Profile of secreted hydrolases, associated proteins, and SlpA in Thermoanaerobacterium saccharolyticum during the degradation of hemicellulose

Applied and Environmental Microbiology

Volumn 80, Issue 16, 2014, Pages 5001-5011

  Currie, D H ^a,b   Guss, A M ^a,c   Herring, C D ^b   Giannone, R J ^c   Johnson, C M ^c   Lankford, P K ^c   Brown, S D ^c   Hettich, R L ^c   Lynd, L R ^a,b  

^a DARTMOUTH COLLEGE   (United States)

^b Mascoma Corporation   (United States)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; HYDROLASES; PROTEINS; STARCH;

CONDITIONAL EXPRESSIONS; HEMICELLULOSE DEGRADATION; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; MORPHOLOGICAL CHANGES; PHOSPHOTRANSFERASE SYSTEM; THERMOANAEROBACTERIUM; THERMOPHILIC ANAEROBIC BACTERIA; TRANS-MEMBRANE PROTEINS;

CELLULOSE;

BACTERIAL PROTEIN; HEMICELLULOSE; HYDROLASE; POLYSACCHARIDE;

BIOREMEDIATION; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN TRANSPORT; THERMOANAEROBACTERIUM;

BACTERIAL PROTEINS; BIODEGRADATION, ENVIRONMENTAL; HYDROLASES; POLYSACCHARIDES; PROTEIN TRANSPORT; THERMOANAEROBACTERIUM;

EID: 84904876100     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00998-14     Document Type: Article

References (73)

1. Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Hogberg P, Linder S, Mackenzie FT, Moore B, III, Pedersen T, Rosenthal Y, Seitzinger S, Smetacek V, Steffen W. 2000. The global carbon cycle: a test of our knowledge of earth as a system. Science 290:291-296. http://dx.doi.org/10.1126/science.290.5490.291.
2. Klemm D, Heublein B, Fink HP, Bohn A. 2005. Cellulose: fascinating biopolymer and sustainable raw material. Angew. Chem. Int. Ed. 44: 3358-3393. http://dx.doi.org/10.1002/anie.200460587.
3. Wilson DB. 2011. Microbial diversity of cellulose hydrolysis. Curr. Opin. Microbiol. 14:259-263. http://dx.doi.org/10.1016/j.mib.2011.04.004.
4. Popper ZA. 2008. Evolution and diversity of green plant cell walls. Curr. Opin. Plant Biol. 11:286-292. http://dx.doi.org/10.1016/j.pbi.2008.02.012.
5. McKendry P. 2002. Energy production from biomass (part 1): overview of biomass. Bioresour. Technol. 83:37-46. http://dx.doi.org/10.1016/S0960-8524(01)00118-3.
6. Conners SB, Montero CI, Comfort DA, Shockley KR, Johnson MR, Chhabra SR, Kelly RM. 2005. An expression-driven approach to the prediction of carbohydrate transport and utilization regulons in the hyperthermophilic bacterium Thermotoga maritima. J. Bacteriol. 187:7267-7282. http://dx.doi.org/10.1128/JB.187.21.7267-7282.2005.
7. Dodd D, Moon YH, Swaminathan K, Mackie RI, Cann IKO. 2010. Transcriptomic analyses of xylan degradation by Prevotella bryantii and insights into energy acquisition by xylanolytic Bacteroidetes. J. Biol. Chem. 285:30261-30273. http://dx.doi.org/10.1074/jbc.M110.141788.
8. Dunne JC, Li D, Kelly WJ, Leahy SC, Bond JJ, Attwood GT, Jordan TW. 2012. Extracellular polysaccharide-degrading proteome of Butyrivibrio proteoclasticus. J. Proteome Res. 11:131-142. http://dx.doi.org/10.1021/pr200864j.
9. Gilad O, Jacobsen S, Stuer-Lauridsen B, Pedersen MB, Garrigues C, Svensson B. 2010. Combined transcriptome and proteome analysis of Bifidobacterium animalis subsp. lactis BB-12 grown on xylooligosaccharides and a model of their utilization. Appl. Environ. Microbiol. 76:7285-7291. http://dx.doi.org/10.1128/AEM.00738-10.
10. Raberg M, Peplinski K, Heiss S, Ehrenreich A, Voigt B, Doring C, Bomeke M, Hecker M, Steinbuchel A. 2011. Proteomic and transcriptomic elucidation of the mutant Ralstonia eutropha G(+)1 with regard to glucose utilization. Appl. Environ. Microbiol 77:2058-2070. http://dx.doi.org/10.1128/AEM.02015-10.
11. Fischer A, Yang SJ, Bayer AS, Vaezzadeh AR, Herzig S, Stenz L, Girard M, Sakoulas G, Scherl A, Yeaman MR, Proctor RA, Schrenzel J, Francois P. 2011. Daptomycin resistance mechanisms in clinically derived Staphylococcus aureus strains assessed by a combined transcriptomics and proteomics approach. J. Antimicrob. Chemother. 66:1696-1711. http://dx.doi.org/10.1093/jac/dkr195.
12. Pohl S, Tu WY, Aldridge PD, Gillespie C, Hahne H, Mader U, Read TD, Harwood CR. 2011. Combined proteomic and transcriptomic analysis of the response of Bacillus anthracis to oxidative stress. Proteomics 11:3036-3055. http://dx.doi.org/10.1002/pmic.201100085.
13. Sleytr UB, Sara M. 1997. Bacterial and archaeal S-layer proteins: structure-function relationships and their biotechnological applications. Trends Biotechnol. 15:20-26. http://dx.doi.org/10.1016/S0167-7799(96) 10063-9.
14. Sara M, Sleytr UB. 2000. S-layer proteins. J. Bacteriol. 182:859-868. http://dx.doi.org/10.1128/JB.182.4.859-868.2000.
15. Rothfuss H, Lara JC, Schmid AK, Lidstrom ME. 2006. Involvement of the S-layer proteins Hpi and SlpA in the maintenance of cell envelope integrity in Deinococcus radiodurans R1. Microbiology 152:2779-2787. http://dx.doi.org/10.1099/mic.0.28971-0.
16. Sleytr UB, Thorne KJ. 1976. Chemical characterization of the regularly arranged surface layers of Clostridium thermosaccharolyticum and Clostridium thermohydrosulfuricum. J. Bacteriol. 126:377-383.
17. Schaffer C, Wugeditsch T, Kahlig H, Scheberl A, Zayni S, Messner P. 2002. The surface layer (S-layer) glycoprotein of Geobacillus stearothermophilus NRS 2004/3a-analysis of its glycosylation. J. Biol. Chem. 277: 6230-6239. http://dx.doi.org/10.1074/jbc.M108873200.
18. Sara M, Sleytr UB. 1987. Molecular-sieving through S layers of Bacillus stearothermophilus strains. J. Bacteriol. 169:4092-4098.
19. Sara M, Sleytr UB. 1987. Production and characteristics of ultrafiltration membranes with uniform pores from two-dimensional arrays of proteins. J. Membr. Sci. 33:27-49. http://dx.doi.org/10.1016/S0376-7388(00)80050-2.
20. Sara M, Pum D, Sleytr UB. 1992. Permeability and charge-dependent adsorption properties of the S-layer lattice from Bacillus coagulans E38-66. J. Bacteriol. 174:3487-3493.
21. Egelseer E, Schocher I, Sara M, Sleytr UB. 1995. The S-layer from Bacillus stearothermophilus DSM-2358 functions as an adhesion site for a high-molecular-weight amylase. J. Bacteriol. 177:1444-1451.
22. Izquierdo JA, Sizova MV, Lynd LR. 2010. Diversity of bacteria and glycosyl hydrolase family 48 genes in cellulolytic consortia enriched from thermophilic biocompost. Appl. Environ. Microbiol. 76:3545-3553. http://dx.doi.org/10.1128/AEM.02689-09.
23. Lee YE, Jain MK, Lee CY, Lowe SE, Zeikus JG. 1993. Taxonomic distinction of saccharolytic thermophilic anaerobes: description of Thermoanaerobacterium xylanolyticum gen. nov., sp. nov., and Thermoanaerobacterium saccharolyticum gen. nov., sp. nov., reclassification of Thermoanaerobium brockii, Clostridium thermosulfurogenes, and Clostridium thermohydrosulfuricum E100-69 as Thermoanaerobacter brockii comb. nov., Thermoanaerobacterium thermosulfurigenes comb. nov., and Thermoanaerobacter thermohydrosulfuricus comb. nov., respectively; and transfer of Clostridium thermohydrosulfuricum 39E to Thermoanaerobacter ethanolicus. Int. J. Syst. Bacteriol. 43:41-51. http://dx.doi.org/10.1099/00207713-43-1-41.
24. 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.
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. Shaw AJ, Covalla SF, Hogsett DA, Herring CD. 2011. Marker removal system for Thermoanaerobacterium saccharolyticum and development of a markerless ethanologen. Appl. Environ. Microbiol. 77:2534-2536. http://dx.doi.org/10.1128/AEM.01731-10.
27. 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.
28. Podkaminer KK, Shao XJ, Hogsett DA, Lynd LR. 2011. Enzyme inactivation by ethanol and development of a kinetic model for thermophilic simultaneous saccharification and fermentation at 50 degrees C with Thermoanaerobacterium saccharolyticum ALK2. Biotechnol. Bioeng. 108: 1268-1278. http://dx.doi.org/10.1002/bit.23050.
29. Lee YE, Lowe SE, Zeikus JG. 1993. Regulation and characterization of xylanolytic enzymes of Thermoanaerobacterium saccharolyticum B6A-RI. Appl. Environ. Microbiol. 59:763-771.
30. Lee YE, Lowe SE, Zeikus JG. 1993. Gene cloning, sequencing, and biochemical characterization of endoxylanase from Thermoanaerobacterium saccharolyticum B6A-RI. Appl. Environ. Microbiol. 59:3134-3137.
31. Lee YE, Zeikus JG. 1993. Genetic organization, sequence and biochemical characterization of recombinant beta-xylosidase from Thermoanaerobacterium saccharolyticum strain B6A-RI. J. Gen. Microbiol. 139(Pt 6):1235-1243. http://dx.doi.org/10.1099/00221287-139-6-1235.
32. Lee YE, Ramesh MV, Zeikus JG. 1993. Cloning, sequencing and biochemical characterization of xylose isomerase from Thermoanaerobacterium saccharolyticum strain B6A-RI. J. Gen. Microbiol. 139(Pt 6):1227-1234. http://dx.doi.org/10.1099/00221287-139-6-1227.
33. Ramesh MV, Podkovyrov SM, Lowe SE, Zeikus JG. 1994. Cloning and sequencing of the Thermoanaerobacterium saccharolyticum B6A-RI apu gene and purification and characterization of the amylopullulanase from Escherichia coli. Appl. Environ. Microbiol. 60:94-101.
34. Bronnenmeier K, Meissner H, Stocker S, Staudenbauer WL. 1995. Alpha-D-glucuronidases from the xylanolytic thermophiles Clostridium stercorarium and Thermoanaerobacterium saccharolyticum. Microbiology 141(Pt 9):2033-2040. http://dx.doi.org/10.1099/13500872-141-9-2033.
35. Liu SY, Wiegel J, Gherardini FC. 1996. Purification and cloning of a thermostable xylose (glucose) isomerase with an acidic pH optimum from Thermoanaerobacterium strain JW/SL-YS 489. J. Bacteriol. 178:5938-5945.
36. Lorenz WW, Wiegel J. 1997. Isolation, analysis, and expression of two genes from Thermoanaerobacterium sp. strain JW/SL YS485: a betaxylosidase and a novel acetyl xylan esterase with cephalosporin C deacetylase activity. J. Bacteriol. 179:5436-5441.
37. Podkaminer KK, Guss AM, Trajano HL, Hogsett DA, Lynd LR. 2012. Characterization of xylan utilization and discovery of a new endoxylanase in Thermoanaerobacterium saccharolyticum through targeted gene deletions. Appl. Environ. Microbiol. 78:8441-8447. http://dx.doi.org/10.1128/AEM.02130-12.
38. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8:785-786. http://dx.doi.org/10.1038/nmeth.1701.
39. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580. http://dx.doi.org/10.1006/jmbi.2000.4315.
40. Li X, He Z, Zhou J. 2005. Selection of optimal oligonucleotide probes for microarrays using multiple criteria, global alignment and parameter estimation. Nucleic Acids Res. 33:6114-6123. http://dx.doi.org/10.1093/nar/gki914.
41. Brown SD, Raman B, McKeown CK, Kale SP, He ZL, Mielenz JR. 2007. Construction and evaluation of a Clostridium thermocellum ATCC 27405 whole-genome oligonucleotide microarray. Appl. Biochem. Biotechnol. 137:663-674. http://dx.doi.org/10.1007/s12010-007-9087-6.
42. Chhabra SR, He Q, Huang KH, Gaucher SP, Alm EJ, He Z, Hadi MZ, Hazen TC, Wall JD, Zhou J, Arkin AP, Singh AK. 2006. Global analysis of heat shock response in Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 188:1817-1828. http://dx.doi.org/10.1128/JB.188.5.1817-1828.2006.
43. Brown SD, Martin M, Deshpande S, Seal S, Huang K, Alm E, Yang YF, Wu LY, Yan TF, Liu XD, Arkin A, Chourey K, Zhou JZ, Thompson DK. 2006. Cellular response of Shewanella oneidensis to strontium stress. Appl. Environ. Microbiol. 72:890-900. http://dx.doi.org/10.1128/AEM.72.1.890-900.2006.
44. Washburn MP, Wolters D, Yates JR. 2001. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19:242-247. http://dx.doi.org/10.1038/85686.
45. McDonald WH, Ohi R, Miyamoto DT, Mitchison TJ, Yates JR. 2002. Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins from complex mixtures: single-dimension LC-MS/MS, 2-phase MudPIT, and 3-phase MudPIT. Int. J. Mass Spectrom. 219: 245-251. http://dx.doi.org/10.1016/S1387-3806(02)00563-8.
46. Eng JK, McCormack AL, Yates JR. 1994. An approach to correlate tandem mass-spectral data of peptides with amino-acid-sequences in a protein database. J. Am. Soc. Mass Spectrom. 5:976-989. http://dx.doi.org/10.1016/1044-0305(94)80016-2.
47. Tabb DL, McDonald WH, Yates JR. 2002. DTASelect and contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1:21-26. http://dx.doi.org/10.1021/pr015504q.
48. Zybailov B, Mosley AL, Sardiu ME, Coleman MK, Florens L, Washburn MP. 2006. Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J. Proteome Res. 5:2339-2347. http://dx.doi.org/10.1021/pr060161n.
49. Griffin NM, Yu J, Long F, Oh P, Shore S, Li Y, Koziol JA, Schnitzer JE. 2009. Label-free, normalized quantification of complex mass spectrometry data for proteomic analysis. Nat. Biotechnol. 28:83-89. http://dx.doi.org/10.1038/nbt.1592.
50. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2:953-971. http://dx.doi.org/10.1038/nprot.2007.131.
51. Erickson BK, Mueller RS, VerBerkmoes NC, Shah M, Singer SW, Thelen MP, Banfield JF, Hettich RL. 2010. Computational prediction and experimental validation of signal peptide cleavages in the extracellular proteome of a natural microbial community. J. Proteome Res. 9:2148-2159. http://dx.doi.org/10.1021/pr900877a.
52. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA, Smith HO. 2009. Enzymatic assembly ofDNAmolecules up to several hundred kilobases. Nat. Methods 6:343-345. http://dx.doi.org/10.1038/nmeth.1318.
53. Gibson DG, Smith HO, Hutchison CA, Venter JC, Merryman C. 2010. Chemical synthesis of the mouse mitochondrial genome. Nat. Methods 7:901-903. http://dx.doi.org/10.1038/nmeth.1515.
54. Core Team R. 2012. R: a language and environment for statistical computing. Core Team R, Vienna, Austria.
55. 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.
56. Freudl R. 2013. Leaving home ain't easy: protein export systems in Grampositive bacteria. Res. Microbiol. 164:664-674. http://dx.doi.org/10.1016/j.resmic.2013.03.014.
57. Desvaux M, Khan A, Scott-Tucker A, Chaudhuri RR, Pallen MJ, Henderson IR. 2005. Genomic analysis of the protein secretion systems in Clostridium acetobutylicum ATCC 824. Biochim. Biophys. Acta 1745:223-253. http://dx.doi.org/10.1016/j.bbamcr.2005.04.006.
58. Messner P, Steiner K, Zarschler K, Schaffer C. 2008. S-layer nanoglycobiology of bacteria. Carbohydr. Res. 343:1934-1951. http://dx.doi.org/10.1016/j.carres.2007.12.025.
59. Schneewind O, Missiakas DM. 2012. Protein secretion and surface display in Gram-positive bacteria. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367:1123-1139. http://dx.doi.org/10.1098/rstb.2011.0210.
60. 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.
61. Viollier PH, Weihofen A, Folcher M, Thompson CJ. 2003. Posttranscriptional regulation of the Streptomyces coelicolor stress responsive sigma factor, SigH, involves translational control, proteolytic processing, and an anti-sigma factor homolog. J. Mol. Biol. 325:637-649. http://dx.doi.org/10.1016/S0022-2836(02)01280-9.
62. Dierks T, Miech C, Hummerjohann J, Schmidt B, Kertesz MA, von Figura K. 1998. Posttranslational formation of formylglycine in prokaryotic sulfatases by modification of either cysteine or serine. J. Biol. Chem. 273:25560-25564. http://dx.doi.org/10.1074/jbc.273.40.25560.
63. Dierks T, Lecca MR, Schlotterhose P, Schmidt B, von Figura K. 1999. Sequence determinants directing conversion of cysteine to formylglycine in eukaryotic sulfatases. EMBO J. 18:2084-2091. http://dx.doi.org/10.1093/emboj/18.8.2084.
64. Sardiello M, Annunziata I, Roma G, Ballabio A. 2005. Sulfatases and sulfatase modifying factors: an exclusive and promiscuous relationship. Hum. Mol. Genet. 14:3203-3217. http://dx.doi.org/10.1093/hmg/ddi351.
65. Parenti G, Meroni G, Ballabio A. 1997. The sulfatase gene family. Curr. Opin. Genet. Dev. 7:386-391. http://dx.doi.org/10.1016/S0959-437X(97) 80153-0.
66. Hanson SR, Best MD, Wong CH. 2004. Sulfatases: structure, mechanism, biological activity, inhibition, and synthetic utility. Angew. Chem. Int. Ed. Engl. 43:5736-5763. http://dx.doi.org/10.1002/anie.200300632.
67. Landgrebe J, Dierks T, Schmidt B, von Figura K. 2003. The human SUMF1 gene, required for posttranslational sulfatase modification, defines a new gene family which is conserved from pro-to eukaryotes. Gene 316:47-56. http://dx.doi.org/10.1016/S0378-1119(03)00746-7.
68. Salyers AA, Vercellotti JR, West SE, Wilkins TD. 1977. Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon. Appl. Environ. Microbiol. 33:319-322.
69. Wolf DM, Fontaine-Bodin L, Bischofs I, Price G, Keasling J, Arkin AP. 2008. Memory in microbes: quantifying history-dependent behavior in a bacterium. PLoS One 3:e1700. http://dx.doi.org/10.1371/journal.pone.0001700.
70. Gawande PV, Griffiths MW. 2005. Growth history influences starvationinduced expression of uspA, grpE, and rpoS and subsequent cryotolerance in Escherichia coli O157:H7. J. Food Prot. 68:1154-1158.
71. Rozen Y, Belkin S. 2001. Survival of enteric bacteria in seawater. FEMS Microbiol. Rev. 25:513-529. http://dx.doi.org/10.1111/j.1574-6976.2001.tb00589.x.
72. Song YJ, Xue YF, Ma YH. 2013. Global microarray analysis of carbohydrate use in alkaliphilic hemicellulolytic bacterium Bacillus sp. N16-5. PLoS One 8:e54090. http://dx.doi.org/10.1371/journal.pone.0054090.
73. Hottes AK, Meewan M, Yang D, Arana N, Romero P, McAdams HH, Stephens C. 2004. Transcriptional profiling of Caulobacter crescentus during growth on complex and minimal media. J. Bacteriol. 186:1448-1461. http://dx.doi.org/10.1128/JB.186.5.1448-1461.2004.