Nontargeted in vitro metabolomics for high-throughput identification of novel enzymes in Escherichia coli

Nature Methods

Volumn 14, Issue 2, 2017, Pages 187-194

  Sévin, Daniel C ^a,b,c   Fuhrer, Tobias ^a   Zamboni, Nicola ^a   Sauer, Uwe ^a  

^a ETH ZURICH   (Switzerland)

^b Life Science Zurich   (Switzerland)

^c GLAXOSMITHKLINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; ESCHERICHIA COLI PROTEIN; GLUCOSE; NUCLEOSIDE; ENZYME;

ACCURACY; AEROBIC FERMENTATION; ARTICLE; CATALYSIS; CELL ASSAY; CELL LYSATE; CHEMOMETRICS; CONTROLLED STUDY; DELETION MUTANT; ENZYME ACTIVITY; ENZYME ASSAY; ESCHERICHIA COLI; HOMEOSTASIS; IN VITRO STUDY; MASS SPECTROMETRY; METABOLOME; METABOLOMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PURIFICATION; REACTION ANALYSIS; SUBSTRATE CONCENTRATION; BATCH CELL CULTURE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SCREENING; ISOLATION AND PURIFICATION; METABOLISM; PROCEDURES; REPRODUCIBILITY;

BATCH CELL CULTURE TECHNIQUES; ENZYMES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HIGH-THROUGHPUT SCREENING ASSAYS; MASS SPECTROMETRY; METABOLOMICS; REPRODUCIBILITY OF RESULTS;

EID: 85004191344     PISSN: 15487091     EISSN: 15487105     Source Type: Journal    
DOI: 10.1038/nmeth.4103     Document Type: Article

References (51)

1. Hanson, A.D., Pribat, A., Waller, J.C. & de Crécy-Lagard, V. 'Unknown' proteins and 'orphan' enzymes: the missing half of the engineering parts list-and how to find it. Biochem. J. 425, 1-11 (2009).
2. Galperin, M.Y. & Koonin, E.V. 'Conserved hypothetical' proteins: prioritization of targets for experimental study. Nucleic Acids Res. 32, 5452-5463 (2004).
3. Jaroszewski, L. et al. Exploration of uncharted regions of the protein universe. PLoS Biol. 7, e1000205 (2009).
4. Sorokina, M., Stam, M., Médigue, C., Lespinet, O. & Vallenet, D. Profiling the orphan enzymes. Biol. Direct 9, 10 (2014).
5. Chen, L. & Vitkup, D. Distribution of orphan metabolic activities. Trends Biotechnol. 25, 343-348 (2007).
6. Tian, W. & Skolnick, J. How well is enzyme function conserved as a function of pairwise sequence identity? J. Mol. Biol. 333, 863-882 (2003).
7. Bork, P. Powers and pitfalls in sequence analysis: the 70% hurdle. Genome Res. 10, 398-400 (2000).
8. Blaby-Haas, C.E. & de Crécy-Lagard, V. Mining high-throughput experimental data to link gene and function. Trends Biotechnol. 29, 174-182 (2011).
9. Galperin, M.Y. Conserved 'hypothetical' proteins: new hints and new puzzles. Comp. Funct. Genomics 2, 14-18 (2001).
10. Tipton, K. & Boyce, S. Nomenclature committee of the international union of biochemistry and molecular biology (NC-IUBMB), Enzyme Supplement 5 (1999). Eur. J. Biochem. 264, 610-650 (1999).
11. Pouliot, Y. & Karp, P.D. A survey of orphan enzyme activities. BMC Bioinformatics 8, 244 (2007).
12. Shearer, A.G., Altman, T. & Rhee, C.D. Finding sequences for over 270 orphan enzymes. PLoS One 9, e97250 (2014).
13. Lespinet, O. Orphan enzymes? Science 307, 42 (2005).
14. Sévin, D.C., Kuehne, A., Zamboni, N. & Sauer, U. Biological insights through nontargeted metabolomics. Curr. Opin. Biotechnol. 34, 1-8 (2015).
15. Feist, A.M., Herrgård, M.J., Thiele, I., Reed, J.L. & Palsson, B.Ø. Reconstruction of biochemical networks in microorganisms. Nat. Rev. Microbiol. 7, 129-143 (2009).
16. Nam, H. et al. Network context and selection in the evolution to enzyme specificity. Science 337, 1101-1104 (2012).
17. Kuznetsova, E. et al. Enzyme genomics: application of general enzymatic screens to discover new enzymes. FEMS Microbiol. Rev. 29, 263-279 (2005).
18. Prosser, G.A., Larrouy-Maumus, G. & de Carvalho, L.P. Metabolomic strategies for the identification of new enzyme functions and metabolic pathways. EMBO Rep. 15, 657-669 (2014).
19. Lee, D., Redfern, O. & Orengo, C. Predicting protein function from sequence and structure. Nat. Rev. Mol. Cell Biol. 8, 995-1005 (2007).
20. Plata, G., Fuhrer, T., Hsiao, T.-L., Sauer, U. & Vitkup, D. Global probabilistic annotation of metabolic networks enables enzyme discovery. Nat. Chem. Biol. 8, 848-854 (2012).
21. Zhao, S. et al. Discovery of new enzymes and metabolic pathways by using structure and genome context. Nature 502, 698-702 (2013).
22. Saito, N. et al. Metabolite profiling reveals YihU as a novel hydroxybutyrate dehydrogenase for alternative succinic semialdehyde metabolism in Escherichia coli. J. Biol. Chem. 284, 16442-16451 (2009).
23. Notebaart, R.A. et al. Network-level architecture and the evolutionary potential of underground metabolism. Proc. Natl. Acad. Sci. USA 111, 11762-11767 (2014).
24. Guzmán, G.I. et al. Model-driven discovery of underground metabolic functions in Escherichia coli. Proc. Natl. Acad. Sci. USA 112, 929-934 (2014).
25. Coelho, P.S. et al. A serine-substituted P450 catalyzes highly efficient carbene transfer to olefins in vivo. Nat. Chem. Biol. 9, 485-487 (2013).
26. Saito, N. et al. Metabolomics approach for enzyme discovery. J. Proteome Res. 5, 1979-1987 (2006).
27. Kuznetsova, E. et al. Genome-wide analysis of substrate specificities of the Escherichia coli haloacid dehalogenase-like phosphatase family. J. Biol. Chem. 281, 36149-36161 (2006).
28. Bennett, B.D. et al. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 5, 593-599 (2009).
29. Fuhrer, T., Heer, D., Begemann, B. & Zamboni, N. High-throughput, accurate mass metabolome profiling of cellular extracts by flow injection-time-of-flight mass spectrometry. Anal. Chem. 83, 7074-7080 (2011).
30. Kanehisa, M. et al. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 42, D199-D205 (2014).
31. Xu, Y.F., Lu, W. & Rabinowitz, J.D. Avoiding misannotation of in-source fragmentation products as cellular metabolites in liquid chromatography-mass spectrometry-based metabolomics. Anal. Chem. 87, 2273-2281 (2015).
32. Kitagawa, M. et al. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 12, 291-299 (2005).
33. Hattori, M., Okuno, Y., Goto, S. & Kanehisa, M. Development of a chemical structure comparison method for integrated analysis of chemical and genomic information in the metabolic pathways. J. Am. Chem. Soc. 125, 11853-11865 (2003).
34. Hattori, M., Tanaka, N., Kanehisa, M. & Goto, S. SIMCOMP/SUBCOMP: chemical structure search servers for network analyses. Nucleic Acids Res. 38, W652-W656 (2010).
35. da Silva, R.R., Dorrestein, P.C. & Quinn, R.A. Illuminating the dark matter in metabolomics. Proc. Natl. Acad. Sci. USA 112, 12549-12550 (2015).
36. Yamamoto, N. et al. Update on the Keio collection of Escherichia coli single-gene deletion mutants. Mol. Syst. Biol. 5, 335 (2009).
37. Struys, E.A. et al. Mutations in the D-2-hydroxyglutarate dehydrogenase gene cause D-2-hydroxyglutaric aciduria. Am. J. Hum. Genet. 76, 358-360 (2005).
38. Dang, L. et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462, 739-744 (2009).
39. Linster, C.L., Van Schaftingen, E. & Hanson, A.D. Metabolite damage and its repair or pre-emption. Nat. Chem. Biol. 9, 72-80 (2013).
40. Amend, J.P. & Shock, E.L. Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and bacteria. FEMS Microbiol. Rev. 25, 175-243 (2001).
41. Khersonsky, O. & Tawfik, D.S. Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu. Rev. Biochem. 79, 471-505 (2010).
42. Nobeli, I., Favia, A.D. & Thornton, J.M. Protein promiscuity and its implications for biotechnology. Nat. Biotechnol. 27, 157-167 (2009).
43. Fuhrer, T. & Zamboni, N. High-throughput discovery metabolomics. Curr. Opin. Biotechnol. 31, 73-78 (2015).
44. Dunn, W.B. et al. Mass appeal: metabolite identification in mass spectrometry-focused untargeted metabolomics. Metabolomics 9, 44-66 (2013).
45. Li, L. et al. MyCompoundID: using an evidence-based metabolome library for metabolite identification. Anal. Chem. 85, 3401-3408 (2013).
46. Nichols, R.J. et al. Phenotypic landscape of a bacterial cell. Cell 144, 143-156 (2011).
47. Lorenz, P. & Eck, J. Metagenomics and industrial applications. Nat. Rev. Microbiol. 3, 510-516 (2005).
48. Figge, R., Barbier, G. & Bestel-Corre, G. Production of N-acylated sulphur-containing amino acids with microorganisms having enhanced N-acyltransferase enzymatic activity. US patent US20100047880 A1 (2010).
49. Zor, T. & Selinger, Z. Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies. Anal. Biochem. 236, 302-308 (1996).
50. Riesenberg, D. et al. High cell density cultivation of Escherichia coli at controlled specific growth rate. J. Biotechnol. 20, 17-27 (1991).
51. Kashket, E.R. Effects of aerobiosis and nitrogen source on the proton motive force in growing Escherichia coli and Klebsiella pneumoniae cells. J. Bacteriol. 146, 377-384 (1981).