Escherichia coli adapts to tetracycline resistance plasmid (pBR322) by mutating endogenous potassium transport: In silico hypothesis testing

FEMS Microbiology Ecology

Volumn 83, Issue 3, 2013, Pages 622-631

  Hellweger, Ferdi L ^a  

^a Northeastern University   (United States)

Author keywords

Adaptation; Agent based modeling; Antibiotic resistance; Cost of resistance; Evolution

Indexed keywords

ANTIINFECTIVE AGENT; ANTIPORTER; BACTERIAL PROTEIN; POTASSIUM; TETA PROTEIN, BACTERIA; TETRACYCLINE;

ADAPTATION; ANTIBIOTIC RESISTANCE; BACTERIUM; CHROMOSOME; EVOLUTIONARY BIOLOGY; FECAL COLIFORM; FITNESS; GENE EXPRESSION; MUTATION; PLASMID; POTASSIUM;

ANTIBIOTIC RESISTANCE; ARTICLE; BIOLOGICAL MODEL; DRUG EFFECT; ESCHERICHIA COLI; GENETICS; ION TRANSPORT; METABOLISM; MOLECULAR EVOLUTION; PLASMID; REPRODUCTIVE FITNESS;

ANTI-BACTERIAL AGENTS; ANTIPORTERS; BACTERIAL PROTEINS; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENETIC FITNESS; ION TRANSPORT; MODELS, BIOLOGICAL; PLASMIDS; POTASSIUM; TETRACYCLINE; TETRACYCLINE RESISTANCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84873173712     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12019     Document Type: Article

References (46)

1. Austin DJ & Anderson RM (1999) Studies of antibiotic resistance within the patient, hospitals and the community using simple mathematical models. Philos Trans R Soc Lond B Biol Sci 354: 721-738.
2. Booth IR (1985) Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49: 359-378.
3. Bossemeyer D, Borchard A, Dosch D, Helmer G, Epstein W, Booth I & Bakker E (1989) K+-transport protein TrkA of Escherichia coli is a peripheral membrane protein that requires other trk gene products for attachment to the cytoplasmic membrane. J Biol Chem 264: 16403-16410.
4. Bouma JE & Lenski RE (1988) Evolution of a bacteria/plasmid association. Nature 335: 351-352.
5. Castellanos M, Wilson DB & Shuler ML (2004) A modular minimal cell model: purine and pyrimidine transport and metabolism. P Natl Acad Sci USA 101: 6681-6686.
6. Coleman ML & Chisholm SW (2007) Code and context: Prochlorococcus as a model for cross-scale biology. Trends Microbiol 15: 398-407.
7. De Gelder L, Ponciano JM, Abdo Z, Joyce P, Forney LJ & Top EM (2004) Combining mathematical models and statistical methods to understand and predict the dynamics of antibiotic-sensitive mutants in a population of resistant bacteria during experimental evolution. Genetics 168: 1131-1144.
8. Domach MM, Leung SK, Cahn RE, Cocks GG & Shuler ML (1984) Computer model for glucose-limited growth of a single cell of Escherichia coli B/r-A. Biotechnol Bioeng 26: 203-216.
9. Dosch DC, Salvacion FF & Epstein W (1984) Tetracycline resistance element of pBR322 mediates potassium transport. J Bacteriol 160: 1188-1190.
10. Dosch DC, Helmer GL, Sutton SH, Salvacion FF & Epstein W (1991) Genetic analysis of potassium transport loci in Escherichia coli: evidence for three constitutive systems mediating uptake potassium. J Bacteriol 173: 687-696.
11. Epstein W (2003) The Roles and Regulation of Potassium in Bacteria. Progress in Nucleic Acid Research and Molecular Biology, Vol. 75 (Moldave K. ed.), pp. 293-320. Academic Press, Amsterdam.
12. Epstein W & Schultz SG (1966) Cation transport in Escherichia coli. J Gen Physiol 49: 469-481.
13. Fange D, Nilsson K, Tenson T & Ehrenberg M (2009) Drug efflux pump deficiency and drug target resistance masking in growing bacteria. P Natl Acad Sci USA 106: 8215-8220.
14. Ferrer J, Prats C & López D (2008) Individual-based modelling: an essential tool for microbiology. J Biol Phys 34: 19-37.
15. Gilmour R, Messner P, Guffanti AA, Kent R, Scheberl A, Kendrick N & Krulwich TA (2000) Two-dimensional gel electrophoresis analyses of pH-dependent protein expression in facultatively alkaliphilic Bacillus pseudofirmus OF4 lead to characterization of an S-layer protein with a role in alkaliphily. J Bacteriol 182: 5969-5981.
16. Godwin D & Slater JH (1979) The influence of the growth environment on the stability of a drug resistance plasmid in Escherichia coli K12. J Gen Microbiol 111: 201-210.
17. Helling RB, Kinney T & Adams J (1981) The maintenance of plasmid-containing organisms in populations of Escherichia coli. J Gen Microbiol 123: 129-141.
18. Hellweger FL (2009) Carrying photosynthesis genes increases ecological fitness of cyanophage in silico. Environ Microbiol 11: 1386-1394.
19. Hellweger FL (2010) Resonating circadian clocks enhance fitness in cyanobacteria in silico. Ecol Model 221: 1620-1629.
20. Hellweger FL & Bucci V (2009) A bunch of tiny individuals-individual-based modeling for microbes. Ecol Model 220: 8-22.
21. Kaern M, Elston TC, Blake WJ & Collins JJ (2005) Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 6: 451-464.
22. Kim BG & Shuler ML (1990a) Analysis of pBR322 replication kinetics and its dependency on growth rate. Biotechnol Bioeng 36: 233-242.
23. Kim BG & Shuler ML (1990b) A structured, segregated model for genetically modified Escherichia coli cells and its use for prediction of plasmid stability. Biotechnol Bioeng 36: 581-592.
24. Klitgord N & Segrè D (2011) Ecosystems biology of microbial metabolism. Curr Opin Biotechnol 22: 541-546.
25. Koelle K, Khatri P, Kamradt M & Kepler TB (2010) A two-tiered model for simulating the ecological and evolutionary dynamics of rapidly evolving viruses, with an application to influenza. J R Soc Interface 7: 1257-1274.
26. Kreft J-U, Booth G & Wimpenny JWT (1998) BacSim, a simulator for individual-based modelling of bacterial colony growth. Microbiology 144: 3275-3287.
27. Krulwich TA, Jin J, Guffanti AA & Bechhofer H (2001) Functions of tetracycline efflux proteins that do not involve tetracycline. J Mol Microbiol Biotechnol 3: 237-246.
28. Laffend L & Shuler ML (1994) Ribosomal protein limitations in Escherichia coli under conditions of high translational activity. Biotechnol Bioeng 43: 388-398.
29. Lenski RE, Simpson SC & Nguyen TT (1994) Genetic analysis of a plasmid-encoded, host genotype-specific enhancement of bacterial fitness. J Bacteriol 176: 3140-3147.
30. Levin BR (2001) Minimizing potential resistance: a population dynamics view. Clin Infect Dis 33: S161-S169.
31. Levin BR, Perrot V & Walker N (2000) Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154: 985-997.
32. Levy SB (1986) Ecology of antibiotic resistance determinants. Banbury Report 24: Antibiotic Resistance Genes: Ecology, Transfer, and Expression (Levy SB & Novick RP, eds), pp. 17-30. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
33. Levy SB & Marshall B (2004) Antibacterial resistance worldwide: causes, challenges and responses. Nat Med 10: S122-S129.
34. McDermott PJ, Gowland P & Gowland PC (1993) Adaptation of Escherichia coli growth rates to the presence of pBR322. Lett Appl Microbiol 17: 139-143.
35. Meury J & Kepes A (1981) The regulation of potassium fluxes for the adjustment and maintenance of potassium levels in Escherichia coli. Eur J Biochem 119: 165-170.
36. Modi RI & Adams J (1991) Coevolution in bacterial-plasmid populations. Evolution 45: 656-667.
37. Murphy JT, Walshe R & Devocelle M (2008) A computational model of antibiotic-resistance mechanisms in methicillin-resistant Staphylococcus aureus (MRSA). J Theor Biol 254: 284-293.
38. Nakamura T, Matsuba Y, Ishihara A, Kitagawa T, Suzuki F & Unemoto T (1995) N-terminal quarter part of tetracycline transporter from pACYC184 complements K+ uptake activity in K+ uptake-deficient mutants of Escherichia coli and Vibrio alginolyticus. Biol Pharm Bull 18: 1189-1193.
39. Noack D, Roth M, Geuther R, Müller G, Undisz K, Hoffmeier C & Gáspár S (1981) Maintenance and genetic stability of vector plasmids pBR322 and pBR325 in Escherichia coli K12 strains grown in a chemostat. Mol Gen Genet 184: 121-124.
40. Raes J & Bork P (2008) Molecular eco-systems biology: towards an understanding of community function. Nat Rev Microbiol 6: 693-699.
41. Rhoads DB & Epstein W (1978) Cation transport in Escherichia coli. IX. Regulation of K transport. J Gen Physiol 72: 283-295.
42. Rhoads DB, Waters FB & Epstein W (1976) Cation transport in Escherichia coli. VIII. Potassium transport mutants. J Gen Physiol 67: 325-341.
43. Shuler ML, Leung S & Dick CC (1979) A mathematical model for the growth of a single bacterial cell. Ann NY Acad Sci 326: 35-52.
44. Stumpe S & Bakker EP (1997) Requirement of a large K+-uptake capacity and of extracytoplasmic protease activity for protamine resistance of Escherichia coli. Arch Microbiol 167: 126-136.
45. Stumpe S, Schlösser A, Schleyer M & Bakker EP (1996) K+ circulation across the prokaryotic cell membrane: K+-uptake systems. Handbook of Biological Physics, Vol. 2 (Konings WN, Kaback HR & Lolkema JS, eds), pp. 473-499. Elsevier Science, Amsterdam.
46. Young D, Stark J & Kirschner D (2008) Systems biology of persistent infection: tuberculosis as a case study. Nat Rev Microbiol 6: 520-528.