A computational knowledge-base elucidates the response of Staphylococcus aureus to different media types

PLoS Computational Biology

Volumn 15, Issue 1, 2019, Pages

  Seif, Yara ^a   Monk, Jonathan M ^a   Mih, Nathan ^a   Tsunemoto, Hannah ^b   Poudel, Saugat ^a   Zuniga, Cristal ^a   Broddrick, Jared ^a   Zengler, Karsten ^a,c   Palsson, Bernhard O ^a,b,c  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOCHEMISTRY; GENES; KNOWLEDGE BASED SYSTEMS; METABOLISM; METABOLITES; PHYSIOLOGY; PROTEINS; THREE DIMENSIONAL COMPUTER GRAPHICS;

3-DIMENSIONAL PROTEIN STRUCTURES; CLASSIFIEDS; GENOME-SCALE MODEL; ITS SYSTEMS; MEDIA TYPES; METABOLIC CAPABILITIES; PROTEINS STRUCTURES; S. AUREUS; STAPHYLOCOCCUS AUREUS; SYSTEM LEVELS;

BIOSYNTHESIS;

GLUCOSE; MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; PURINE; STAPHYLOXANTHIN; UNCLASSIFIED DRUG;

AEROBIC FERMENTATION; AMINO ACID SYNTHESIS; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL METABOLISM; BACTERIAL STRAIN; BIOSYNTHESIS; CATABOLISM; CELL GROWTH; CONTROLLED STUDY; DNA BARCODING; DNA MICROARRAY; EXTRACELLULAR MATRIX; GENE CONTROL; GENE SEQUENCE; GENETIC MODEL; GENOMICS; KNOWLEDGE BASE; METABOLIC FLUX ANALYSIS; METABOLOMICS; MICROBIAL BIOMASS; MOLECULAR BIOLOGY; NONHUMAN; PHENOTYPE; PREDICTION; PROTEIN ANALYSIS; PROTEIN STRUCTURE; PROTEOMICS; PURINE SYNTHESIS; STAPHYLOCOCCUS AUREUS; THREE DIMENSIONAL IMAGING; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; TRANSPOSON; BIOLOGICAL MODEL; CULTURE MEDIUM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METABOLOME; PHARMACOLOGY; PHYSIOLOGY; PROCEDURES; SYSTEMS BIOLOGY;

CULTURE MEDIA; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; KNOWLEDGE BASES; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; METABOLOMICS; MODELS, BIOLOGICAL; STAPHYLOCOCCUS AUREUS; SYSTEMS BIOLOGY;

EID: 85059797530     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1006644     Document Type: Article

References (98)

1. Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, Carey RB, et al. Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med. 2006;355: 666-674. doi: 10.1056/NEJMoa055356 pmid: 16914702
2. Bancroft EA, Antimicrobial resistance: it's not just for hospitals. JAMA. 2007;298: 1803-1804. doi: 10.1001/jama.298.15.1803 pmid: 17940239
3. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, et al. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA. 2007;298: 1763-1771. doi: 10.1001/jama.298.15.1763 pmid: 17940231
4. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG, et al. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet. 2006;367: 731-739. doi: 10.1016/S0140-6736(06)68231-7 pmid: 16517273
5. Tattevin Pierre, Diep Binh An, Jula Michael, Perdreau-Remington Françoise, Methicillin-Resistant Staphylococcus aureus USA300 Clone in Long-Term Care Facility. Emerging Infectious Disease journal. 2009;15: 953.
6. Boswihi SS, Udo EE, Methicillin-resistant Staphylococcus aureus: An update on the epidemiology, treatment options and infection control. Current Medicine Research and Practice. Elsevier; 2018; Available: http://www.cmrp-journal.com/article/S2352-0817(17)30170-8/abstract
7. Lin L, Nonejuie P, Munguia J, Hollands A, Olson J, Dam Q, et al. Azithromycin Synergizes with Cationic Antimicrobial Peptides to Exert Bactericidal and Therapeutic Activity Against Highly Multidrug-Resistant Gram-Negative Bacterial Pathogens. EBioMedicine. 2015;2: 690-698. doi: 10.1016/j.ebiom.2015.05.021 pmid: 26288841
8. Ebrahim A, Brunk E, Tan J, O'Brien EJ, Kim D, Szubin R, et al. Multi-omic data integration enables discovery of hidden biological regularities. Nat Commun. 2016;7: 13091. doi: 10.1038/ncomms13091 pmid: 27782110
9. Hyduke DR, Lewis NE, Palsson BØ, Analysis of omics data with genome-scale models of metabolism. Mol Biosyst. 2013;9: 167-174. doi: 10.1039/c2mb25453k pmid: 23247105
10. O'Brien EJ, Monk JM, Palsson BO, Using Genome-scale Models to Predict Biological Capabilities. Cell. 2015;161: 971-987. doi: 10.1016/j.cell.2015.05.019 pmid: 26000478
11. Bosi E, Monk JM, Aziz RK, Fondi M, Nizet V, Palsson BØ, Comparative genome-scale modelling of Staphylococcus aureus strains identifies strain-specific metabolic capabilities linked to pathogenicity. Proc Natl Acad Sci U S A. 2016;113: E3801-9. doi: 10.1073/pnas.1523199113 pmid: 27286824
12. Heinemann M, Kümmel A, Ruinatscha R, Panke S, In silico genome-scale reconstruction and validation of the Staphylococcus aureus metabolic network. Biotechnol Bioeng. 2005;92: 850-864. doi: 10.1002/bit.20663 pmid: 16155945
13. Lee D-S, Burd H, Liu J, Almaas E, Wiest O, Barabási A-L, et al. Comparative genome-scale metabolic reconstruction and flux balance analysis of multiple Staphylococcus aureus genomes identify novel antimicrobial drug targets. J Bacteriol. 2009;191: 4015-4024. doi: 10.1128/JB.01743-08 pmid: 19376871
14. Becker SA, Palsson BØ, Genome-scale reconstruction of the metabolic network in Staphylococcus aureus N315: an initial draft to the two-dimensional annotation. BMC Microbiol. 2005;5: 8. doi: 10.1186/1471-2180-5-8 pmid: 15752426
15. Thiele I, Palsson BØ, A protocol for generating a high-quality genome-scale metabolic reconstruction. Nat Protoc. 2010;5: 93-121. doi: 10.1038/nprot.2009.203 pmid: 20057383
16. Fey PD, Endres JL, Yajjala VK, Widhelm TJ, Boissy RJ, Bose JL, et al. A genetic resource for rapid and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. MBio. 2013;4: e00537-12. doi: 10.1128/mBio.00537-12 pmid: 23404398
17. Somerville GA, Saïd-Salim B, Wickman JM, Raffel SJ, Kreiswirth BN, Musser JM, Correlation of acetate catabolism and growth yield in Staphylococcus aureus: implications for host-pathogen interactions. Infect Immun. 2003;71: 4724-4732. doi: 10.1128/IAI.71.8.4724-4732.2003 pmid: 12874354
18. Wakeman CA, Hammer ND, Stauff DL, Attia AS, Anzaldi LL, Dikalov SI, et al. Menaquinone biosynthesis potentiates haem toxicity in Staphylococcus aureus. Mol Microbiol. 2012;86: 1376-1392. doi: 10.1111/mmi.12063 pmid: 23043465
19. Fuller JR, Vitko NP, Perkowski EF, Scott E, Khatri D, Spontak JS, et al. Identification of a lactate-quinone oxidoreductase in Staphylococcus aureus that is essential for virulence. Front Cell Infect Microbiol. 2011;1: 19. doi: 10.3389/fcimb.2011.00019 pmid: 22919585
20. Sena FV, Batista AP, Catarino T, Brito JA, Archer M, Viertler M, et al. Type-II NADH:quinone oxidoreductase from Staphylococcus aureus has two distinct binding sites and is rate limited by quinone reduction. Mol Microbiol. 2015;98: 272-288. doi: 10.1111/mmi.13120 pmid: 26172206
21. Mayer S, Steffen W, Steuber J, Götz F, The Staphylococcus aureus NuoL-like protein MpsA contributes to the generation of membrane potential. J Bacteriol. 2015;197: 794-806. doi: 10.1128/JB.02127-14 pmid: 25448817
22. Hammer ND, Schurig-Briccio LA, Gerdes SY, Gennis RB, Skaar EP, CtaM Is Required for Menaquinol Oxidase aa3 Function in Staphylococcus aureus. MBio. 2016;7. doi: 10.1128/mBio.00823-16 pmid: 27406563
23. Fritzemeier CJ, Hartleb D, Szappanos B, Papp B, Lercher MJ, Erroneous energy-generating cycles in published genome scale metabolic networks: Identification and removal. PLoS Comput Biol. 2017;13: e1005494. doi: 10.1371/journal.pcbi.1005494 pmid: 28419089
24. Du Q, Wang H, Xie J, Thiamin (vitamin B1) biosynthesis and regulation: a rich source of antimicrobial drug targets?Int J Biol Sci. 2011;7: 41-52. pmid: 21234302
25. Hiron A, Borezée-Durant E, Piard J-C, Juillard V, Only one of four oligopeptide transport systems mediates nitrogen nutrition in Staphylococcus aureus. J Bacteriol. 2007;189: 5119-5129. doi: 10.1128/JB.00274-07 pmid: 17496096
26. Borezée-Durant E, Hiron A, Piard J-C, Juillard V, Dual role of the oligopeptide permease Opp3 during growth of Staphylococcus aureus in milk. Appl Environ Microbiol. 2009;75: 3355-3357. doi: 10.1128/AEM.02819-08 pmid: 19286789
27. Hiron A, Posteraro B, Carrière M, Remy L, Delporte C, La Sorda M, et al. A nickel ABC-transporter of Staphylococcus aureus is involved in urinary tract infection. Mol Microbiol. 2010;77: 1246-1260. doi: 10.1111/j.1365-2958.2010.07287.x pmid: 20662775
28. Remy L, Carrière M, Derré-Bobillot A, Martini C, Sanguinetti M, Borezée-Durant E, The Staphylococcus aureus Opp1 ABC transporter imports nickel and cobalt in zinc-depleted conditions and contributes to virulence. Mol Microbiol. 2013;87: 730-743. doi: 10.1111/mmi.12126 pmid: 23279021
29. Kaiser JC, Sen S, Sinha A, Wilkinson BJ, Heinrichs DE, The role of two branched-chain amino acid transporters in Staphylococcus aureus growth, membrane fatty acid composition and virulence. Mol Microbiol. 2016;102: 850-864. doi: 10.1111/mmi.13495 pmid: 27589208
30. Kehl-Fie TE, Zhang Y, Moore JL, Farrand AJ, Hood MI, Rathi S, et al. MntABC and MntH contribute to systemic Staphylococcus aureus infection by competing with calprotectin for nutrient manganese. Infect Immun. 2013;81: 3395-3405. doi: 10.1128/IAI.00420-13 pmid: 23817615
31. Ghssein G, Brutesco C, Ouerdane L, Fojcik C, Izaute A, Wang S, et al. Biosynthesis of a broad-spectrum nicotianamine-like metallophore in Staphylococcus aureus. Science. 2016;352: 1105-1109. doi: 10.1126/science.aaf1018 pmid: 27230378
32. Cotton JL, Tao J, Balibar CJ, Identification and characterization of the Staphylococcus aureus gene cluster coding for staphyloferrin A. Biochemistry. 2009;48: 1025-1035. doi: 10.1021/bi801844c pmid: 19138128
33. Cheung J, Beasley FC, Liu S, Lajoie GA, Heinrichs DE, Molecular characterization of staphyloferrin B biosynthesis in Staphylococcus aureus. Mol Microbiol. 2009;74: 594-608. doi: 10.1111/j.1365-2958.2009.06880.x pmid: 19775248
34. Friedman DB, Stauff DL, Pishchany G, Whitwell CW, Torres VJ, Skaar EP, Staphylococcus aureus redirects central metabolism to increase iron availability. PLoS Pathog. 2006;2: e87. doi: 10.1371/journal.ppat.0020087 pmid: 16933993
35. Ledala N, Zhang B, Seravalli J, Powers R, Somerville GA, Influence of iron and aeration on Staphylococcus aureus growth, metabolism, and transcription. J Bacteriol. 2014;196: 2178-2189. doi: 10.1128/JB.01475-14 pmid: 24706736
36. Kuhn S, Slavetinsky CJ, Peschel A, Synthesis and function of phospholipids in Staphylococcus aureus. Int J Med Microbiol. 2015;305: 196-202. doi: 10.1016/j.ijmm.2014.12.016 pmid: 25595024
37. Miller DJ, Jerga A, Rock CO, White SW, Analysis of the Staphylococcus aureus DgkB structure reveals a common catalytic mechanism for the soluble diacylglycerol kinases. Structure. 2008;16: 1036-1046. doi: 10.1016/j.str.2008.03.019 pmid: 18611377
38. Jorge AM, Schneider J, Unsleber S, Göhring N, Mayer C, Peschel A, Utilization of glycerophosphodiesters by Staphylococcus aureus. Mol Microbiol. 2017;103: 229-241. doi: 10.1111/mmi.13552 pmid: 27726204
39. Halsey CR, Lei S, Wax JK, Lehman MK, Nuxoll AS, Steinke L, et al. Amino Acid Catabolism in Staphylococcus aureus and the Function of Carbon Catabolite Repression. MBio. 2017;8. doi: 10.1128/mBio.01434-16 pmid: 28196956
40. Soutourina O, Poupel O, Coppée J-Y, Danchin A, Msadek T, Martin-Verstraete I, CymR, the master regulator of cysteine metabolism in Staphylococcus aureus, controls host sulphur source utilization and plays a role in biofilm formation. Mol Microbiol. 2009;73: 194-211. doi: 10.1111/j.1365-2958.2009.06760.x pmid: 19508281
41. Nuxoll AS, Halouska SM, Sadykov MR, Hanke ML, Bayles KW, Kielian T, et al. CcpA regulates arginine biosynthesis in Staphylococcus aureus through repression of proline catabolism. PLoS Pathog. 2012;8: e1003033. doi: 10.1371/journal.ppat.1003033 pmid: 23209408
42. Roberts CA, Al-Tameemi HM, Mashruwala AA, Rosario-Cruz Z, Chauhan U, Sause WE, et al. The Suf Iron-Sulfur Cluster Biosynthetic System Is Essential in Staphylococcus aureus, and Decreased Suf Function Results in Global Metabolic Defects and Reduced Survival in Human Neutrophils. Infect Immun. 2017;85. doi: 10.1128/IAI.00100-17 pmid: 28320837
43. Rosario-Cruz Z, Chahal HK, Mike LA, Skaar EP, Boyd JM, Bacillithiol has a role in Fe-S cluster biogenesis in Staphylococcus aureus. Mol Microbiol. 2015;98: 218-242. doi: 10.1111/mmi.13115 pmid: 26135358
44. Mashruwala AA, Pang YY, Rosario-Cruz Z, Chahal HK, Benson MA, Mike LA, et al. Nfu facilitates the maturation of iron-sulfur proteins and participates in virulence in Staphylococcus aureus. Mol Microbiol. 2015;95: 383-409. doi: 10.1111/mmi.12860 pmid: 25388433
45. Chang RL, Xie L, Xie L, Bourne PE, Palsson BØ, Drug off-target effects predicted using structural analysis in the context of a metabolic network model. PLoS Comput Biol. 2010;6: e1000938. doi: 10.1371/journal.pcbi.1000938 pmid: 20957118
46. Brunk E, Sahoo S, Zielinski DC, Altunkaya A, Dräger A, Mih N, et al. Recon3D enables a three-dimensional view of gene variation in human metabolism. Nat Biotechnol. 2018;36: 272-281. doi: 10.1038/nbt.4072 pmid: 29457794
47. Chang RL, Andrews K, Kim D, Li Z, Godzik A, Palsson BO, Structural systems biology evaluation of metabolic thermotolerance in Escherichia coli. Science. 2013;340: 1220-1223. doi: 10.1126/science.1234012 pmid: 23744946
48. Mih N, Brunk E, Chen K, Catoiu E, Sastry A, Kavvas E, et al. ssbio: A Python Framework for Structural Systems Biology [Internet]. bioRxiv. 2017. p. 165506. doi: 10.1101/165506
49. Bank RPD. RCSB PDB: Homepage [Internet]. [cited 13 Apr 2018]. Available: https://www.rcsb.org/
50. Feist AM, Palsson BO, The biomass objective function. Curr Opin Microbiol. 2010;13: 344-349. doi: 10.1016/j.mib.2010.03.003 pmid: 20430689
51. Lachance J-C, Monk JM, Lloyd CJ, Seif Y, Palsson BO, Rodrigue S, et al. BOFdat: generating biomass objective function stoichiometric coefficients from experimental data [Internet]. bioRxiv. 2018. p. 243881. doi: 10.1101/243881
52. Liebeke M, Meyer H, Donat S, Ohlsen K, Lalk M, A metabolomic view of Staphylococcus aureus and its ser/thr kinase and phosphatase deletion mutants: involvement in cell wall biosynthesis. Chem Biol. 2010;17: 820-830. doi: 10.1016/j.chembiol.2010.06.012 pmid: 20797611
53. Krismer B, Liebeke M, Janek D, Nega M, Rautenberg M, Hornig G, et al. Nutrient limitation governs Staphylococcus aureus metabolism and niche adaptation in the human nose. PLoS Pathog. 2014;10: e1003862. doi: 10.1371/journal.ppat.1003862 pmid: 24453967
54. Hussain M, Hastings JG, White PJ, A chemically defined medium for slime production by coagulase-negative staphylococci. J Med Microbiol. 1991;34: 143-147. doi: 10.1099/00222615-34-3-143 pmid: 2010904
55. Carvalho SM, de Jong A, Kloosterman TG, Kuipers OP, Saraiva LM, The Staphylococcus aureus α-Acetolactate Synthase ALS Confers Resistance to Nitrosative Stress. Front Microbiol. 2017;8: 1273. doi: 10.3389/fmicb.2017.01273 pmid: 28744267
56. Gertz S, Engelmann S, Schmid R, Ohlsen K, Hacker J, Hecker M, Regulation of sigmaB-dependent transcription of sigB and asp23 in two different Staphylococcus aureus strains. Mol Gen Genet. 1999;261: 558-566. pmid: 10323238
57. Neubauer H, Pantel I, Lindgren PE, Götz F, Characterization of the molybdate transport system ModABC of Staphylococcus carnosus. Arch Microbiol. 1999;172: 109-115. pmid: 10415172
58. Zheng W, Cai X, Xie M, Liang Y, Wang T, Li Z, Structure-Based Identification of a Potent Inhibitor Targeting Stp1-Mediated Virulence Regulation in Staphylococcus aureus. Cell Chem Biol. 2016;23: 1002-1013. doi: 10.1016/j.chembiol.2016.06.014 pmid: 27499528
59. Eyal Z, Matzov D, Krupkin M, Wekselman I, Paukner S, Zimmerman E, et al. Structural insights into species-specific features of the ribosome from the pathogen Staphylococcus aureus. Proc Natl Acad Sci U S A. 2015;112: E5805-14. doi: 10.1073/pnas.1517952112 pmid: 26464510
60. Hammer ND, Skaar EP, Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu Rev Microbiol. 2011;65: 129-147. doi: 10.1146/annurev-micro-090110-102851 pmid: 21639791
61. Knight BC, The nutrition of Staphylococcus aureus; nicotinic acid and vitamin B(1). Biochem J. 1937;31: 731-737. pmid: 16746392
62. Monk J, Palsson BO, Genetics. Predicting microbial growth. Science. 2014;344: 1448-1449. doi: 10.1126/science.1253388 pmid: 24970063
63. Bæk KT, Bowman L, Millership C, Dupont Søgaard M, Kaever V, Siljamäki P, et al. The Cell Wall Polymer Lipoteichoic Acid Becomes Nonessential in Staphylococcus aureus Cells Lacking the ClpX Chaperone. MBio. 2016;7. doi: 10.1128/mBio.01228-16 pmid: 27507828
64. D'Elia MA, Pereira MP, Chung YS, Zhao W, Chau A, Kenney TJ, et al. Lesions in teichoic acid biosynthesis in Staphylococcus aureus lead to a lethal gain of function in the otherwise dispensable pathway. J Bacteriol. 2006;188: 4183-4189. doi: 10.1128/JB.00197-06 pmid: 16740924
65. Bates DM, von Eiff C, McNamara PJ, Peters G, Yeaman MR, Bayer AS, et al. Staphylococcus aureus menD and hemB mutants are as infective as the parent strains, but the menadione biosynthetic mutant persists within the kidney. J Infect Dis. 2003;187: 1654-1661. doi: 10.1086/374642 pmid: 12721946
66. Lannergård J, von Eiff C, Sander G, Cordes T, Seggewiss J, Peters G, et al. Identification of the genetic basis for clinical menadione-auxotrophic small-colony variant isolates of Staphylococcus aureus. Antimicrob Agents Chemother. 2008;52: 4017-4022. doi: 10.1128/AAC.00668-08 pmid: 18779359
67. Bazaid AS, Forbes S, Humphreys GJ, Ledder RG, O'Cualain R, McBain AJ, Fatty Acid Supplementation Reverses the Small Colony Variant Phenotype in Triclosan-Adapted Staphylococcus aureus: Genetic, Proteomic and Phenotypic Analyses. Sci Rep. 2018;8: 3876. doi: 10.1038/s41598-018-21925-6 pmid: 29497096
68. Dean MA, Olsen RJ, Long SW, Rosato AE, Musser JM, Identification of point mutations in clinical Staphylococcus aureus strains that produce small-colony variants auxotrophic for menadione. Infect Immun. 2014;82: 1600-1605. doi: 10.1128/IAI.01487-13 pmid: 24452687
69. Goldenbaum PE, Keyser PD, White DC, Role of vitamin K2 in the organization and function of Staphylococcus aureua membranes. J Bacteriol. 1975;121: 442-449. pmid: 1112772
70. Monk JM, Lloyd CJ, Brunk E, Mih N, Sastry A, King Z, et al. iML1515, a knowledgebase that computes Escherichia coli traits. Nat Biotechnol. 2017;35: 904-908. doi: 10.1038/nbt.3956 pmid: 29020004
71. Lan L, Cheng A, Dunman PM, Missiakas D, He C, Golden pigment production and virulence gene expression are affected by metabolisms in Staphylococcus aureus. J Bacteriol. 2010;192: 3068-3077. doi: 10.1128/JB.00928-09 pmid: 20400547
72. Connolly J, Boldock E, Prince LR, Renshaw SA, Whyte MK, Foster SJ, Identification of Staphylococcus aureus Factors Required for Pathogenicity and Growth in Human Blood. Infect Immun. 2017;85. doi: 10.1128/IAI.00337-17 pmid: 28808156
73. Bilder P, Lightle S, Bainbridge G, Ohren J, Finzel B, Sun F, et al. The structure of the carboxyltransferase component of acetyl-coA carboxylase reveals a zinc-binding motif unique to the bacterial enzyme. Biochemistry. 2006;45: 1712-1722. doi: 10.1021/bi0520479 pmid: 16460018
74. Torres-Larios A, Sankaranarayanan R, Rees B, Dock-Bregeon AC, Moras D, Conformational movements and cooperativity upon amino acid, ATP and tRNA binding in threonyl-tRNA synthetase. J Mol Biol. 2003;331: 201-211. pmid: 12875846
75. Mehboob S, Mulhearn DC, Truong K, Johnson ME, Santarsiero BD, Structure of dihydroorotase from Bacillus anthracis at 2.6 resolution. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2010;66: 1432-1435. doi: 10.1107/S1744309110037085 pmid: 21045288
76. Appel CD, Feld GK, Wallace BD, Williams RS, Structure of the sirtuin-linked macrodomain SAV0325 from Staphylococcus aureus. Protein Sci. 2016;25: 1682-1691. doi: 10.1002/pro.2974 pmid: 27345688
77. Brown DC, Collins KD, Dihydroorotase from Escherichia coli. Substitution of Co (II) for the active site Zn (II). J Biol Chem. ASBMB; 1991;266: 1597-1604. pmid: 1671037
78. Irrthum A, Wehenkel L. Predicting gene essentiality from expression patterns in Escherichia coli. 2008; Available: http://orbi.ulg.ac.be/bitstream/2268/83052/1/essentiality_mlsb08.pdf
79. Halsey CR, Lei S, Wax JK, Lehman MK, Nuxoll AS, Steinke L, et al. Amino Acid Catabolism in Staphylococcus aureus and the Function of Carbon Catabolite Repression. MBio. 2017;8. doi: 10.1128/mBio.01434-16 pmid: 28196956
80. Han J, He L, Shi W, Xu X, Wang S, Zhang S, et al. Glycerol uptake is important for L-form formation and persistence in Staphylococcus aureus. PLoS One. 2014;9: e108325. doi: 10.1371/journal.pone.0108325 pmid: 25251561
81. Samant S, Lee H, Ghassemi M, Chen J, Cook JL, Mankin AS, et al. Nucleotide biosynthesis is critical for growth of bacteria in human blood. PLoS Pathog. 2008;4: e37. doi: 10.1371/journal.ppat.0040037 pmid: 18282099
82. Dunyach-Remy C, Ngba Essebe C, Sotto A, Lavigne J-P, Staphylococcus aureus Toxins and Diabetic Foot Ulcers: Role in Pathogenesis and Interest in Diagnosis. Toxins. 2016;8. doi: 10.3390/toxins8070209 pmid: 27399775
83. Vitko NP, Grosser MR, Khatri D, Lance TR, Richardson AR, Expanded Glucose Import Capability Affords Staphylococcus aureus Optimized Glycolytic Flux during Infection. MBio. 2016;7. doi: 10.1128/mBio.00296-16 pmid: 27329749
84. Vemuri GN, Altman E, Sangurdekar DP, Khodursky AB, Eiteman MA, Overflow metabolism in Escherichia coli during steady-state growth: transcriptional regulation and effect of the redox ratio. Appl Environ Microbiol. 2006;72: 3653-3661. doi: 10.1128/AEM.72.5.3653-3661.2006 pmid: 16672514
85. Wickersham M, Wachtel S, Wong Fok Lung T, Soong G, Jacquet R, Richardson A, et al. Metabolic Stress Drives Keratinocyte Defenses against Staphylococcus aureus Infection. Cell Rep. 2017;18: 2742-2751. doi: 10.1016/j.celrep.2017.02.055 pmid: 28297676
86. Sadykov MR, Olson ME, Halouska S, Zhu Y, Fey PD, Powers R, et al. Tricarboxylic acid cycle-dependent regulation of Staphylococcus epidermidis polysaccharide intercellular adhesin synthesis. J Bacteriol. 2008;190: 7621-7632. doi: 10.1128/JB.00806-08 pmid: 18820013
87. Orth JD, Fleming RMT, Palsson BØ, Reconstruction and Use of Microbial Metabolic Networks: the Core Escherichia coli Metabolic Model as an Educational Guide. EcoSal Plus. 2010;4. doi: 10.1128/ecosalplus.10.2.1 pmid: 26443778
88. Orth JD, Conrad TM, Na J, Lerman JA, Nam H, Feist AM, et al. A comprehensive genome-scale reconstruction of Escherichia coli metabolism—2011. Mol Syst Biol. 2011;7: 535. doi: 10.1038/msb.2011.65 pmid: 21988831
89. Ebrahim A, Lerman JA, Palsson BO, Hyduke DR, COBRApy: COnstraints-Based Reconstruction and Analysis for Python. BMC Syst Biol. 2013;7: 74. doi: 10.1186/1752-0509-7-74 pmid: 23927696
90. Nature Research: science journals, jobs, information and services [Internet]. 30 Nov 2017 [cited 6 Dec 2017]. Available: https://www.nature.com/articles/nprot.2009.20
91. King ZA, Lu J, Dräger A, Miller P, Federowicz S, Lerman JA, et al. BiGG Models: A platform for integrating, standardizing and sharing genome-scale models. Nucleic Acids Res. 2016;44: D515-22. doi: 10.1093/nar/gkv1049 pmid: 26476456
92. Boeckmann B, Bairoch A, Apweiler R, Blatter M-C, Estreicher A, Gasteiger E, et al. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 2003;31: 365-370. pmid: 12520024
93. Schmelling N, Reciprocal Best Hit BLAST v1 [Internet]. protocols.io. 2016. doi: 10.17504/protocols.io.grnbv5e
94. Fritzemeier CJ, Hartleb D, Szappanos B, Papp B, Lercher MJ, Erroneous energy-generating cycles in published genome scale metabolic networks: Identification and removal. PLoS Comput Biol. 2017;13: e1005494. doi: 10.1371/journal.pcbi.1005494 pmid: 28419089
95. Orth JD, Thiele I, Palsson BØ, What is flux balance analysis?Nat Biotechnol. 2010;28: 245-248. doi: 10.1038/nbt.1614 pmid: 20212490
96. Carvalho SM, de Jong A, Kloosterman TG, Kuipers OP, Saraiva LM, The Staphylococcus aureus α-Acetolactate Synthase ALS Confers Resistance to Nitrosative Stress. Front Microbiol. 2017;8: 1273. doi: 10.3389/fmicb.2017.01273 pmid: 28744267
97. Mladenova SR, Stein KR, Bartlett L, Sheppard K, Relaxed tRNA specificity of the Staphylococcus aureus aspartyl-tRNA synthetase enables RNA-dependent asparagine biosynthesis. FEBS Lett. 2014;588: 1808-1812. doi: 10.1016/j.febslet.2014.03.042 pmid: 24685427
98. Christian JH, Waltho JA, THE COMPOSITION OF STAPHYLOCOCCUS AUREUS IN RELATION TO THE WATER ACTIVITY OF THE GROWTH MEDIUM. J Gen Microbiol. 1964;35: 205-213. doi: 10.1099/00221287-35-2-205 pmid: 14179669