53:175-188. http://dx.doi.org/10.1023/B:PLAN.0000009274.19340.36.
20. Lo J, Zheng T, Hon S, Olson DG, Lynd LR. 2015. The bifunctional alcohol and aldehyde dehydrogenase gene, adhE, is necessary for ethanol production in Clostridium thermocellum and Thermoanaerobacterium saccharolyticum. J Bacteriol 197:1386-1393. http://dx.doi.org/10.1128/JB.02450-14.
21. Brown SD, Guss AM, Karpinets TV, Parks JM, Smolin N, Yang S, Land ML, Klingeman DM, Bhandiwad A, Rodriguez M, Jr, Raman B, Shao X, Mielenz JR, Smith JC, Keller M, Lynd LR. 2011. Mutant alcohol dehydrogenase leads to improved ethanol tolerance in Clostridium thermocellum. Proc Natl Acad Sci U S A 108:13752-13757. http://dx.doi.org/10.1073/pnas.1102444108.
22. Biswas R, Zheng T, Olson DG, Lynd LR, Guss AM. 2015. Elimination of hydrogenase active site assembly blocks H2 production and increases ethanol yield in Clostridium thermocellum. Biotechnol Biofuels 8:20. http://dx .doi.org/10.1186/s13068-015-0204-4.
23. Shaw AJ, Miller BB, Rogers SR, Kenealy WR, Meola A, Bhandiwad A, Sillers WR, Shikhare I, Hogsett DA, Herring CD. 2015. Anaerobic detoxification of acetic acid in a thermophilic ethanologen. Biotechnol Biofuels 8:75. http://dx.doi.org/10.1186/s13068-015-0257-4.
24. Olson DG, Lynd LR. 2012. Transformation of Clostridium thermocellum by electroporation. Methods Enzymol 510:317-330. http://dx.doi.org/10.1016/B978-0-12-415931-0.00017-3.
25. Shaw AJ, Hogsett DA, Lynd LR. 2010. Natural competence in Thermoanaerobacter and Thermoanaerobacterium species. Appl Environ Microbiol 76:4713-4719. http://dx.doi.org/10.1128/AEM.00402-10.
26. Zhou J, Olson DG, Argyros DA, Deng Y, van Gulik WM, van Dijken JP, Lynd LR. 2013. Atypical glycolysis in Clostridium thermocellum. Appl Environ Microbiol 79:3000-3008. http://dx.doi.org/10.1128/AEM .04037-12.
27. Zhang Y, Lynd LR. 2003. Quantification of cell and cellulase mass concentrations during anaerobic cellulose fermentation: development of an enzyme-linked immunosorbent assay-based method with application to Clostridium thermocellum batch cultures. Anal Chem 75:3131-3139. http://dx.doi.org/10.1021/ac020271n.
28. Espinosa A, Yan L, Zhang Z, Foster L, Clark D, Li E, Stanley SL, Jr. 2001. The bifunctional Entamoeba histolytica alcohol dehydrogenase 2 (EhADH2) protein is necessary for amebic growth and survival and requires an intact C-terminal domain for both alcohol dehydrogenase and acetaldehyde dehydrogenase activity. J Biol Chem 276:20136-20143. http://dx.doi.org/10.1074/jbc.M101349200.
29. Schwarzenbacher R, von Delft F, Canaves JM, Brinen LS, Dai X, Deacon AM, Elsliger MA, Eshaghi S, Floyd R, Godzik A, Grittini C, Grzechnik SK, Guda C, Jaroszewski L, Karlak C, Klock HE, Koesema E, Kovarik JS, Kreusch A, Kuhn P, Lesley SA, Mcmullan D, Mcphillips TM, Miller MA, Miller MD, Morse A, Moy K, Ouyang J, Page R, Robb A, Rodrigues K, Selby TL, Spraggon G, Stevens RC, van den Bedem H, Velasquez J, Vincent J, Wang X, West B, Wolf G, Hodgson KO, Wooley J, Wilson IA. 2004. Crystal structure of an iron-containing 1,3- propanediol dehydrogenase (TM0920) from Thermotoga maritima at 1.3 Å resolution. Proteins 54:174-177. http://dx.doi.org/10.1002/prot.10594.
30. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. 1983. Comparison of simple potential functions for simulating liquid water. J Chem Phys 79:926-935. http://dx.doi.org/10.1063/1.445869.
31. Jo S, Kim T, Iyer VG, Im W. 2008. CHARMM-GUI: a web-based graphical user interface for CHARMM. J Comput Chem 29:1859-1865. http://dx.doi.org/10.1002/jcc.20945.
32. Koukos PI, Glykos NM. 2013. Grcarma: a fully automated task-oriented interface for the analysis of molecular dynamics trajectories. J Comput Chem 34:2310-2312. http://dx.doi.org/10.1002/jcc.23381.
33. Arnau J, Jørgensen F, Madsen SM, Vrang A, Israelsen H. 1998. Cloning of the Lactococcus lactis adhE gene, encoding a multifunctional alcohol dehydrogenase, by complementation of a fermentative mutant of Escherichia coli. J Bacteriol 180:3049-3055.
34. Bruchhaus I, Tannich E. 1994. Purification and molecular characterization of the NAD(+)-dependent acetaldehyde/alcohol dehydrogenase from Entamoeba histolytica. Biochem J 303:743-748.
35. Dailly Y, Bunch P, Clark D. 2000. Comparison of the fermentative alcohol dehydrogenases of Salmonella typhimurium and Escherichia coli. Microbios 103:179-196.
36. Pei J, Zhou Q, Jiang Y, Le Y, Li H, Shao W, Wiegel J. 2010. Thermoanaerobacter spp. control ethanol pathway via transcriptional regulation and versatility of key enzymes. Metab Eng 12:420-428. http://dx.doi.org /10.1016/j.ymben.2010.06.001.
37. Yao S, Mikkelsen MJ. 2010. Identification and overexpression of a bifunctional aldehyde/alcohol dehydrogenase responsible for ethanol production in Thermoanaerobacter mathranii. J Mol Microbiol Biotechnol 19:123-133. http://dx.doi.org/10.1159/000321498.
38. Koo OK, Jeong DW, Lee JM, Kim MJ, Lee JH, Chang HC, Kim JH, Lee HJ. 2005. Cloning and characterization of the bifunctional alcohol/acetaldehyde dehydrogenase gene (adhE) in Leuconostoc mesenteroides isolated from kimchi. Biotechnol Lett 27:505-510. http://dx.doi.org/10.1007/s10529-005-2541-z.
39. Chen M, Li E, Stanley SL. 2004. Structural analysis of the acetaldehyde dehydrogenase activity of Entamoeba histolytica alcohol dehydrogenase 2 (EhADH2), a member of the ADHE enzyme family. Mol Biochem Parasitol 137:201-205. http://dx.doi.org/10.1016/j.molbiopara.2004.06.002.
40. Montella C, Bellsolell L, Perez-Luque R, Badia J, Baldoma L, Coll M, Aguilar J. 2005. Crystal structure of an iron-dependent group III dehydrogenase that interconverts L-lactaldehyde and L-1,2-propanediol in Escherichia coli. J Bacteriol 187:4957-4966. http://dx.doi.org/10.1128/JB .187.14.4957-4966.2005.
41. Huang H, Wang S, Moll J, Thauer RK. 2012. Electron bifurcation involved in the energy metabolism of the acetogenic bacterium Moorella thermoacetica growing on glucose or H2 plus CO2. J Bacteriol 194:3689-3699. http://dx.doi.org/10.1128/JB.00385-12.
42. Currie DH, Guss AM, Herring CD, Giannone RJ, Johnson CM, Lankford PK, Brown SD, Hettich RL, Lynd LR. 2014. Profile of secreted hydrolases, associated proteins, and SlpA in Thermoanaerobacterium saccharolyticum during the degradation of hemicellulose. Appl Environ Microbiol 80:5001-5011. http://dx.doi.org/10.1128/AEM.00998-14.
43. Verbeke TJ, Zhang X, Henrissat B, Spicer V, Rydzak T, Krokhin OV, Fristensky B, Levin DB, Sparling R. 2013. Genomic evaluation of Thermoanaerobacter spp. for the construction of designer co-cultures to improve lignocellulosic biofuel production. PLoS One 8:e59362. http://dx .doi.org/10.1371/journal.pone.0059362.
44. Radianingtyas H, Wright PC. 2003. Alcohol dehydrogenases from thermophilic and hyperthermophilic archaea and bacteria. FEMS Microbiol Rev 27:593-616. http://dx.doi.org/10.1016/S0168-6445(03)00068-8.
45. Burdette D, Zeikus JG. 1994. Purification of acetaldehyde dehydrogenase and alcohol dehydrogenases from Thermoanaerobacter ethanolicus 39E and characterization of the secondary-alcohol dehydrogenase (2 degrees Adh) as a bifunctional alcohol dehydrogenase-acetyl-CoA reductive thioesterase. Biochem J 302:163-170.
46. Lamed R, Zeikus JG. 1980. Ethanol production by thermophilic bacteria:relationship between fermentation product yields of and catabolic enzyme activities in Clostridium thermocellum and Thermoanaerobium brockii. J Bacteriol 144:569-578.
47. Neale AD, Scopes RK, Kelly JM, Wettenhall REH. 1986. The two alcohol dehydrogenases of Zymomonas mobilis purification by differential dye ligand chromatography, molecular characterisation and physiological roles. Eur J Biochem 154:119-124. http://dx.doi.org/10.1111/j.1432-1033.1986.tb09366.x.
48. Chen Z, Lee WR, Chang SH. 1991. Role of aspartic acid 38 in the cofactor specificity of Drosophila alcohol dehydrogenase. Eur J Biochem 202:263-267. http://dx.doi.org/10.1111/j.1432-1033.1991.tb16371.x.
49. Kessler D, Herth W, Knappe J. 1992. Ultrastructure and pyruvate formate- lyase radical quenching property of the multienzymic AdhE protein of Escherichia coli. J Biol Chem 267:18073-18073.
50. Extance JP. 2012. Ph.D. thesis. University of Bath, Bath, United Kingdom.
51. Lee JM, Venditti RA, Jameel H, Kenealy WR. 2011. Detoxification of woody hydrolyzates with activated carbon for bioconversion to ethanol by the thermophilic anaerobic bacterium Thermoanaerobacterium saccharolyticum. Biomass Bioenergy 35:626-636. http://dx.doi.org/10.1016/j.biombioe.2010.10.021.