Sequence-based network completion reveals the integrality of missing reactions in metabolic networks

Journal of Biological Chemistry

Volumn 290, Issue 31, 2015, Pages 19197-19207

  Krumholz, Elias W ^a   Libourel, Igor G L ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENES;

GENOME-SCALE MODEL; IN NETWORKS; METABOLIC NETWORK; PREDICTIVE POWER; SYNTHETIC BIOLOGY;

METABOLISM;

ACYL CARRIER PROTEIN; GLOBALLY ORPHANED ENZYME; GLYCEROL TEICHOIC ACID; LOCALLY ORPHANED ENZYME; PEPTIDOGLYCAN; SPERMIDINE; TEICHOIC ACID; UNCLASSIFIED DRUG; UNCLASSIFIED ENZYME;

ACINETOBACTER BAYLYI; ALGORITHM; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENOME; BIOCHEMISTRY; BIOMASS PRODUCTION; CANONICAL GAP FILLING; CHEMICAL PARAMETERS; CONTROLLED STUDY; DATA PROCESSING; ENZYME ACTIVITY; ENZYME SEQUENCE SUPPORT; ERRONEOUS GAP FILLING REACTION; ESCHERICHIA COLI; GAP FILLING ALGORITHM; GENE ESSENTIALITY; GENE INACTIVATION; GENE LIBRARY; GENE REGULATORY NETWORK; GENE SEQUENCE; GENETIC DATABASE; GENETIC MODEL; GENETIC PARAMETERS; GENETIC PROCEDURES; GENOME SCALE DRAFT METABOLIC NETWORK; GENOME SCALE METABOLIC MODEL; INFORMATION PROCESSING; MINIMAL SEQUENCE SIMILARITY; MODEL SEED DATABASE; NONHUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL; PROCESS OPTIMIZATION; QUADRATIC PROGRAMMING; QUALITY CONTROL; SENSITIVITY ANALYSIS; SEQUENCE BASED NETWORK COMPLETION; SEQUENCE HOMOLOGY; STREPTOCOCCUS PNEUMONIAE; SYNTHETIC BIOLOGY; SYSTEM ANALYSIS; BACTERIAL GENE; DNA SEQUENCE; GENETICS; GENOMICS; METABOLISM; MOLECULAR GENETICS;

ESCHERICHIA COLI; GENES, BACTERIAL; GENOMICS; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE ANNOTATION; SEQUENCE ANALYSIS, DNA;

EID: 84940514861     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.634121     Document Type: Article

References (51)

1. Thiele, I., and Palsson, B. (2010) A protocol for generating a highquality genome-scale metabolic reconstruction. Nat. Protoc. 5, 93-121
2. Thiele, I., Fleming, R. M. T., Que, R., Bordbar, A., Diep, D., and Palsson, B. O. (2012) Multiscale modeling of metabolism and macromolecular synthesis in E. coli and its application to the evolution of codo n usage. PLoS One 7, e45635
3. Oberhardt, M. A., Palsson, B., and Papin, J. A. (2009) Applications of genome-scale metabolic reconstructions. Mol. Syst. Biol. 5, 320
4. Reed, J. L., Vo, T. D., Schilling, C. H., and Palsson, B. O. (2003) An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR). Genome Biol. 4, R54
5. Feist, A. M., Henry, C. S., Reed, J. L., Krummenacker, M., Joyce, A. R., Karp, P. D., Broadbelt, L. J., Hatzimanikatis, V., and Palsson, B. (2007) A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol. Syst. Biol. 3, 121
6. Orth, J. D., and Palsson, B. (2012) Gap-filling analysis of the iJO1366 Escherichia coli metabolic network reconstruction for discovery of metabolic functions. BMC Syst. Biol. 6, 30
7. Henry, C. S., Overbeek, R., Xia, F., Best, A. A., Glass, E., Gilbert, J., Larsen, P., Edwards, R., Disz, T., Meyer, F., Vonstein, V., Dejongh, M., Bartels, D., Desai, N., D'Souza, M., Devoid, S., Keegan, K. P., Olson, R., Wilke, A., Wilkening, J., and Stevens, R. L. (2011) Connecting genotype to phenotype in the era of high-throughput sequen cing. Biochim. Biophys. Acta. 1810, 967-977
8. Karr, J. R., Sanghvi, J. C., Macklin, D. N., Gutschow, M. V., Jacobs, J. M., Bolival, B., Jr., Assad-Garcia, N., Glass, J. I., and Covert, M. W. (2012) A whole-cell computational model predicts phenotype from genotype. Cell 150, 389-401
9. Reed, J. L. (2012) Shrinking the metabolic solution space using experimental datasets. PLoS Comput. Biol. 8, e1002662
10. Berestovsky, N., Zhou, W., Nagrath, D., and Nakhleh, L. (2013) Modeling integrated cellular machinery using hybrid Petri-Boolean networks. PLoS Comput. Biol. 9, e1003306
11. Thiele, I., Swainston, N., Fleming, R. M. T., Hoppe, A., Sahoo, S., Aurich, M. K., Haraldsdottir, H., Mo, M. L., Rolfsson, O., Stobbe, M. D., Thorleifsson, S. G., Agren, R., Bö lling, C., Bordel, S., Chavali, A. K., Dobson, P., Dunn, W. B., Endler, L., Hala, D., Hucka, M., Hull, D., Jameson, D., Jamshidi, N., Jonsson, J. J., Juty, N., Keating, S., Nookaew, I., Le Novère, N., Malys , N., Mazein, A., Papin, J. A., Price, N. D., Selkov, E., Sr., Sigurdsson, M. I., Simeonidis, E., Sonnenschein, N., Smallbone, K., Sorokin, A., Van Beek, J. H. G. M., Weichart, D., Goryanin, I., Nielsen, J., Westerhoff, H. V., Kell, D. B., Mendes , P., and Palsson, B. (2013) A community-driven global reconstruction of human metabolism. Nat. Biotechnol. 31, 419-425
12. Heavner, B. D., Smallbone, K., Barker, B., Mendes, P., and Walker, L. P. (2012) Yeast 5: An expanded reconstruction of the Saccharomyces cerevisiae metabolic network. BMC Syst. Biol. 6, 55
13. Dreyfuss J. M. Zucker J. D. Hood H. M. Ocasio L. R. Sachs M. S. Gala gan, J E.(2013) Reconstruction and validation of a genome-scale metabolic model for the filamentous fungus Neurospora crassa using FARM. PLoS Comput. Biol. 9 e1003126
14. Vitkin, E., and Shlomi, T. (2012) MIRAGE: A functional genomics-based approach for metabolic network model reconstruction and its application to cyanobacteria networks. Genome Biol. 13, R111
15. Henry, C. S., DeJongh, M., Best, A. A., Frybarger, P. M., Linsay, B., and Stevens, R. L. (2010) High-throughput generation, optimization and analysis of genome-scale metabolic models. Nat. Biotechnol. 28, 977-982
16. Feng, X., Xu, Y., Chen, Y., and Tang, Y. J. (2012) MicrobesFlux: A web platform for drafting metabolic models from the KEGG database. BMC Syst. Biol. 6, 94
17. Overbeek, R., Olson, R., Pusch, G. D., Olsen, G. J., Davis, J. J., Disz, T., Edwards, R. A., Gerdes, S., Parrello, B., Shukla, M., Vonstein, V., Wattam, A. R., Xia, F., and Stevens, R. (2014) The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res. 42, D206-D214
18. Aziz, R. K., Bartels, D., Best, A. A., DeJongh, M., Disz, T., Edwards, R. A., Formsma, K., Gerdes, S., Glass, E. M., Kubal, M., Meyer, F., Olsen, G. J., Olson, R., Osterman, A. L., Overbeek, R. A., McNeil, L. K., Paarmann, D., Paczian, T., Parrello, B., Pusch, G. D., Reich, C., Stevens, R., Vassieva, O., Vonstein, V., Wilke, A., and Zagnitko, O. (2008) The RAST Server: Rapid annotations using subsystems technology. BMC Genomics 9, 75
19. Konwar, K. M., Hanson, N. W., Pagé, A. P., and Hallam, S. J. (2013) MetaPathway s: A modular pipeline for constructing pathway/genome databases from environmental sequence information. BMC Bioinformatics 14, 202
20. Meyer, F., Paarmann, D., D'Souza, M., Olson, R., Glass, E. M., Kubal, M., Paczian, T., Rodriguez, A., Stevens, R., Wilke, A., Wilkening, J., and Edwards, R. A. (2008) The metagenomics RAST server: A public resource for the automatic phylogenetic and functional analysis of metagenomes.BMC Bioinformatics 9, 386
21. Reed, J. L., and Palsson, B. (2003) Thirteen years of building constraintbased in silico models of Escherichia coli. J. Bacteriol. 185, 2692-2699
22. Karp, P. D., Paley, S. M., Krummenacker, M., Latendresse, M., Dale, J. M., Lee, T. J., Kaipa, P., Gilham, F., Spaulding, A., Popescu, L., Altman, T., Paulsen, I., Keseler, I. M., and Casp i, R. (2010) Pathway Tools version 13.0: Integrated software for pathway/genome informatics and systems biology. Brief. Bioinform. 11, 40-79
23. Feist, A. M., and Palsson, B. (2010) The biomass objective function. Curr. Opin. Microbiol. 13, 344-349
24. Orth, J. D., and Palsson, B. (2010) Systematizing the generation of missing metabolic knowledge. Biotechnol. Bioeng. 107, 403-412
25. Satish Kumar, V., Dasika, M. S., and Maranas, C. D. (2007) Optimization based automated curation of metabolic reconstructions. BMC Bioinformatics 8, 212
26. Fleming, R. M. T., Thiele, I., and Nasheuer, H. P. (2009) Quantitative assignment of reaction directionality in constraint-based models of metabolism: Application to Escherichia coli. Biophys. Chem. 145, 47-56
27. Reed, J. L., Patel, T. R., Chen, K. H., Joyce, A. R., Applebee, M. K., Herring, C. D., Bui, O. T., Knight, E. M., Fong, S. S., and Palsson, B. (2006) Systems approach to refining genome annotatio n. Proc. Natl. Acad. Sci. U.S.A. 103, 17480-17484
28. Zomorrodi, A. R., Suthers, P. F., Ranganathan, S., and Maranas, C. D. (2012) Mathematical optimization applications in metabolic networks. Metab. Eng. 14, 672-686
29. Krumholz, E. W., Yang, H., Weisenhorn, P., Henry, C. S., and Libourel, I. G. L. (2012) Genome-wide metabolic network reconstruction of the picoalga Ostreococcus. J. Exp. Bot. 63, 2353-2362
30. Christian, N., May, P., Kempa, S., Handorf, T., and Ebenhöh, O. (2009) An integrative approach towards completing genome-scale metabolic networks. Mol. Biosyst. 5, 1889-1903
31. Benedict, M. N., Mundy, M. B., Henry, C. S., Chia, N., and Price, N. D. (2014) Likelihood-based gene annotations for gap filling and quality assessment in genome-scale metabolic models. PLoS Comput. Biol. 10, e1003882
32. Rolfsson, O., Palsson, B., and Thiele, I. (2011) The human metabolic reconstruction Recon 1 directs hypotheses of novel human metabolic functions. BMC Syst. Biol. 5, 155
33. RolfssonÓ., Paglia, G., Magnusdóttir, M., Palsson, B., and Thiele, I. (2013) Inferring the metabo lism of human orphan metabolites from their metabolic network context affirms human gluconokinase activity. Biochem. J. 449, 427-435
34. Aziz, R. K., Devoid, S., Disz, T., Edwards, R. A., Henry, C. S., Olsen, G. J., Olson, R., Overbeek, R., Parrello, B., Pusch, G. D., Stevens, R. L., Vonstein, V., and Xia, F. (2012) SEED servers: High-performance access to the SEED genomes, annotations, and metabolic models. PLoS One 7, e48053
35. Camacho C. Coulouris G. Avagyan V. Ma N. Papadopoulos J. Bealer K. Madden T. L. 2009 BLAST-: Architecture and applications. BMC Bioinformatics 10 421
36. Henikoff, S., and Henikoff, J. G. (1992) Amino acid substitution matrices from protein blocks. Proc. Natl. Acad. Sci. U.S.A. 89, 10915-10919
37. Altschul, S. F., Boguski, M. S., Gish, W., and Wootton, J. C. (1994) Issues in searching molecular sequence databases. Nat. Genet. 6, 119-129
38. Orth, J. D., Thiele, I., and Palsson, B. (2010) What is flu x balance analysis? Nat. Biotechnol. 28, 245-248
39. Schellenberger, J., Que, R., Fleming, R. M. T., Thiele, I., Orth, J. D., Feist, A. M., Zielinski, D. C., Bordbar, A., Lewis, N. E., Rahmanian, S., Kang, J., Hyduke, D. R., and Palsson, B. (2011) Quantitative prediction of cellular metabolism with constraint-based models: The COBRA Toolbox v2.0. Nat. Protoc. 6, 1290-1307
40. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K. A., Tomita, M., Wanner, B. L., and Mori, H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol. Syst. Biol. 2, 2006.0008
41. Durot, M., Le Fèvre, F., De Berardinis, V., Kreimeyer, A., Vallenet, D., Combe, C., Smidtas, S., Salanoubat, M., Weissenbach, J., and Schachter, V. (2008) Iterative reconstruction of a global metabolic model of Acinetobacter baylyi ADP1 using high-throughput growth phenotype and gene essentiality data. BMC Syst. Biol. 2, 85
42. Kobayashi, K., Ehrlich, S. D., Albertini, A., Amati, G., Andersen, K. K., Arnaud, M., Asai, K., Ashikaga, S., Aymerich, S., Bessieres, P., Boland, F., Brignell, S. C., Bron, S., Bunai, K., Chapuis, J., Christiansen, L. C., Danchin, A., Débarbouille, M., Dervyn, E., Deuerling, E., Devine, K., Devine, S. K., Dreesen, O., Errington, J., Fillinger, S., Foster, S. J., Fujita, Y., Galiz zi, A., Gardan, R., Eschevins, C., Fukushima, T., Haga, K., Harwood, C. R., Hecker, M., Hosoya, D., Hullo, M. F., Kakeshita, H., Karamata, D., Kasahara, Y., Kawamura, F., Koga, K., Koski, P., Kuw ana, R., Imamura, D., Ishimaru, M., Ishikawa, S., Ishio, I., Le Coq, D., Masson, A., Mauël C.Meima, R., Mellado, R. P., Moir, A., Moriya, S., Nagakawa, E., Nanamiya, H., Nakai, S., Nygaard, P., Ogura, M., Ohanan, T., O'Reilly, M., O'Rourke, M., Pragai, Z., Pooley, H. M., Rapoport, G., Rawlins, J. P., Rivas, L. A., Rivolta, C., Sadaie, A., Sadaie, Y., Sarvas, M., Sato, T., Saxild, H. H., Scanlan, E., Schumann, W., S eegers, J. F. M. L., Sekiguchi, J., Sekowska, A., Séror, S. J., Simon, M., Stragier, P., Studer, R., Takamatsu, H., Tanaka, T., Takeuchi, M., Thomaides, H. B., Vagner, V., Van Dijl, J. M., Watabe, K., Wipat, A., Yamamoto, H., Yamamoto, M., Yamamoto, Y., Ya mane, K., Yata, K., Yoshida, K., Yoshikawa, H., Zuber, U., and Ogasawara, N. (2003) Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. U.S.A. 100, 4678-4683
43. Thanassi, J. A., Hartman-Neumann, S. L., Dougherty, T. J., Dougherty, B. A., and Pucci, M. J. (2002) Identification of 113 conserved essential genes using a high-throughput gene disruption system in Streptococcus pneumoniae. Nucleic Acids Res. 30, 3152-3162
44. Yang, H., Krumholz, E. W., Brutinel, E. D., Palani, N. P., Sadowsky, M. J., Odlyzko, A. M., Gralnick, J. A., and Libourel, I. G. L. (2014) Genome-scale metabolic network validation of Shewanella o neidensis using transposon insertion frequency analysis. PLoS Comput. Biol. 10, e1003848
45. Jankowski, M. D., Henry, C. S., Broadbelt, L. J., and Hatzimanikatis, V. (2008) Group contribution method for thermodynamic analysis of complex metabolic networks. Biophys. J. 95, 1487-1499
46. Joyce, A. R., Reed, J. L., White, A., Edwards, R., Osterman, A., Baba, T., Mori, H., Lesely, S. A., Palsson, B., and Agarwalla, S. (2006) Experimental and computational assessment of conditionally essential genes in Escherichia coli. J. Bacteriol. 188, 8259-82571
47. Bi, H., Bai, Y., Cai, T., Zhuang, Y., Liang, X., Zhang, X., Liu, T., and Ma, Y. (2013) Engineered short branched-chai n acyl-CoA synthesis in E. coli and acylation of chloramphenicol to branched-chain derivatives. Appl. Microbiol. Biotechnol. 97, 10339-10348
48. Haase, I., Sarge, S., Illarionov, B., Laudert, D., Hohmann, H. P., Bacher, A., and Fischer, M. (2013) Enzymes from the haloacid dehalogenase (HAD) superfamily catalyse the elusive dephosphorylation step of riboflavin biosynthesis. ChemBioChem 14, 2272-2275
49. M azelis, M., Levin, B., and Mallinson, N. (1965) Decomposition of methyl methionine sulfonium salts by a bacterial enzyme. Biochim. Biophys. Acta 105, 106-114
50. Kanehisa, M., Goto, S., Sato, Y., Kawashima, M., Furumichi, M., and Tanabe, M. (2014) Data, information, knowledge and principle: BACK TO MEtabolism in KEGG. Nucleic Acids Res. 42, D199-D205
51. Caspi, R., Altman, T., Billington, R., Dreher, K., Foerster, H., Fulcher, C. A., Holland, T. A., Keseler, I. M., Kothari, A., Kubo, A., Krummenacker, M., Latendresse, M., Mueller, L. A., Ong, Q., Paley, S., Subhraveti, P., Weaver, D. S., Weerasinghe, D., Zhang, P., and Karp, P. D. (2014) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 42, D459-D471