Enhanced whole genome sequence and annotation of Clostridium stercorarium DSM8532T using RNA-seq transcriptomics and high-throughput proteomics
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  • 作者:John J Schellenberg (20)
    Tobin J Verbeke (20)
    Peter McQueen (21)
    Oleg V Krokhin (21)
    Xiangli Zhang (22)
    Graham Alvare (22)
    Brian Fristensky (22)
    Gerhard G Thallinger (24) (25)
    Bernard Henrissat (26) (27)
    John A Wilkins (21)
    David B Levin (23)
    Richard Sparling (20)

    20. Department of Microbiology
    ; University of Manitoba ; Winnipeg ; Canada
    21. Manitoba Centre for Proteomics and Systems Biology
    ; University of Manitoba ; Winnipeg ; Canada
    22. Department of Plant Sciences
    ; University of Manitoba ; Winnipeg ; Canada
    24. Core Facility Bioinformatics
    ; Austrian Centre of Industrial Biotechnology (ACIB) ; Graz ; Austria
    25. Institute for Genomics and Bioinformatics
    ; Graz University of Technology ; Graz ; Austria
    26. Architecture et Fonction des Macromol茅cules Biologiques
    ; Universit茅 Aix-Marseille ; Marseille ; France
    27. UMR 7257
    ; Centre National de Recherche Scientifique ; 163 ave. de Luminy ; Marseille ; 13288 ; France
    23. Department of Biosystems Engineering
    ; University of Manitoba ; Winnipeg ; Canada
  • 关键词:Genome ; Proteome ; Transcriptome ; RNA ; seq ; Tandem mass spectrometry ; Proteogenomics ; Glycolysis ; Pentose phosphate pathway ; Transaldolase
  • 刊名:BMC Genomics
  • 出版年:2014
  • 出版时间:December 2014
  • 年:2014
  • 卷:15
  • 期:1
  • 全文大小:2,287 KB
  • 参考文献:1. Jordan, DB, Bowman, MJ, Braker, JD, Dien, BS, Hector, RE, Lee, CC, Mertens, JA, Wagschal, K (2012) Plant cell walls to ethanol. Biochem J 442: pp. 241-252 CrossRef
    2. Levin, DB, Carere, CR, Cicek, N, Sparling, R (2009) Challenges for biohydrogen production via direct lignocellulose fermentation. Int J Hyd Energy 34: pp. 7390-7403 CrossRef
    3. Zverlov, VV, Schwarz, WH (2008) Bacterial cellulose hydrolysis in anaerobic environmental subsystems - Clostridium thermocellum and Clostridium stercorarium, thermophilic plant-fiber degraders. Ann N Y Acad Sci 1125: pp. 298-307 CrossRef
    4. Schwarz, W, Bronnenmeier, K, Landmann, B, Wanner, G, Staudenbauer, W, Kurose, N, Takayama, T (1995) Molecular characterization of four strains of the cellulolytic thermophile Clostridium stercorarium. Biosci Biotech Biochem 59: pp. 1661-1665 CrossRef
    5. Li, Y, Tschaplinski, TJ, Engle, NL, Hamilton, CY, Rodriguez, M, Liao, JC, Schadt, CW, Guss, AM, Yang, Y, Graham, DE (2012) Combined inactivation of the Clostridium cellulolyticum lactate and malate dehydrogenase genes substantially increases ethanol yield from cellulose and switchgrass fermentations. Biotechnol Biofuels 5: pp. 2 CrossRef
    6. Elkins, JG, Raman, B, Keller, M (2010) Engineered microbial systems for enhanced conversion of lignocellulosic biomass. Curr Opin Biotechnol 21: pp. 657-662 CrossRef
    7. Xu, L, Tschirner, U (2011) Improved ethanol production from various carbohydrates through anaerobic thermophilic co-culture. Biores Tech 102: pp. 10065-10071 CrossRef
    8. He, Q, Hemme, CL, Jiang, H, He, Z, Zhou, J (2011) Mechanisms of enhanced cellulosic bioethanol fermentation by co-cultivation of Clostridium and Thermoanaerobacter spp. Biores Tech 102: pp. 9586-9592 CrossRef
    9. Zuroff, TR, Xiques, SB, Curtis, WR (2013) Consortia-mediated bioprocessing of cellulose to ethanol with a symbiotic Clostridium phytofermentans/yeast co-culture. Biotechnol Biofuels 6: pp. 59 CrossRef
    10. Carere, CR, Rydzak, T, Verbeke, TJ, Cicek, N, Levin, DB, Sparling, R (2012) Linking genome content to biofuel production yields: a meta-analysis of major catabolic pathways among select H2 and ethanol-producing bacteria. BMC Microbiol 12: pp. 295 CrossRef
    11. Rydzak, T, McQueen, PD, Krokhin, OV, Spicer, V, Ezzati, P, Dwivedi, RC, Shamshurin, D, Levin, DB, Wilkins, JA, Sparling, R (2012) Proteomic analysis of Clostridium thermocellum core metabolism: relative protein expression profiles and growth phase-dependent changes in protein expression. BMC Microbiol 12: pp. 214 CrossRef
    12. Tolonen, AC, Haas, W, Chilaka, AC, Aach, J, Gygi, SP, Church, GM (2011) Proteome-wide systems analysis of a cellulosic biofuel-producing microbe. Mol Syst Biol 7: pp. 461 CrossRef
    13. Yang, S, Giannone, RJ, Dice, L, Yang, ZK, Engle, NL, Tschaplinski, TJ, Hettich, RL, Brown, SD (2012) Clostridium thermocellum ATCC27405 transcriptomic, metabolomic and proteomic profiles after ethanol stress. BMC Genomics 13: pp. 336 CrossRef
    14. Peterson, ES, McCue, LA, Schrimpe-Rutledge, AC, Jensen, JL, Walker, H, Kobold, MA, Webb, SR, Payne, SH, Ansong, C, Adkins, JN, Cannon, WR, Webb-Robertson, B-JM (2012) VESPA: software to facilitate genomic annotation of prokaryotic organisms through integration of proteomic and transcriptomic data. BMC Genomics 13: pp. 131 CrossRef
    15. Petkau, A, Stuart-Edwards, M, Stothard, P, Van Domselaar, G (2010) Interactive microbial genome visualization with GView. Bioinformatics 26: pp. 3125-3126 CrossRef
    16. Siezen, RJ, Wilson, G, Todt, T (2010) Prokaryotic whole-transcriptome analysis: deep sequencing and tiling arrays. Microb Biotechnol 3: pp. 125-130 CrossRef
    17. 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: pp. e59362 CrossRef
    18. Bronnenmeier, K, Kundt, K, Riedel, K (1997) Structure of the Clostridium stercorarium gene celY encoding the exo-1, 4-{beta}-glucanase Avicelase II. Microbiol 143: pp. 891-898 CrossRef
    19. Nishimoto, M, Fushinobu, S, Miyanaga, A, Wakagi, T, Shoun, H, Sakka, K, Ohmiya, K, Nirasawa, S, Kitaoka, M, Hayashi, K (2004) Crystallization and preliminary X-ray analysis of xylanase B from Clostridium stercorarium. Acta Crystallogr D Biol Crystallogr 60: pp. 342-343 CrossRef
    20. Adelsberger, H, Hertel, C, Glawischnig, E, Zverlov, VV, Schwarz, WH (2004) Enzyme system of Clostridium stercorarium for hydrolysis of arabinoxylan: reconstitution of the in vivo system from recombinant enzymes. Microbiol 150: pp. 2257-2266 CrossRef
    21. Fukumura, M, Sakka, K, Shimada, K, Ohmiya, K (1995) Nucleotide sequence of the Clostridium stercorarium xynB gene encoding an extremely thermostable xylanase, and characterization of the translated product. Biosci Biotech Biochem 59: pp. 40-46 CrossRef
    22. Hla, S, Kurokawa, K, Suryani, , Kimura, T, Ohmiya, K, Sakka, K (2005) A novel thermophilic pectate lyase containing two catalytic modules of Clostridium stercorarium. Biosci Biotech Biochem 69: pp. 2138-2145 CrossRef
    23. Jauris, S, R眉cknagel, KP, Schwarz, WH, Kratzsch, P, Bronnenmeier, K, Staudenbauer, WL (1990) Sequence analysis of the Clostridium stercorarium celZ gene encoding a thermoactive cellulase (Avicelase I): identification of catalytic and cellulose-binding domains. Mol Gen Genet 223: pp. 258-267 CrossRef
    24. Reichenbecher, M, Lottspeich, F, Bronnenmeier, K (1997) Purification and properties of a cellobiose phosphorylase (CepA) and a cellodextrin phosphorylase (CepB) from the cellulolytic thermophile Clostridium stercorarium. Eur J Biochem 247: pp. 262-267 CrossRef
    25. Sakka, K, Yoshikawa, K, Kojima, Y, Karita, S, Ohmiya, K, Shimada, K (1993) Nucleotide sequence of the Clostridium stercorarium xylA gene encoding a bifunctional protein with 尾-d-xylosidase and 伪-L-arabinofuranosidase activities, and properties of the translated product. Biosci Biotech Biochem 57: pp. 268-272 CrossRef
    26. Schwarz, W, Jauris, S, Kouba, M, Bronnenmeier, K, Staudenbauer, WL (1989) Cloning and expression of Clostridium stercorarium cellulase genes in Escherichia coli.. Biotechnol Lett 11: pp. 461-466 CrossRef
    27. Suryani, , Kimura, T, Sakka, K, Ohmiya, K (2003) Cloning, sequencing, and expression of the gene encoding the Clostridium stercorarium 伪-Galactosidase Aga36A in Escherichia coli.. Biosci Biotech Biochem 67: pp. 2160-2166 CrossRef
    28. Suryani, , Kimura, T, Sakka, K, Ohmiya, K (2004) Sequencing and expression of the gene encoding the Clostridium stercorarium beta-xylosidase Xyl43B in Escherichia coli. Biosci Biotech Biochem 68: pp. 609-614 CrossRef
    29. Zverlov, VV, Liebl, W, Bachleitner, M, Schwarz, WH (1998) Nucleotide sequence of arfB of Clostridium stercorarium, and prediction of catalytic residues of 伪鈥扡鈥抋rabinofuranosidases based on local similarity with several families of glycosyl hydrolases. FEMS Microbiol Lett 164: pp. 337-343
    30. Zverlov, V, Hertel, C, Bronnenmeier, K, Hroch, A, Kellermann, J, Schwarz, WH (2000) The thermostable 伪鈥扡鈥抮hamnosidase RamA of Clostridium stercorarium: biochemical characterization and primary structure of a bacterial 伪鈥扡鈥抮hamnoside hydrolase, a new type of inverting glycoside hydrolase. Mol Microbiol 35: pp. 173-179 CrossRef
    31. Ali, MK, Fukumura, M, Sakano, K, Karita, S, Kimura, T, Sakka, K, Ohmiya, K (1999) Cloning, sequencing, and expression of the gene encoding the Clostridium stercorarium xylanase C in Escherichia coli. Biosci Biotech Biochem 63: pp. 1596-1604 CrossRef
    R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing.
    32. Worning, P, Jensen, LJ, Hallin, PF, St忙rfeldt, HH, Ussery, DW (2006) Origin of replication in circular prokaryotic chromosomes. Environ Microbiol 8: pp. 353-361 CrossRef
    33. Markowitz, VM, Mavromatis, K, Ivanova, NN, Chen, I-MA, Chu, K, Kyrpides, NC (2009) IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics 25: pp. 2271-2278 CrossRef
    34. Cantarel, BL, Coutinho, PM, Rancurel, C, Bernard, T, Lombard, V, Henrissat, B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: pp. D233-D238 CrossRef
    35. Saier, MH, Yen, MR, Noto, K, Tamang, DG, Elkan, C (2009) The transporter classification database: recent advances. Nucleic Acids Res 37: pp. D274-D278 CrossRef
    36. Fichant, G, Basse, M-J, Quentin, Y (2007) ABCdb: an online resource for ABC transporter repertories from sequenced archaeal and bacterial genomes. FEMS Microbiol Lett 256: pp. 333-339 CrossRef
    37. Calusinska, M, Happe, T, Joris, B, Wilmotte, A (2010) The surprising diversity of clostridial hydrogenases: a comparative genomic perspective. Microbiol 156: pp. 1575-1588 CrossRef
    38. Pati, A, Ivanova, NN, Mikhailova, N, Ovchinnikova, G, Hooper, SD, Lykidis, A, Kyrpides, NC (2010) GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes. Nat Meth 7: pp. 455-457 CrossRef
    39. Poehlein, A, Zverlov, VV, Daniel, R, Schwarz, WH, Liebl, W (2013) Complete genome sequence of Clostridium stercorarium subsp. stercorarium strain DSM 8532, a thermophilic degrader of plant cell wall fibers. Genome Announc 1: pp. e00073-13
    40. Trapnell, C, Pachter, L, Salzberg, SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: pp. 1105-1111 CrossRef
    41. Li, H, Handsaker, B, Wysoker, A, Fennell, T, Ruan, J, Homer, N, Marth, G, Abecasis, G, Durbin, R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25: pp. 2078-2079 CrossRef
    42. Rydzak, T, Levin, DB, Cicek, N, Sparling, R (2011) End-product induced metabolic shifts in Clostridium thermocellum ATCC 27405. Appl Microbiol Biotechnol 92: pp. 199-209 CrossRef
    43. Verbeke, TJ, Spicer, V, Krokhin, OV, Zhang, X, Schellenberg, JJ, Fristensky, B, Wilkins, JA, Levin, DB, Sparling, R (2014) Thermoanaerobacter thermohydrosulfuricus WC1 shows protein complement stability during fermentation of key lignocellulose-derived substrates. Appl Environ Microbiol 80: pp. 1602-1615 CrossRef
    44. Dwivedi, RC, Spicer, V, Harder, M, Antonovici, M, Ens, W, Standing, KG, Wilkins, JA, Krokhin, OV (2008) Practical implementation of 2D HPLC scheme with accurate peptide retention prediction in both dimensions for high-throughput bottom-up proteomics. Anal Chem 80: pp. 7036-7042 CrossRef
    45. Feny枚, D, Beavis, RC (2003) A method for assessing the statistical significance of mass spectrometry-based protein identifications using general scoring schemes. Anal Chem 75: pp. 768-774 CrossRef
    46. Wang, S, Huang, H, Moll, J, Thauer, RK (2010) NADP鈥?鈥塕eduction with reduced ferredoxin and NADP鈥?鈥塕eduction with NADH are coupled via an electron-bifurcating enzyme complex in clostridium kluyveri. J Bacteriol 192: pp. 5115-5123 CrossRef
    47. Lazarev, VN, Levitskii, SA, Basovskii, YI, Chukin, MM, Akopian, TA, Vereshchagin, VV, Kostrjukova, ES, Kovaleva, GY, Kazanov, MD, Malko, DB, Vitreschak, AG, Sernova, NV, Gelfand, MS, Demina, IA, Serebryakova, MV, Galyamina, MA, Vtyurin, NN, Rogov, SI, Alexeev, DG, Ladygina, VG, Govorun, VM (2011) Complete genome and proteome of Acholeplasma laidlawii. J Bacteriol 193: pp. 4943-4953 CrossRef
    48. Yoon, SH, Han, M-J, Jeong, H, Lee, CH, Xia, X-X, Lee, D-H, Shim, JH, Lee, SY, Oh, TK, Kim, JF (2012) Comparative multi-omics systems analysis of Escherichia coli strains B and K-12. Genome Biol 13: pp. R37 CrossRef
    49. Schrimpe-Rutledge, AC, Jones, MB, Chauhan, S, Purvine, SO, Sanford, JA, Monroe, ME, Brewer, HM, Payne, SH, Ansong, C, Frank, BC, Smith, RD, Peterson, SN, Motin, VL, Adkins, JN (2012) Comparative omics-driven genome annotation refinement: application across Yersiniae. PLoS One 7: pp. e33903 CrossRef
    50. Hu, S, Zheng, H, Gu, Y, Zhao, J, Zhang, W, Yang, Y, Wang, S, Zhao, G, Yang, S, Jiang, W (2011) Comparative genomic and transcriptomic analysis revealed genetic characteristics related to solvent formation and xylose utilization in Clostridium acetobutylicum EA 2018. BMC Genomics 12: pp. 93 CrossRef
    51. Deutschbauer, A, Price, MN, Wetmore, KM, Shao, W, Baumohl, JK, Xu, Z, Nguyen, M, Tamse, R, Davis, RW, Arkin, AP (2011) Evidence-based annotation of gene function in Shewanella oneidensis MR-1 using genome-wide fitness profiling across 121 conditions. PLoS Genet 7: pp. e1002385 CrossRef
    52. Yang, S, Pappas, KM, Hauser, LJ, Land, ML, Chen, G-L, Hurst, GB, Pan, C, Kouvelis, VN, Typas, MA, Pelletier, DA, Klingeman, DM, Chang, Y-J, Samatova, NF, Brown, SD (2009) Improved genome annotation for Zymomonas mobilis. Nat Biotechnol 27: pp. 893-894 CrossRef
    53. Haas, BJ, Chin, M, Nusbaum, C, Birren, BW, Livny, J (2012) How deep is deep enough for RNA-Seq profiling of bacterial transcriptomes?. BMC Genomics 13: pp. 734 CrossRef
    54. Wang, Y, Yu, Y, Pan, B, Hao, P, Li, Y, Shao, Z, Xu, X, Li, X (2012) Optimizing hybrid assembly of next-generation sequence data from Enterococcus faecium: a microbe with highly divergent genome. BMC Syst Biol 6: pp. S21 CrossRef
    55. Adav, SS, Ng, CS, Arulmani, M, Sze, SK (2010) Quantitative iTRAQ secretome analysis of Cellulolytic Thermobifida fusca. J Proteome Res 9: pp. 3016-3024 CrossRef
    56. Bachi, A, Bonaldi, T (2008) Quantitative proteomics as a new piece of the systems biology puzzle. J Proteomics 71: pp. 357-367 CrossRef
    57. Taniguchi, Y, Choi, PJ, Li, GW, Chen, H, Babu, M, Hearn, J, Emili, A, Xie, XS (2010) Quantifying E. coli Proteome and Transcriptome with Single-Molecule Sensitivity in Single Cells.. Science 329: pp. 533-538 CrossRef
    58. Dressaire, C, Gitton, C, Loubi猫re, P, Monnet, V, Queinnec, I, Cocaign-Bousquet, M (2009) Transcriptome and proteome exploration to model translation efficiency and protein stability in Lactococcus lactis. PLoS Comput Biol 5: pp. e1000606 CrossRef
    59. Davidson, AL, Dassa, E, Orelle, C, Chen, J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72: pp. 317-364 CrossRef
    60. Flechner, A, Gross, W, Martin, WF, Schnarrenberger, C (1999) Chloroplast class I and class II aldolases are bifunctional for fructose-1, 6-biphosphate and sedoheptulose-1, 7-biphosphate cleavage in the Calvin cycle. FEBS Lett 447: pp. 200-202 CrossRef
    61. Nakahigashi, K, Toya, Y, Ishii, N, Soga, T, Hasegawa, M, Watanabe, H, Takai, Y, Honma, M, Mori, H, Tomita, M (2009) Systematic phenome analysis of Escherichia coli multiple-knockout mutants reveals hidden reactions in central carbon metabolism. Mol Syst Biol 5: pp. 306 CrossRef
    62. Murray, WD (1986) Acetivibrio cellulosolvens is a synonym for Acetivibrio cellulolyticus: emendation of the genus Acetivibrio. Int J Syst Evol Microbiol 36: pp. 314-316
    63. Bapteste, E, Moreira, D, Philippe, H (2003) Rampant horizontal gene transfer and phospho-donor change in the evolution of the phosphofructokinase. Gene 318: pp. 185-191 CrossRef
    64. Schut, GJ, Adams, MWW (2009) The iron-hydrogenase of Thermotoga maritima Utilizes Ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191: pp. 4451-4457 CrossRef
    65. Madden, R (1983) Isolation and characterization of Clostridium stercorarium sp. nov., cellulolytic thermophile. Int J Syst Bacteriol 33: pp. 837-840 CrossRef
    66. Fardeau, M, Ollivier, B, Garcia, J, Patel, B (2001) Transfer of Thermobacteroides leptospartum and Clostridium thermolacticum as Clostridium stercorarium subsp. leptospartum subsp. nov., comb. nov. and C. stercorarium subsp. thermolacticum subsp. nov., comb. nov. Int J Syst Evol Microbiol 51: pp. 1127-1131 CrossRef
  • 刊物主题:Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
  • 出版者:BioMed Central
  • ISSN:1471-2164
文摘
Background Growing interest in cellulolytic clostridia with potential for consolidated biofuels production is mitigated by low conversion of raw substrates to desired end products. Strategies to improve conversion are likely to benefit from emerging techniques to define molecular systems biology of these organisms. Clostridium stercorarium DSM8532T is an anaerobic thermophile with demonstrated high ethanol production on cellulose and hemicellulose. Although several lignocellulolytic enzymes in this organism have been well-characterized, details concerning carbohydrate transporters and central metabolism have not been described. Therefore, the goal of this study is to define an improved whole genome sequence (WGS) for this organism using in-depth molecular profiling by RNA-seq transcriptomics and tandem mass spectrometry-based proteomics. Results A paired-end Roche/454 WGS assembly was closed through application of an in silico algorithm designed to resolve repetitive sequence regions, resulting in a circular replicon with one gap and a region of 2 kilobases with 10 ambiguous bases. RNA-seq transcriptomics resulted in nearly complete coverage of the genome, identifying errors in homopolymer length attributable to 454 sequencing. Peptide sequences resulting from high-throughput tandem mass spectrometry of trypsin-digested protein extracts were mapped to 1,755 annotated proteins (68% of all protein-coding regions). Proteogenomic analysis confirmed the quality of annotation and improvement pipelines, identifying a missing gene and an alternative reading frame. Peptide coverage of genes hypothetically involved in substrate hydrolysis, transport and utilization confirmed multiple pathways for glycolysis, pyruvate conversion and recycling of intermediates. No sequences homologous to transaldolase, a central enzyme in the pentose phosphate pathway, were observed by any method, despite demonstrated growth of this organism on xylose and xylan hemicellulose. Conclusions Complementary omics techniques confirm the quality of genome sequence assembly, annotation and error-reporting. Nearly complete genome coverage by RNA-seq likely indicates background DNA in RNA extracts, however these preps resulted in WGS enhancement and transcriptome profiling in a single Illumina run. No detection of transaldolase by any method despite xylose utilization by this organism indicates an alternative pathway for sedoheptulose-7-phosphate degradation. This report combines next-generation omics techniques to elucidate previously undefined features of substrate transport and central metabolism for this organism and its potential for consolidated biofuels production from lignocellulose.

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