Genomewide landscape of gene–metabolome associations in Escherichia coli

Molecular Systems Biology

Volumn 13, Issue 1, 2017, Pages

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

^a ETH ZURICH   (Switzerland)

^b GLAXOSMITHKLINE   (Germany)

Author keywords

functional genomics; GWAS; interaction network; metabolism; metabolomics

Indexed keywords

ARTICLE; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE DELETION; GENE FUNCTION; GENE INTERACTION; GENE MAPPING; GENOME-WIDE ASSOCIATION STUDY; METABOLOME; NONHUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL; BACTERIAL GENOME; EPISTASIS; GENE REGULATORY NETWORK; GENETICS; METABOLISM; METABOLOMICS; PROCEDURES;

EPISTASIS, GENETIC; ESCHERICHIA COLI; GENE DELETION; GENE REGULATORY NETWORKS; GENOME, BACTERIAL; GENOME-WIDE ASSOCIATION STUDY; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS;

EID: 85010842085     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.15252/msb.20167150     Document Type: Article

References (34)

1. Andres Leon E, Ezkurdia I, Garcia B, Valencia A, Juan D (2009) EcID. A database for the inference of functional interactions in E. coli. Nucleic Acids Res 37: D629–D635
2. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008
3. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, Prinz J, St Onge RP, VanderSluis B, Makhnevych T, Vizeacoumar FJ, Alizadeh S, Bahr S, Brost RL, Chen Y, Cokol M et al (2010) The genetic landscape of a cell. Science 327: 425–431
4. Faith JJ, Hayete B, Thaden JT, Mogno I, Wierzbowski J, Cottarel G, Kasif S, Collins JJ, Gardner TS (2007) Large-scale mapping and validation of Escherichia coli transcriptional regulation from a compendium of expression profiles. PLoS Biol 5: e8
5. Feist AM, Herrgard MJ, Thiele I, Reed JL, Palsson BO (2009) Reconstruction of biochemical networks in microorganisms. Nat Rev Microbiol 7: 129–143
6. Fendt SM, Buescher JM, Rudroff F, Picotti P, Zamboni N, Sauer U (2010) Tradeoff between enzyme and metabolite efficiency maintains metabolic homeostasis upon perturbations in enzyme capacity. Mol Syst Biol 6: 356
7. Fuhrer T, Heer D, Begemann B, Zamboni N (2011) High-throughput, accurate mass metabolome profiling of cellular extracts by flow injection-time-of-flight mass spectrometry. Anal Chem 83: 7074–7080
8. Ghazalpour A, Bennett BJ, Shih D, Che N, Orozco L, Pan C, Hagopian R, He A, Kayne P, Yang WP, Kirchgessner T, Lusis AJ (2014) Genetic regulation of mouse liver metabolite levels. Mol Syst Biol 10: 730
9. Hanson AD, Pribat A, Waller JC, de Crecy-Lagard V (2010) ‘Unknown’ proteins and ‘orphan’ enzymes: the missing half of the engineering parts list - and how to find it. Biochem J 425: 1–11
10. Heinemann M, Sauer U (2010) Systems biology of microbial metabolism. Curr Opin Microbiol 13: 337–343
11. Hu P, Janga SC, Babu M, Diaz-Mejia JJ, Butland G, Yang W, Pogoutse O, Guo X, Phanse S, Wong P, Chandran S, Christopoulos C, Nazarians-Armavil A, Nasseri NK, Musso G, Ali M, Nazemof N, Eroukova V, Golshani A, Paccanaro A et al (2009) Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins. PLoS Biol 7: e96
12. Ishii N, Nakahigashi K, Baba T, Robert M, Soga T, Kanai A, Hirasawa T, Naba M, Hirai K, Hoque A, Ho PY, Kakazu Y, Sugawara K, Igarashi S, Harada S, Masuda T, Sugiyama N, Togashi T, Hasegawa M, Takai Y et al (2007) Multiple high-throughput analyses monitor the response of E. coli to perturbations. Science 316: 593–597
13. Jaroszewski L, Li Z, Krishna SS, Bakolitsa C, Wooley J, Deacon AM, Wilson IA, Godzik A (2009) Exploration of uncharted regions of the protein universe. PLoS Biol 7: e1000205
14. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40: D109–D114
15. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, Mori H (2005) 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
16. Link H, Kochanowski K, Sauer U (2013) Systematic identification of allosteric protein-metabolite interactions that control enzyme activity in vivo. Nat Biotechnol 31: 357–361
17. McNeil MB, Clulow JS, Wilf NM, Salmond GP, Fineran PC (2012) SdhE is a conserved protein required for flavinylation of succinate dehydrogenase in bacteria. J Biol Chem 287: 18418–18428
18. McNeil MB, Iglesias-Cans MC, Clulow JS, Fineran PC (2013) YgfX (CptA) is a multimeric membrane protein that interacts with the succinate dehydrogenase assembly factor SdhE (YgfY). Microbiology 159: 1352–1365
19. McNeil MB, Hampton HG, Hards KJ, Watson BN, Cook GM, Fineran PC (2014) The succinate dehydrogenase assembly factor, SdhE, is required for the flavinylation and activation of fumarate reductase in bacteria. FEBS Lett 588: 414–421
20. Merritt ME, Donaldson JR (2009) Effect of bile salts on the DNA and membrane integrity of enteric bacteria. J Med Microbiol 58: 1533–1541
21. Nichols RJ, Sen S, Choo YJ, Beltrao P, Zietek M, Chaba R, Lee S, Kazmierczak KM, Lee KJ, Wong A, Shales M, Lovett S, Winkler ME, Krogan NJ, Typas A, Gross CA (2011) Phenotypic landscape of a bacterial cell. Cell 144: 143–156
22. Nozaki S, Webb ME, Niki H (2012) An activator for pyruvoyl-dependent l-aspartate alpha-decarboxylase is conserved in a small group of the gamma-proteobacteria including Escherichia coli. Microbiologyopen 1: 298–310
23. Orth JD, Conrad TM, Na J, Lerman JA, Nam H, Feist AM, Palsson BO (2011) A comprehensive genome-scale reconstruction of Escherichia coli metabolism–2011. Mol Syst Biol 7: 535
24. Reizer J, Reizer A, Saier MH Jr (1994) A functional superfamily of sodium/solute symporters. Biochim Biophys Acta 1197: 133–166
25. Salgado H, Peralta-Gil M, Gama-Castro S, Santos-Zavaleta A, Muniz-Rascado L, Garcia-Sotelo JS, Weiss V, Solano-Lira H, Martinez-Flores I, Medina-Rivera A, Salgado-Osorio G, Alquicira-Hernandez S, Alquicira-Hernandez K, Lopez-Fuentes A, Porron-Sotelo L, Huerta AM, Bonavides-Martinez C, Balderas-Martinez YI, Pannier L, Olvera M et al (2013) RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more. Nucleic Acids Res 41: D203–D213
26. Sevin DC, Sauer U (2014) Ubiquinone accumulation improves osmotic-stress tolerance in Escherichia coli. Nat Chem Biol 10: 266–272
27. Sevin DC, Kuehne A, Zamboni N, Sauer U (2015) Biological insights through nontargeted metabolomics. Curr Opin Biotechnol 34: 1–8
28. Shin SY, Fauman EB, Petersen AK, Krumsiek J, Santos R, Huang J, Arnold M, Erte I, Forgetta V, Yang TP, Walter K, Menni C, Chen L, Vasquez L, Valdes AM, Hyde CL, Wang V, Ziemek D, Roberts P, Xi L et al (2014) An atlas of genetic influences on human blood metabolites. Nat Genet 46: 543–550
29. Stuecker TN, Hodge KM, Escalante-Semerena JC (2012) The missing link in coenzyme A biosynthesis: PanM (formerly YhhK), a yeast GCN5 acetyltransferase homologue triggers aspartate decarboxylase (PanD) maturation in Salmonella enterica. Mol Microbiol 84: 608–619
30. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J, Bork P, Jensen LJ, von Mering C (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39: D561–D568
31. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41
32. Varghese S, Tang Y, Imlay JA (2003) Contrasting sensitivities of Escherichia coli aconitases A and B to oxidation and iron depletion. J Bacteriol 185: 221–230
33. van Wageningen S, Kemmeren P, Lijnzaad P, Margaritis T, Benschop JJ, de Castro IJ, van Leenen D, Groot Koerkamp MJ, Ko CW, Miles AJ, Brabers N, Brok MO, Lenstra TL, Fiedler D, Fokkens L, Aldecoa R, Apweiler E, Taliadouros V, Sameith K, van de Pasch LA et al (2010) Functional overlap and regulatory links shape genetic interactions between signaling pathways. Cell 143: 991–1004
34. Wang K, Li M, Hakonarson H (2010) Analysing biological pathways in genome-wide association studies. Nat Rev Genet 11: 843–854