Integrated omics analyses reveal the details of metabolic adaptation of Clostridium thermocellum to lignocellulose-derived growth inhibitors released during the deconstruction of switchgrass

Biotechnology for Biofuels

Volumn 10, Issue 1, 2017, Pages

  Poudel, Suresh ^a,b   Giannone, Richard J ^a   Rodriguez, Miguel ^a   Raman, Babu ^a,c   Martin, Madhavi Z ^a   Engle, Nancy L ^a   Mielenz, Jonathan R ^a   Nookaew, Intawat ^a,d   Brown, Steven D ^a,b   Tschaplinski, Timothy J ^a   Ussery, David ^a,d   Hettich, Robert L ^a,b  

^a OAK RIDGE NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

^c DOW AGROSCIENCES LLC   (United States)

^d UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Biofuel; Cellulosome; Clostridium thermocellum; Ethanol; Lignocellulosic; Mass spectrometry; Metabolomics; Proteomics; Switchgrass; Transcriptomics

Indexed keywords

AMINO ACIDS; BIOFUELS; BIOMASS; CARBON; CELL MEMBRANES; CELLULOSE; CLOSTRIDIUM; ECOLOGY; ENZYMES; ETHANOL; LIGNIN; MASS SPECTROMETRY; METABOLISM; MOLECULAR BIOLOGY; PHYSIOLOGY; PLANTS (BOTANY); SUBSTRATES;

CELLULOSOMES; CLOSTRIDIUM THERMOCELLUM; LIGNOCELLULOSIC; METABOLOMICS; PROTEOMICS; SWITCHGRASS; TRANSCRIPTOMICS;

FATTY ACIDS;

BIOFUEL; BIOMASS; CELLULOSE; ETHANOL; GRASS; INHIBITOR; MASS SPECTROMETRY; METABOLISM; PROTEOMICS; THERMOPHILIC BACTERIUM;

BIOMASS; ETHANOL; LIGNOCELLULOSE; MASS SPECTROMETERS;

CLOSTRIDIUM THERMOCELLUM; PANICUM VIRGATUM;

EID: 85008699086     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/s13068-016-0697-5     Document Type: Article

References (55)

1. Keshwani DR, Cheng JJ. Switchgrass for bioethanol and other value-added applications: a review. Bioresour Technol. 2009;100(4):1515-23.
2. Kacurakova M, Capek P, Sasinkova V, Wellner N, Ebringerova A. FT-IR study of plant cell wall model compounds: pectic polysaccharides and hemicelluloses. Carbohydr Polym. 2000;43(2):195-203.
3. Himmel ME, Ding S-Y, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD. Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science. 2007;315(5813):804-7.
4. Raman B, Pan C, Hurst GB, Rodriguez M Jr, McKeown CK, Lankford PK, Samatova NF, Mielenz JR. Impact of pretreated switchgrass and biomass carbohydrates on Clostridium thermocellum ATCC 27405 cellulosome composition: a quantitative proteomic analysis. PLoS ONE. 2009;4(4):e5271.
5. Bayer EA, Shoham Y, Lamed R. Cellulose-decomposing bacteria and their enzyme systems. In: The prokaryotes. Berlin: Springer; 2006. p. 578-617.
6. Xu Q, Resch MG, Podkaminer K, Yang S, Baker JO, Donohoe BS, Wilson C, Klingeman DM, Olson DG, Decker SR. Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities. Sci Adv. 2016;2(2):e1501254.
7. Blumer-Schuette SE, Brown SD, Sander KB, Bayer EA, Kataeva I, Zurawski JV, Conway JM, Adams MW, Kelly RM. Thermophilic lignocellulose deconstruction. FEMS Microbiol Rev. 2014;38(3):393-448.
8. Lynd LR, Van Zyl WH, McBride JE, Laser M. Consolidated bioprocessing of cellulosic biomass: an update. Curr Opin Biotechnol. 2005;16(5):577-83.
9. Park BH, Karpinets TV, Syed MH, Leuze MR, Uberbacher EC. CAZymes analysis toolkit (CAT): web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. Glycobiology. 2010;20(12):1574-84.
10. Demain AL, Newcomb M, Wu JHD. Cellulase, clostridia, and ethanol. Microbiol Mol Biol Rev. 2005;69(1):124-54.
11. Papanek B, Biswas R, Rydzak T, Guss AM. Elimination of metabolic pathways to all traditional fermentation products increases ethanol yields in Clostridium thermocellum. Metab Eng. 2015;32:49-54.
12. Yang S, Giannone RJ, Dice L, Yang ZK, Engle NL, Tschaplinski TJ, Hettich RL, Brown SD. Clostridium thermocellum ATCC27405 transcriptomic, metabolomic and proteomic profiles after ethanol stress. BMC Genom. 2012;13(1):336.
13. Raman B, McKeown CK, Rodriguez M, Brown SD, Mielenz JR. Transcriptomic analysis of Clostridium thermocellum ATCC 27405 cellulose fermentation. BMC Microbiol. 2011;11(1):134.
14. Riederer A, Takasuka TE, Makino S-I, Stevenson DM, Bukhman YV, Elsen NL, Fox BG. Global gene expression patterns in Clostridium thermocellum as determined by microarray analysis of chemostat cultures on cellulose or cellobiose. Appl Environ Microbiol. 2011;77(4):1243-53.
15. Gold ND, Martin VJJ. Global view of the Clostridium thermocellum cellulosome revealed by quantitative proteomic analysis. J Bacteriol. 2007;189(19):6787-95.
16. Mussatto SI, Roberto IC. Alternatives for detoxification of diluted-acid lignocellulosic hydrolyzates for use in fermentative processes: a review. Bioresour Technol. 2004;93(1):1-10.
17. Larsson S, Reimann A, Nilvebrant N-O, Jönsson LJ. Comparison of different methods for the detoxification of lignocellulose hydrolyzates of spruce. Appl Biochem Biotechnol. 1999;77(1-3):91-103.
18. Wilson CM, Rodriguez CM, Johnson SL, Martin T, Chu RD, Wolfinger LJ, Hauser ML, Land DM, Klingeman MH, Syed AJ, et al. Global transcriptome analysis of Clostridium thermocellum ATCC 27405 during growth on dilute acid pretreated Populus and switchgrass. Biotechnol Biofuels. 2013;6(1):179.
19. Wei H, Fu Y, Magnusson L, Baker JO, Maness P-C, Xu Q, Yang S, Bowersox A, Bogorad I, Wang W. Comparison of transcriptional profiles of Clostridium thermocellum grown on cellobiose and pretreated yellow poplar using RNA-Seq. Front Microbiol. 2014;5:142.
20. Kridelbaugh DM, Nelson J, Engle NL, Tschaplinski TJ, Graham DE. Nitrogen and sulfur requirements for Clostridium thermocellum and Caldicellulosiruptor bescii on cellulosic substrates in minimal nutrient media. Bioresour Technol. 2013;130:125-35.
21. Tschaplinski TJ, Standaert RF, Engle NL, Martin MZ, Sangha AK, Parks JM, Smith JC, Samuel R, Jiang N, Pu Y. Down-regulation of the caffeic acid O-methyltransferase gene in switchgrass reveals a novel monolignol analog. Biotechnol Biofuels. 2012;5:71.
22. Tabb DL, Narasimhan C, Strader MB, Hettich RL. DBDigger: reorganized proteomic database identification that improves flexibility and speed. Anal Chem. 2005;77(8):2464-74.
23. Florens L, Carozza MJ, Swanson SK, Fournier M, Coleman MK, Workman JL, Washburn MP. Analyzing chromatin remodeling complexes using shotgun proteomics and normalized spectral abundance factors. Methods. 2006;40(4):303-11.
24. Kumar L, Futschik ME. Mfuzz: a software package for soft clustering of microarray data. Bioinformation. 2007;2(1):5.
25. Väremo L, Nookaew I. Platform for integrative analysis of omics data. 2013.
26. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28(1):27-30.
27. Dumitrache A, Akinosho H, Rodriguez M, Meng X, Yoo CG, Natzke J, Engle NL, Sykes RW, Tschaplinski TJ, Muchero W. Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure. Biotechnol Biofuels. 2016;9(1):1.
28. Shekiro J, Kuhn EM, Selig MJ, Nagle NJ, Decker SR, Elander RT. Enzymatic conversion of xylan residues from dilute acid-pretreated corn stover. Appl Biochem Biotechnol. 2012;168(2):421-33.
29. Currie DH, Raman B, Gowen CM, Tschaplinski TJ, Land ML, Brown SD, Covalla SF, Klingeman DM, Yang ZK, Engle NL. Genome-scale resources for Thermoanaerobacterium saccharolyticum. BMC Syst Biol. 2015;9(1):1.
30. Ktsoyan ZA, Beloborodova NV, Sedrakyan AM, Osipov GA, Khachatryan ZA, Kelly D, Manukyan GP, Arakelova KA, Hovhannisyan AI, Olenin AY. Profiles of microbial fatty acids in the human metabolome are disease-specific. Front Microbiol. 2010;1:148.
31. Timmons MD, Knutson BL, Nokes SE, Strobel HJ, Lynn BC. Analysis of composition and structure of Clostridium thermocellum membranes from wild-type and ethanol-adapted strains. Appl Microbiol Biotechnol. 2009;82(5):929-39.
32. Ibraheem O, Ndimba BK. Molecular adaptation mechanisms employed by ethanologenic bacteria in response to lignocellulose-derived inhibitory compounds. Int J Biol Sci. 2013;9(6):598.
33. Murínová S, Dercová K. Response mechanisms of bacterial degraders to environmental contaminants on the level of cell walls and cytoplasmic membrane. Int J Microbiol. 2014;2014:16.
34. Linville JL, Rodriguez M Jr, Land M, Syed MH, Engle NL, Tschaplinski TJ, Mielenz JR, Cox CD. Industrial robustness: understanding the mechanism of tolerance for the Populus hydrolysate-tolerant mutant strain of Clostridium thermocellum. PLoS ONE. 2013;8(10):e78829.
35. Burton E, Martin VJJ. Proteomic analysis of Clostridium thermocellum ATCC 27405 reveals the upregulation of an alternative transhydrogenase-malate pathway and nitrogen assimilation in cells grown on cellulose. Can J Microbiol. 2012;58(12):1378-88.
36. Martín J-F, Liras P. Engineering of regulatory cascades and networks controlling antibiotic biosynthesis in Streptomyces. Curr Opin Microbiol. 2010;13(3):263-73.
37. Pedersen AG, Jensen LJ, Brunak S, Stærfeldt H-H, Ussery DW. A DNA structural atlas for Escherichia coli. J Mol Biol. 2000;299(4):907-30.
38. Satchwell SC, Drew HR, Travers AA. Sequence periodicities in chicken nucleosome core DNA. J Mol Biol. 1986;191(4):659-75.
39. Bayer EA, Chanzy H, Lamed R, Shoham Y. Cellulose, cellulases and cellulosomes. Curr Opin Struct Biol. 1998;8(5):548-57.
40. Zhang Y-HP, Lynd LR. Cellulose utilization by Clostridium thermocellum: bioenergetics and hydrolysis product assimilation. Proc Natl Acad Sci USA. 2005;102(20):7321-5.
41. Dürre P. Handbook on clostridia. Boca Raton: CRC Press; 2005.
42. Dror TW, Rolider A, Bayer EA, Lamed R, Shoham Y. Regulation of major cellulosomal endoglucanases of Clostridium thermocellum differs from that of a prominent cellulosomal xylanase. J Bacteriol. 2005;187(7):2261-6.
43. Strobel H, Caldwell F, Dawson K. Carbohydrate transport by the anaerobic thermophile Clostridium thermocellum LQRI. Appl Environ Microbiol. 1995;61(11):4012-5.
44. Zhou J, Olson DG, Argyros DA, Deng Y, van Gulik WM, van Dijken JP, Lynd LR. Atypical glycolysis in Clostridium thermocellum. Appl Environ Microbiol. 2013;79(9):3000-8.
45. Lo J, Zheng T, Hon S, Olson DG, Lynd LR. The bifunctional alcohol and aldehyde dehydrogenase gene, adhE, is necessary for ethanol production in Clostridium thermocellum and Thermoanaerobacterium saccharolyticum. J Bacteriol. 2015;197(8):1386-93.
46. Brown SD, Guss AM, Karpinets TV, Parks JM, Smolin N, Yang S, Land ML, Klingeman DM, Bhandiwad A, Rodriguez M. Mutant alcohol dehydrogenase leads to improved ethanol tolerance in Clostridium thermocellum. Proc Natl Acad Sci. 2011;108(33):13752-7.
47. Holwerda EK, Thorne PG, Olson DG, Amador-Noguez D, Engle NL, Tschaplinski TJ, van Dijken JP, Lynd LR. The exometabolome of Clostridium thermocellum reveals overflow metabolism at high cellulose loading. Biotechnol Biofuels. 2014;7(1):155.
48. Granström TB, Izumori K, Leisola M. A rare sugar xylitol. Part II: biotechnological production and future applications of xylitol. Appl Microbiol Biotechnol. 2007;74(2):273-6.
49. Alves LA, Felipe MG, Silva JBAE, Silva SS, Prata AM. Pretreatment of sugarcane bagasse hemicellulose hydrolysate for xylitol production by Candida guilliermondii. Appl Biochem Biotechnol. 1998;70(1):89-98.
50. Van Der Veen D, Lo J, Brown SD, Johnson CM, Tschaplinski TJ, Martin M, Engle NL, Van den Berg RA, Argyros AD, Caiazza NC. Characterization of Clostridium thermocellum strains with disrupted fermentation end-product pathways. J Ind Microbiol Biotechnol. 2013;40(7):725-34.
51. Klein W, Weber MH, Marahiel MA. Cold shock response of Bacillus subtilis: isoleucine-dependent switch in the fatty acid branching pattern for membrane adaptation to low temperatures. J Bacteriol. 1999;181(17):5341-9.
52. Roberts SB, Gowen CM, Brooks JP, Fong SS. Genome-scale metabolic analysis of Clostridium thermocellum for bioethanol production. BMC Syst Biol. 2010;4(1):1.
53. Cronan JE, Thomas J. Bacterial fatty acid synthesis and its relationships with polyketide synthetic pathways. Methods Enzymol. 2009;459:395-433.
54. Unell M, Kabelitz N, Jansson JK, Heipieper HJ. Adaptation of the psychrotroph Arthrobacter chlorophenolicus A6 to growth temperature and the presence of phenols by changes in the anteiso/iso ratio of branched fatty acids. FEMS Microbiol Lett. 2007;266(2):138-43.
55. Berg JM, Tymoczko JL, Stryer L. Biochemistry. In: Freeman WH, editor. Fatty acids are synthesized and degraded by different pathways, 5th edition, Section 22.4. New York: Basingstoke; 2002.