Comparative analysis of extremely thermophilic Caldicellulosiruptor species reveals common and unique cellular strategies for plant biomass utilization

Applied and Environmental Microbiology

Volumn 81, Issue 20, 2015, Pages 7159-7170

  Zurawski, Jeffrey V ^a   Conway, Jonathan M ^a   Lee, Laura L ^a   Simpson, Hunter J ^a   Izquierdo, Javier A ^a,e   Blumer Schuette, Sara ^a,d   Nookaew, Intawat ^b   Adams, Michael W W ^c   Kelly, Robert M ^a  

^a North Carolina State University   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c University of Georgia   (United States)

^d OAKLAND UNIVERSITY   (United States)

^e HOFSTRA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOMASS; CARBOHYDRATES; CELLULOSE; ECOLOGY; ENCODING (SYMBOLS); ENZYME ACTIVITY; GENES; HYDROLASES; PLANTS (BOTANY); SUGARS; TRANSCRIPTION;

CARBOHYDRATE CONTENT; COMPARATIVE ANALYSIS; CRYSTALLINE CELLULOSE; GLYCOSIDE HYDROLASES; LIGNOCELLULOSIC BIOMASS; SUBSTRATE COMPOSITION; SUBSTRATE UTILIZATION; TRANSCRIPTION LEVEL;

BACTERIA;

BIOTECHNOLOGY; CARBOHYDRATE; CELLS AND CELL COMPONENTS; CELLULOSE; CHEMOTAXIS; COMPARATIVE STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; GRASS; LIGNIN; MICROBIAL ACTIVITY; PHYTOMASS; TEMPERATURE EFFECT;

BACTERIA; BIOMASS; GENETIC ENGINEERING; GENOTYPES; PLANTS; SPECIES IDENTIFICATION;

BACTERIA (MICROORGANISMS); CALDICELLULOSIRUPTOR; CALDICELLULOSIRUPTOR SACCHAROLYTICUS; PANICUM VIRGATUM;

CELLULASE;

BACTERIUM; BIOMASS; ENZYMOLOGY; METABOLISM; PANICUM; PLANT;

BACTERIA; BIOMASS; CELLULASE; PANICUM; PLANTS;

EID: 84943338596     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01622-15     Document Type: Article

References (65)

1. Blumer-Schuette SE, Brown SD, Sander KB, Bayer EA, Kataeva I, Zurawski JV, Conway JM, Adams MW, Kelly RM. 2014. Thermophilic lignocellulose deconstruction. FEMS Microbiol Rev 38:393-448. http://dx.doi.org/10.1111/1574-6976.12044.
2. Blumer-Schuette SE, Ozdemir I, Mistry D, Lucas S, Lapidus A, Cheng JF, Goodwin LA, Pitluck S, Land ML, Hauser LJ, Woyke T, Mikhailova N, Pati A, Kyrpides NC, Ivanova N, Detter JC, Walston-Davenport K, Han S, Adams MW, Kelly RM. 2011. Complete genome sequences for the anaerobic, extremely thermophilic plant biomass-degrading bacteria Caldicellulosiruptor hydrothermalis, Caldicellulosiruptor kristjanssonii, Caldicellulosiruptor kronotskyensis, Caldicellulosiruptor owensensis, and Caldicellulosiruptor lactoaceticus. J Bacteriol 193:1483-1484. http://dx.doi.org/10.1128/JB.01515-10.
3. Huang CY, Patel BK, Mah RA, Baresi L. 1998. Caldicellulosiruptor owensensis sp. nov., an anaerobic, extremely thermophilic, xylanolytic bacterium. Int J Syst Bacteriol 48:91-97. http://dx.doi.org/10.1099/00207713-48-1-91.
4. Elkins JG, Lochner A, Hamilton-Brehm SD, Davenport KW, Podar M, Brown SD, Land ML, Hauser LJ, Klingeman DM, Raman B, Goodwin LA, Tapia R, Meincke LJ, Detter JC, Bruce DC, Han CS, Palumbo AV, Cottingham RW, Keller M, Graham DE. 2010. Complete genome sequence of the cellulolytic thermophile Caldicellulosiruptor obsidiansis OB47T. J Bacteriol 192:6099-6100. http://dx.doi.org/10.1128/JB.00950-10.
5. Hamilton-Brehm SD, Mosher JJ, Vishnivetskaya T, Podar M, Carroll S, Allman S, Phelps TJ, Keller M, Elkins JG. 2010. Caldicellulo siruptor obsidiansis sp. nov., an anaerobic, extremely thermophilic, cellulolytic bacterium isolated from Obsidian Pool, Yellowstone National Park. Appl Environ Microbiol 76:1014-1020. http://dx.doi.org/10.1128/AEM.01903-09.
6. Kataeva IA, Yang SJ, Dam P, Poole FL, II, Yin Y, Zhou F, Chou WC, Xu Y, Goodwin L, Sims DR, Detter JC, Hauser LJ, Westpheling J, Adams MW. 2009. Genome sequence of the anaerobic, thermophilic, and cellulolytic bacterium "Anaerocellum thermophilum" DSM 6725. J Bacteriol 191:3760-3761. http://dx.doi.org/10.1128/JB.00256-09.
7. Svetlichnyi VA, Svetlichnaya TP, Chernykh NA, Zavarzin GA. 1990. Anaerocellum thermophilum gen. nov. sp. nov.: an extremely thermophilic cellulolytic eubacterium isolated from hot-springs in the Valley of Geysers. Microbiology 59:598-604.
8. Miroshnichenko ML, Kublanov IV, Kostrikina NA, Tourova TP, Kolganova TV, Birkeland NK, Bonch-Osmolovskaya EA. 2008. Caldicellulosiruptor kronotskyensis sp. nov. and Caldicellulosiruptor hydrothermalis sp. nov., two extremely thermophilic, cellulolytic, anaerobic bacteria from Kamchatka thermal springs. Int J Syst Evol Microbiol 58:1492-1496. http://dx.doi.org/10.1099/ijs.0.65236-0.
9. Rainey FA, Janssen PH, Morgan HW, Stackebrandt E. 1993. A biphasic approach to the determination of the phenotypic and genotypic diversity of some anaerobic, cellulolytic, thermophilic, rod-shaped bacteria. Antonie Van Leeuwenhoek 64:341-355.
10. van de Werken HJ, Verhaart MR, VanFossen AL, Willquist K, Lewis DL, Nichols JD, Goorissen HP, Mongodin EF, Nelson KE, van Niel EW, Stams AJ, Ward DE, de Vos WM, van der Oost J, Kelly RM, Kengen SW. 2008. Hydrogenomics of the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus. Appl Environ Microbiol 74:6720-6729. http://dx.doi.org/10.1128/AEM.00968-08.
11. Rainey FA, Donnison AM, Janssen PH, Saul D, Rodrigo A, Bergquist PL, Daniel RM, Stackebrandt E, Morgan HW. 1994. Description of Caldicellulosiruptor saccharolyticus gen. sp. nov.: an obligately anaerobic, extremely thermophilic, cellulolytic bacterium. FEMS Microbiol Lett 120: 263-266. http://dx.doi.org/10.1111/j.1574-6968.1994.tb07043.x.
12. Bredholt S, Sonne-Hansen J, Nielsen P, Mathrani IM, Ahring BK. 1999. Caldicellulosiruptor kristjanssonii sp. nov., a cellulolytic, extremely thermophilic, anaerobic bacterium. Int J Syst Bacteriol 49(Part 3):991-996.
13. Mladenovska Z, Mathrani IM, Ahring BK. 1995. Isolation and characterization of Caldicellulosiruptor lactoaceticus sp. nov, an extremely thermophilic, cellulolytic, anaerobic bacterium. Arch Microbiol 163:223-230. http://dx.doi.org/10.1007/BF00305357.
14. Brunecky R, Alahuhta M, Xu Q, Donohoe BS, Crowley MF, Kataeva IA, Yang SJ, Resch MG, Adams MWW, Lunin VV, Himmel ME, Bomble YJ. 2013. Revealing nature's cellulase diversity: the digestion mechanism of Caldicellulosiruptor bescii CelA. Science 342:1513-1516. http://dx.doi.org/10.1126/science.1244273.
15. Ozdemir I, Blumer-Schuette SE, Kelly RM. 2012. S-layer homology domain proteins C. saccharolyticus_0678 and C. saccharolyticus_2722 are implicated in plant polysaccharide deconstruction by the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus. Appl Environ Microbiol 78:768-777. http://dx.doi.org/10.1128/AEM.07031-11.
16. VanFossen AL, Ozdemir I, Zelin SL, Kelly RM. 2011. Glycoside hydrolase inventory drives plant polysaccharide deconstruction by the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus. Biotechnol Bioeng 108:1559-1569. http://dx.doi.org/10.1002/bit.23093.
17. Blumer-Schuette SE, Giannone RJ, Zurawski JV, Ozdemir I, Ma Q, Yin Y, Xu Y, Kataeva I, Poole FL, II, Adams MW, Hamilton-Brehm SD, Elkins JG, Larimer FW, Land ML, Hauser LJ, Cottingham RW, Hettich RL, Kelly RM. 2012. Caldicellulosiruptor core and pangenomes reveal determinants for noncellulosomal thermophilic deconstruction of plant biomass. J Bacteriol 194:4015-4028. http://dx.doi.org/10.1128/JB.00266-12.
18. Blumer-Schuette SE, Lewis DL, Kelly RM. 2010. Phylogenetic, microbiological, and glycoside hydrolase diversities within the extremely thermophilic, plant biomass-degrading genus Caldicellulosiruptor. Appl Environ Microbiol 76:8084-8092. http://dx.doi.org/10.1128/AEM.01400-10.
19. Blumer-Schuette SE, Alahuhta M, Conway JM, Lee LL, Zurawski JV, Giannone RJ, Hettich RL, Lunin VV, Himmel ME, Kelly RM. 2015. Discrete and structurally unique proteins (tapirins) mediate attachment of extremely thermophilic Caldicellulosiruptor species to cellulose. J Biol Chem 290:10645-10656. http://dx.doi.org/10.1074/jbc.M115.641480.
20. Basen M, Rhaesa AM, Kataeva I, Prybol CJ, Scott IM, Poole FL, Adams MW. 2014. Degradation of high loads of crystalline cellulose and of unpretreated plant biomass by the thermophilic bacterium Caldicellulosiruptor bescii. Bioresour Technol 152:384-392. http://dx.doi.org/10.1016/j.biortech.2013.11.024.
21. Yang SJ, Kataeva I, Wiegel J, Yin Y, Dam P, Xu Y, Westpheling J, Adams MW. 2010. Classification of 'Anaerocellum thermophilum' strain DSM 6725 as Caldicellulosiruptor bescii sp. nov. Int J Syst Evol Microbiol 60:2011-2015. http://dx.doi.org/10.1099/ijs.0.017731-0.
22. Chung D, Cha M, Guss AM, Westpheling J. 2014. Direct conversion of plant biomass to ethanol by engineered Caldicellulosiruptor bescii. Proc Natl Acad Sci U S A 111:8931-8936. http://dx.doi.org/10.1073/pnas.1402210111.
23. Zurawski JV, Blumer-Schuette SE, Conway JM, Kelly RM. 2014. The extremely thermophilic genus Caldicellulosiruptor: physiological and genomic characteristics for complex carbohydrate conversion to molecular hydrogen, p 177-195. In Zannoni D, De Philippis R (ed), Advances in photosynthesis and respiration, vol 38. Microbial bioenergy: hydrogen production. Springer Science + Business Media, Dordrecht, Netherlands.
24. Sluiter AHB, Ruiz R, Scarlata C, Sluiter J, Templeton D, Crocker D. 2012. Determination of structural carbohydrates and lignin in biomass. Technical report NREL/TP-510-42618. National Renewable Energy Laboratory, Golden, CO. http://www.nrel.gov/biomass/pdfs/42618.pdf.
25. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Anal Chem 28:350-356. http://dx.doi.org/10.1021/ac60111a017.
26. de Vrije T, Mars AE, Budde MA, Lai MH, Dijkema C, de Waard P, Claassen PA. 2007. Glycolytic pathway and hydrogen yield studies of the extreme thermophile Caldicellulosiruptor saccharolyticus. Appl Microbiol Biotechnol 74:1358-1367. http://dx.doi.org/10.1007/s00253-006-0783-x.
27. Chen SF, Mowery RA, Sevcik RS, Scarlata CJ, Chambliss CK. 2010. Compositional analysis of water-soluble materials in switchgrass. J Agric Food Chem 58:3251-3258. http://dx.doi.org/10.1021/jf9033877.
28. Thammasouk K, Tandjo D, Penner MH. 1997. Influence of extractives on the analysis of herbaceous biomass. J Agric Food Chem 45:437-443. http://dx.doi.org/10.1021/jf960401r.
29. Lochner A, Giannone RJ, Keller M, Antranikian G, Graham DE, Hettich RL. 2011. Label-free quantitative proteomics for the extremely thermophilic bacterium Caldicellulosiruptor obsidiansis reveal distinct abundance patterns upon growth on cellobiose, crystalline cellulose, and switchgrass. J Proteome Res 10:5302-5314. http://dx.doi.org/10.1021/pr200536j.
30. Lochner A, Giannone RJ, Rodriguez M, Jr, Shah MB, Mielenz JR, Keller M, Antranikian G, Graham DE, Hettich RL. 2011. Use of label-free quantitative proteomics to distinguish the secreted cellulolytic systems of Caldicellulosiruptor bescii and Caldicellulosiruptor obsidiansis. Appl Environ Microbiol 77:4042-4054. http://dx.doi.org/10.1128/AEM.02811-10.
31. Kataeva I, Foston MB, Yang S-J, Pattathil S, Biswal AK, Poole Ii FL, Basen M, Rhaesa AM, Thomas TP, Azadi P, Olman V, Saffold TD, Mohler KE, Lewis DL, Doeppke C, Zeng Y, Tschaplinski TJ, York WS, Davis M, Mohnen D, Xu Y, Ragauskas AJ, Ding S-Y, Kelly RM, Hahn MG, Adams MWW. 2013. Carbohydrate and lignin are simultaneously solubilized from unpretreated switchgrass by microbial action at high temperature. Energ Environ Sci 6:2186. http://dx.doi.org/10.1039/c3ee40932e.
32. van Niel EWJ, Claassen PAM, Stams AJM. 2003. Substrate and product inhibition of hydrogen production by the extreme thermophile, Caldicellulosiruptor saccharolyticus. Biotechnol Bioeng 81:255-262. http://dx.doi.org/10.1002/bit.10463.
33. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. http://dx.doi.org/10.1093/bioinformatics/btq461.
34. Koning SM, Albers SV, Konings WN, Driessen AJ. 2002. Sugar transport in (hyper)thermophilic archaea. Res Microbiol 153:61-67. http://dx.doi.org/10.1016/S0923-2508(01)01289-X.
35. Vanfossen AL, Verhaart MR, Kengen SM, Kelly RM. 2009. Carbohydrate utilization patterns for the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus reveal broad growth substrate preferences. Appl Environ Microbiol 75:7718-7724. http://dx.doi.org/10.1128/AEM.01959-09.
36. Verhaart MR, Bielen AA, van der Oost J, Stams AJ, Kengen SW. 2010. Hydrogen production by hyperthermophilic and extremely thermophilic bacteria and archaea: mechanisms for reductant disposal. Environ Technol 31:993-1003. http://dx.doi.org/10.1080/09593331003710244.
37. Pawar SS, van Niel EWJ. 2014. Evaluation of assimilatory sulphur me tabolism in Caldicellulosiruptor saccharolyticus. Bioresource Technol 169: 677-685. http://dx.doi.org/10.1016/j.biortech.2014.07.059.
38. Yokoyama K, Leimkuhler S. 2015. The role of FeS clusters for molybdenum cofactor biosynthesis and molybdoenzymes in bacteria. Biochim Biophys Acta 1853:1335-1349. http://dx.doi.org/10.1016/j.bbamcr.2014.09.021.
39. Segall JE, Ishihara A, Berg HC. 1985. Chemotactic signaling in filamentous cells of Escherichia coli. J Bacteriol 161:51-59.
40. Ninfa EG, Stock A, Mowbray S, Stock J. 1991. Reconstitution of the bacterial chemotaxis signal transduction system from purified components. J Biol Chem 266:9764-9770.
41. Stock JB, Lukat GS, Stock AM. 1991. Bacterial chemotaxis and the molecular logic of intracellular signal transduction networks. Annu Rev Biophys Biophys Chem 20:109-136. http://dx.doi.org/10.1146/annurev.bb.20.060191.000545.
42. Wuichet K, Alexander RP, Zhulin IB. 2007. Comparative genomic and protein sequence analyses of a complex system controlling bacterial chemotaxis. Methods Enzymol 422:1-31.
43. Szurmant H, Ordal GW. 2004. Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol Mol Biol Rev 68:301-319. http://dx.doi.org/10.1128/MMBR.68.2.301-319.2004.
44. Hengge R. 2009. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263-273. http://dx.doi.org/10.1038/nrmicro2109.
45. Pawar SS VT, Grey C, van Niel EW. 2015. Biofilm formation by designed co-cultures of Caldicellulosiruptor species as a means to improve hydrogen productivity. Biotechnol Biofuels 8:19. http://dx.doi.org/10.1186/s13068-015-0201-7.
46. Wang ZW, Hamilton-Brehm SD, Lochner A, Elkins JG, Morrell-Falvey JL. 2011. Mathematical modeling of hydrolysate diffusion and utilization in cellulolytic biofilms of the extreme thermophile Caldicellulosiruptor obsidiansis. Bioresource Technol 102:3155-3162. http://dx.doi.org/10.1016/j.biortech.2010.10.104.
47. Wang ZW, Lee SH, Elkins JG, Morrell-Falvey JL. 2011. Spatial and temporal dynamics of cellulose degradation and biofilm formation by Caldicellulosiruptor obsidiansis and Clostridium thermocellum. AMB Express 1:30. http://dx.doi.org/10.1186/2191-0855-1-30.
48. Chan C, Paul R, Samoray D, Amiot NC, Giese B, Jenal U, Schirmer T. 2004. Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci U S A 101:17084-17089. http://dx.doi.org/10.1073/pnas.0406134101.
49. Hickman JW, Tifrea DF, Harwood CS. 2005. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102:14422-14427. http://dx.doi.org/10.1073/pnas.0507170102.
50. Paul R, Abel S, Wassmann P, Beck A, Heerklotz H, Jenal U. 2007. Activation of the diguanylate cyclase PleD by phosphorylation-mediated dimerization. J Biol Chem 282:29170-29177. http://dx.doi.org/10.1074/jbc.M704702200.
51. Taylor BL, Zhulin IB. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63:1092-2172.
52. Galperin MY, Nikolskaya AN, Koonin EV. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203:11-21.
53. Guttenplan SB, Kearns DB. 2013. Regulation of flagellar motility during biofilm formation. FEMS Microbiol Rev 37:849-871. http://dx.doi.org/10.1111/1574-6976.12018.
54. Paul K, Nieto V, Carlquist WC, Blair DF, Harshey RM. 2010. The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a "backstop brake" mechanism. Mol Cell 38:128-139. http://dx.doi.org/10.1016/j.molcel.2010.03.001.
55. Ryjenkov DA, Simm R, Romling U, Gomelsky M. 2006. The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J Biol Chem 281:30310-30314. http://dx.doi.org/10.1074/jbc.C600179200.
56. Bordeleau E, Purcell EB, Lafontaine DA, Fortier LC, Tamayo R, Burrus V. 2015. Cyclic di-GMP riboswitch-regulated type IV pili contribute to aggregation of Clostridium difficile. J Bacteriol 197:819-832. http://dx.doi.org/10.1128/JB.02340-14.
57. Chen Y, Chai Y, Guo JH, Losick R. 2012. Evidence for cyclic di-GMPmediated signaling in Bacillus subtilis. J Bacteriol 194:5080-5090. http://dx.doi.org/10.1128/JB.01092-12.
58. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490-D495. http://dx.doi.org/10.1093/nar/gkt1178.
59. Biely P. 2012. Microbial carbohydrate esterases deacetylating plant polysaccharides. Biotechnol Adv 30:1575-1588. http://dx.doi.org/10.1016/j.biotechadv.2012.04.010.
60. Williamson G, Kroon PA, Faulds CB. 1998. Hairy plant polysaccharides: a close shave with microbial esterases. Microbiology 144(Part 8):2011-2023.
61. Garron ML, Cygler M. 2014. Uronic polysaccharide degrading enzymes. Curr Opin Struct Biol 28:87-95. http://dx.doi.org/10.1016/j.sbi.2014.07.012.
62. Mohnen D. 2008. Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266-277. http://dx.doi.org/10.1016/j.pbi.2008.03.006.
63. Chung D, Pattathil S, Biswal AK, Hahn MG, Mohnen D, Westpheling J. 2014. Deletion of a gene cluster encoding pectin degrading enzymes in Caldicellulosiruptor bescii reveals an important role for pectin in plant biomass recalcitrance. Biotechnol Biofuels 7:147. http://dx.doi.org/10.1186/s13068-014-0147-1.
64. Young J, Chung D, Bomble YJ, Himmel ME, Westpheling J. 2014. Deletion of Caldicellulosiruptor bescii CelA reveals its crucial role in the deconstruction of lignocellulosic biomass. Biotechnol Biofuels 7:142. http://dx.doi.org/10.1186/s13068-014-0142-6.
65. Shockley KR, Ward DE, Chhabra SR, Conners SB, Montero CI, Kelly RM. 2003. Heat shock response by the hyperthermophilic archaeon Pyrococcus furiosus. Appl Environ Microbiol 69:2365-2371. http://dx.doi.org/10.1128/AEM.69.4.2365-2371.2003.