Metabolic constraints on the evolution of antibiotic resistance

Molecular Systems Biology

Volumn 13, Issue 3, 2017, Pages

  Zampieri, Mattia ^a   Enke, Tim ^a   Chubukov, Victor ^a   Ricci, Vito ^b   Piddock, Laura ^b   Sauer, Uwe ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

antibiotic resistance; constraint based modeling; efflux pump; evolution; metabolism

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; CARBON; CHLORAMPHENICOL; FOSFOMYCIN; GLUCOSE; NORFLOXACIN; PENICILLIN BINDING PROTEIN; RNA POLYMERASE; BACTERIAL DNA;

ADAPTATION; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; CARBON METABOLISM; CARBON SOURCE; ENERGY METABOLISM; ESCHERICHIA COLI; GENE OVEREXPRESSION; GENOME ANALYSIS; GLUCONEOGENESIS; GLYCOLYSIS; METABOLOME; MOLECULAR EVOLUTION; NONHUMAN; PENICILLIN RESISTANCE; POPULATION; PRIORITY JOURNAL; SEQUENCE ANALYSIS; DNA SEQUENCE; DRUG EFFECTS; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLOMICS; PROCEDURES;

AMPICILLIN; BIOLOGICAL EVOLUTION; DNA, BACTERIAL; DRUG RESISTANCE, MICROBIAL; ENERGY METABOLISM; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GLUCONEOGENESIS; GLYCOLYSIS; METABOLOMICS; SEQUENCE ANALYSIS, DNA;

EID: 85016250410     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.15252/msb.20167028     Document Type: Article

References (56)

1. Auriol C, Bestel-Corre G, Claude J-B, Soucaille P, Meynial-Salles I (2011) Stress-induced evolution of Escherichia coli points to original concepts in respiratory cofactor selectivity. Proc Natl Acad Sci USA 108: 1278–1283
2. Björkman J, Nagaev I, Berg OG, Hughes D, Andersson DI (2000) Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 287: 1479–1482
3. Blair JMA, Bavro VN, Ricci V, Modi N, Cacciotto P, Kleinekathöfer U, Ruggerone P, Vargiu AV, Baylay AJ, Smith HE, Brandon Y, Galloway D, Piddock LJV (2015a) AcrB drug-binding pocket substitution confers clinically relevant resistance and altered substrate specificity. Proc Natl Acad Sci USA 112: 3511–3516
4. Blair JMA, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJV (2015b) Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol 13: 42–51
5. Boer VM, Crutchfield CA, Bradley PH, Botstein D, Rabinowitz JD (2010) Growth-limiting intracellular metabolites in yeast growing under diverse nutrient limitations. Mol Biol Cell 21: 198–211
6. Cheng AA, Ding H, Lu TK (2014) Enhanced killing of antibiotic-resistant bacteria enabled by massively parallel combinatorial genetics. Proc Natl Acad Sci USA 111: 12462–12467
7. Chubukov V, Uhr M, Le Chat L, Kleijn RJ, Jules M, Link H, Aymerich S, Stelling J, Sauer U (2013) Transcriptional regulation is insufficient to explain substrate-induced flux changes in Bacillus subtilis. Mol Syst Biol 9: 709
8. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6: 80–92
9. Claudi B, Spröte P, Chirkova A, Personnic N, Zankl J, Schürmann N, Schmidt A, Bumann D (2014) Phenotypic variation of salmonella in host tissues delays eradication by antimicrobial chemotherapy. Cell 158: 722–733
10. Covert MW, Knight EM, Reed JL, Herrgard MJ, Palsson BO (2004) Integrating high-throughput and computational data elucidates bacterial networks. Nature 429: 92–96
11. Dahlberg C, Chao L (2003) Amelioration of the cost of conjugative plasmid carriage in Eschericha coli K12. Genetics 165: 1641–1649
12. Fendt S-M, 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
13. Fieller EC, Hartley HO, Pearson ES (1957) Tests for rank correlation coefficients. I. Biometrika 44: 470–481
14. Fong SS, Palsson BØ (2004) Metabolic gene–deletion strains of Escherichia coli evolve to computationally predicted growth phenotypes. Nat Genet 36: 1056–1058
15. Foti JJ, Devadoss B, Winkler JA, Collins JJ, Walker GC (2012) Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science 336: 315–319
16. 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
17. Gardete S, Ludovice AM, Sobral RG, Filipe SR, Lencastre H, Tomasz A (2004) Role of murE in the expression of β-lactam antibiotic resistance in Staphylococcus aureus. J Bacteriol 186: 1705–1713
18. Gerosa L, Haverkorn van Rijsewijk BRB, Christodoulou D, Kochanowski K, Schmidt TSB, Noor E, Sauer U (2015) Pseudo-transition analysis identifies the key regulators of dynamic metabolic adaptations from steady-state data. Cell Syst 1: 270–282
19. Gilbert P, Collier PJ, Brown MR (1990) Influence of growth rate on susceptibility to antimicrobial agents: biofilms, cell cycle, dormancy, and stringent response. Antimicrob Agents Chemother 34: 1865–1868
20. Gisin J, Schneider A, Nägele B, Borisova M, Mayer C (2013) A cell wall recycling shortcut that bypasses peptidoglycan de novo biosynthesis. Nat Chem Biol 9: 491–493
21. Gonzales PR, Pesesky MW, Bouley R, Ballard A, Biddy BA, Suckow MA, Wolter WR, Schroeder VA, Burnham C-AD, Mobashery S, Chang M, Dantas G (2015) Synergistic, collaterally sensitive β-lactam combinations suppress resistance in MRSA. Nat Chem Biol 11: 855–861
22. Hoffman LR, Richardson AR, Houston LS, Kulasekara HD, Martens-Habbena W, Klausen M, Burns JL, Stahl DA, Hassett DJ, Fang FC, Miller SI (2010) Nutrient availability as a mechanism for selection of antibiotic tolerant Pseudomonas aeruginosa within the CF airway. PLoS Pathog 6: e1000712
23. Hui S, Silverman JM, Chen SS, Erickson DW, Basan M, Wang J, Hwa T, Williamson JR (2015) Quantitative proteomic analysis reveals a simple strategy of global resource allocation in bacteria. Mol Syst Biol 11: 784
24. King T, Seeto S, Ferenci T (2006) Genotype-by-environment interactions influencing the emergence of rpoS mutations in Escherichia coli populations. Genetics 172: 2071–2079
25. van Klinken JB, Willems van Dijk K (2016) FluxModeCalculator: an efficient tool for large-scale flux mode computation. Bioinformatics 32: 1265–1266
26. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359
27. Lázár V, Pal Singh G, Spohn R, Nagy I, Horváth B, Hrtyan M, Busa-Fekete R, Bogos B, Méhi O, Csörgő B, Pósfai G, Fekete G, Szappanos B, Kégl B, Papp B, Pál C (2013) Bacterial evolution of antibiotic hypersensitivity. Mol Syst Biol 9: 700
28. Levin BR, Lipsitch M, Perrot V, Schrag S, Antia R, Simonsen L, Walker NM, Stewart FM (1997) The population genetics of antibiotic resistance. Clin Infect Dis Off Publ Infect Dis Soc Am 24(Suppl. 1): S9–S16
29. Lewis NE, Hixson KK, Conrad TM, Lerman JA, Charusanti P, Polpitiya AD, Adkins JN, Schramm G, Purvine SO, Lopez-Ferrer D, Weitz KK, Eils R, König R, Smith RD, Palsson BØ (2010) Omic data from evolved E. coli are consistent with computed optimal growth from genome-scale models. Mol Syst Biol 6: 390
30. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079
31. Li G-W, Burkhardt D, Gross C, Weissman JS (2014) Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157: 624–635
32. Lindsey HA, Gallie J, Taylor S, Kerr B (2013) Evolutionary rescue from extinction is contingent on a lower rate of environmental change. Nature 494: 463–467
33. Luria SE, Delbrück M (1943) Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28: 491–511
34. van der Maaten L, Hinton G (2008) Visualizing data using t-SNE. J Mach Learn Res 9: 2579–2605
35. Marciano DC, Karkouti OY, Palzkill T (2007) A fitness cost associated with the antibiotic resistance enzyme SME-1 β-lactamase. Genetics 176: 2381–2392
36. Marcusson LL, Frimodt-Møller N, Hughes D (2009) Interplay in the selection of fluoroquinolone resistance and bacterial fitness. PLoS Pathog 5: e1000541
37. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297–1303
38. Melnyk AH, Wong A, Kassen R (2015) The fitness costs of antibiotic resistance mutations. Evol Appl 8: 273–283
39. 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
40. Oh M-K, Rohlin L, Kao KC, Liao JC (2002) Global expression profiling of acetate-grown Escherichia coli. J Biol Chem 277: 13175–13183
41. Orth JD, Conrad TM, Na J, Lerman JA, Nam H, Feist AM, Palsson BØ (2011) A comprehensive genome-scale reconstruction of Escherichia coli metabolism–2011. Mol Syst Biol 7: 535
42. Pál C, Papp B, Lercher MJ, Csermely P, Oliver SG, Hurst LD (2006) Chance and necessity in the evolution of minimal metabolic networks. Nature 440: 667–670
43. Palmer AC, Kishony R (2013) Understanding, predicting and manipulating the genotypic evolution of antibiotic resistance. Nat Rev Genet 14: 243–248
44. Palmer AC, Kishony R (2014) Opposing effects of target overexpression reveal drug mechanisms. Nat Commun 5: 4296
45. Reznik E, Mehta P, Segrè D (2013) Flux imbalance analysis and the sensitivity of cellular growth to changes in metabolite pools. PLoS Comput Biol 9: e1003195
46. Schuetz R, Kuepfer L, Sauer U (2007) Systematic evaluation of objective functions for predicting intracellular fluxes in Escherichia coli. Mol Syst Biol 3: 119
47. Schuetz R, Zamboni N, Zampieri M, Heinemann M, Sauer U (2012) Multidimensional optimality of microbial metabolism. Science 336: 601–604
48. Schuster S, Hilgetag C (1994) On elementary flux modes in biochemical reaction systems at steady state. J Biol Syst 02: 165–182
49. Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc Ser B 64: 479–498
50. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102: 15545–15550
51. Testerman TL, Conn PB, Mobley HLT, McGee DJ (2006) Nutritional requirements and antibiotic resistance patterns of Helicobacter species in chemically defined media. J Clin Microbiol 44: 1650–1658
52. Toprak E, Veres A, Michel J-B, Chait R, Hartl DL, Kishony R (2012) Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nat Genet 44: 101–105
53. Villagra NA, Fuentes JA, Jofré MR, Hidalgo AA, García P, Mora GC (2012) The carbon source influences the efflux pump-mediated antimicrobial resistance in clinically important Gram-negative bacteria. J Antimicrob Chemother 67: 921–927
54. Wagner S, Baars L, Ytterberg AJ, Klussmeier A, Wagner CS, Nord O, Nygren P-A, van Wijk KJ, de Gier J-W (2007) Consequences of membrane protein overexpression in Escherichia coli. Mol Cell Proteomics MCP 6: 1527–1550
55. Zhang Q, Lambert G, Liao D, Kim H, Robin K, Tung C, Pourmand N, Austin RH (2011) Acceleration of emergence of bacterial antibiotic resistance in connected microenvironments. Science 333: 1764–1767
56. Zhuang K, Vemuri GN, Mahadevan R (2011) Economics of membrane occupancy and respiro-fermentation. Mol Syst Biol 7: 500