Escape from growth restriction in small colony variants of Salmonella typhimurium by gene amplification and mutation

Molecular Microbiology

Volumn 79, Issue 2, 2011, Pages 305-315

  Pränting, Maria ^a   Andersson, Dan I ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HEME; PROTAMINE; PROTEIN HEMC; UNCLASSIFIED DRUG;

ADAPTATION; AMINO ACID SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM COLONY; BACTERIUM MUTANT; CONTROLLED STUDY; FITNESS; GENE AMPLIFICATION; GENE DOSAGE; GENE MUTATION; GENETIC SELECTION; GROWTH INHIBITION; HAPLOIDY; HEME SYNTHESIS; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR EVOLUTION; NONHUMAN; POPULATION SIZE; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM; STRAIN DIFFERENCE; WILD TYPE;

ADAPTATION, BIOLOGICAL; GENE AMPLIFICATION; GENOMIC INSTABILITY; HYDROXYMETHYLBILANE SYNTHASE; MUTATION, MISSENSE; SALMONELLA TYPHIMURIUM; SELECTION, GENETIC;

SALMONELLA TYPHIMURIUM;

EID: 78651088019     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07458.x     Document Type: Article

References (52)

1. Acar, J.F., Goldstein, F.W., and Lagrange, P. (1978) Human infections caused by thiamine- or menadione-requiring Staphylococcus aureus. J Clin Microbiol 8: 142-147.
2. Anderson, P., and Roth, J. (1981) Spontaneous tandem genetic duplications in Salmonella typhimurium arise by unequal recombination between rRNA (rrn) cistrons. Proc Natl Acad Sci USA 78: 3113-3117.
3. Andersson, D.I. (2006) The biological cost of mutational antibiotic resistance: any practical conclusions? Curr Opin Microbiol 9: 461-465.
4. Andersson, D.I., and Hughes, D. (2009) Gene amplification and adaptive evolution in bacteria. Annu Rev Genet 43: 167-195.
5. Andersson, D.I., and Hughes, D. (2010) Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol 8: 260-271.
6. Andersson, D.I., and Levin, B.R. (1999) The biological cost of antibiotic resistance. Curr Opin Microbiol 2: 489-493.
7. Andersson, D.I., Slechta, E.S., and Roth, J.R. (1998) Evidence that gene amplification underlies adaptive mutability of the bacterial lac operon. Science 282: 1133-1135.
8. Aspedon, A., and Groisman, E.A. (1996) The antibacterial action of protamine: evidence for disruption of cytoplasmic membrane energization in Salmonella typhimurium. Microbiology 142 (Part 12): 3389-3397.
9. Baumert, N., von Eiff, C., Schaaff, F., Peters, G., Proctor, R.A., and Sahl, H.G. (2002) Physiology and antibiotic susceptibility of Staphylococcus aureus small colony variants. Microb Drug Resist 8: 253-260.
10. Beljanski, M. (1957) [Formation of respiratory enzymes in streptomycin-resistant and heme-auxotrophic mutant of Escherichia coli]. Ann Inst Pasteur (Paris) 92: 396-412.
11. Besier, S., Ludwig, A., Ohlsen, K., Brade, V., and Wichelhaus, T.A. (2007) Molecular analysis of the thymidine-auxotrophic small colony variant phenotype of Staphylococcus aureus. Int J Med Microbiol 297: 217-225.
12. Bjorkman, J., Hughes, D., and Andersson, D.I. (1998) Virulence of antibiotic-resistant Salmonella typhimurium. Proc Natl Acad Sci USA 95: 3949-3953.
13. Cano, D.A., Pucciarelli, M.G., Martinez-Moya, M., Casadesus, J., and Garcia-del Portillo, F. (2003) Selection of small-colony variants of Salmonella enterica serovar typhimurium in nonphagocytic eucaryotic cells. Infect Immun 71: 3690-3698.
14. Chatterjee, I., Kriegeskorte, A., Fischer, A., Deiwick, S., Theimann, N., Proctor, R.A., et al. (2008) In vivo mutations of thymidylate synthase (encoded by thyA) are responsible for thymidine dependency in clinical small-colony variants of Staphylococcus aureus. J Bacteriol 190: 834-842.
15. Colwell, C.A. (1946) Small Colony Variants of Escherichia coli. J Bacteriol 52: 417-422.
16. von Eiff, C., Heilmann, C., Proctor, R.A., Woltz, C., Peters, G., and Gotz, F. (1997) A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly. J Bacteriol 179: 4706-4712.
17. Fogel, S., and Welch, J.W. (1982) Tandem gene amplification mediates copper resistance in yeast. Proc Natl Acad Sci USA 79: 5342-5346.
18. Hancock, R.E. (1997) Peptide antibiotics. Lancet 349: 418-422.
19. Haussler, S., Tummler, B., Weissbrodt, H., Rohde, M., and Steinmetz, I. (1999) Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin Infect Dis 29: 621-625.
20. Hudson, R.E., Bergthorsson, U., Roth, J.R., and Ochman, H. (2002) Effect of chromosome location on bacterial mutation rates. Mol Biol Evol 19: 85-92.
21. Jensen, V.J., and Thofern, E. (1953) Chlorhämin (ferriporphyrinchlorid) als Bakterienwuchstoff I. Z Naturforsch 8b: 599.
22. Johansen, C., Verheul, A., Gram, L., Gill, T., and Abee, T. (1997) Protamine-induced permeabilization of cell envelopes of gram-positive and gram-negative bacteria. Appl Environ Microbiol 63: 1155-1159.
23. Kahl, B., Herrmann, M., Everding, A.S., Koch, H.G., Becker, K., Harms, E., et al. (1998) Persistent infection with small colony variant strains of Staphylococcus aureus in patients with cystic fibrosis. J Infect Dis 177: 1023-1029.
24. Kugelberg, E., Kofoid, E., Andersson, D.I., Lu, Y., Mellor, J., Roth, F.P., and Roth, J.R. (2010) The tandem inversion duplication in Salmonella enterica: selection drives unstable precursors to final mutation types. Genetics 185: 65-80.
25. Levin, B.R., Perrot, V., and Walker, N. (2000) Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154: 985-997.
26. Lewis, L.A., Lewis, D., Persaud, V., Gopaul, S., and Turner, B. (1994) Transposition of IS2 into the hemB gene of Escherichia coli K-12. J Bacteriol 176: 2114-2120.
27. Maisnier-Patin, S., Berg, O.G., Liljas, L., and Andersson, D.I. (2002) Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium. Mol Microbiol 46: 355-366.
28. Morris, J.F., Barnes, C.G., and Sellers, T.F. (1943) An Outbreak of Typhoid Fever Due to the Small Colony Variety of Eberthella typhosa. Am J Public Health Nations Health 33: 246-248.
29. Nagaev, I., Bjorkman, J., Andersson, D.I., and Hughes, D. (2001) Biological cost and compensatory evolution in fusidic acid-resistant Staphylococcus aureus. Mol Microbiol 40: 433-439.
30. Newcomb, R.D., Gleeson, D.M., Yong, C.G., Russell, R.J., and Oakeshott, J.G. (2005) Multiple mutations and gene duplications conferring organophosphorus insecticide resistance have been selected at the Rop-1 locus of the sheep blowfly, Lucilia cuprina. J Mol Evol 60: 207-220.
31. Nguyen, H.A., Denis, O., Vergison, A., Theunis, A., Tulkens, P.M., Struelens, M.J., and Van Bambeke, F. (2009) Intracellular activity of antibiotics in a model of human THP-1 macrophages infected by a Staphylococcus aureus small-colony variant strain isolated from a cystic fibrosis patient: pharmacodynamic evaluation and comparison with isogenic normal-phenotype and revertant strains. Antimicrob Agents Chemother 53: 1434-1442.
32. Nilsson, A.I., Zorzet, A., Kanth, A., Dahlstrom, S., Berg, O.G., and Andersson, D.I. (2006) Reducing the fitness cost of antibiotic resistance by amplification of initiator tRNA genes. Proc Natl Acad Sci USA 103: 6976-6981.
33. Paulander, W., Maisnier-Patin, S., and Andersson, D.I. (2007) Multiple mechanisms to ameliorate the fitness burden of mupirocin resistance in Salmonella typhimurium. Mol Microbiol 64: 1038-1048.
34. Paulander, W., Andersson, D.I., and Maisnier-Patin, S.E. (2010) Amplification of the Gene for isoleucyl-tRNA Synthetase Facilitates Adaptation to the Fitness Cost of Mupirocin Resistance in Salmonella enterica. Genetics 185: 305-312.
35. Pelletier, L.L., Jr, Richardson, M., and Feist, M. (1979) Virulent gentamicin-induced small colony variants of Staphylococcus aureus. J Lab Clin Med 94: 324-334.
36. Pettersson, M.E., Sun, S., Andersson, D.I., and Berg, O.G. (2009) Evolution of new gene functions: simulation and analysis of the amplification model. Genetica 135: 309-324.
37. Pränting, M., and Andersson, D.I. (2010) Mechanisms and physiological effects of protamine resistance in Salmonella enterica serovar Typhimurium LT2. J Antimicrob Chemother 65: 876-887.
38. Proctor, R.A., and von Humboldt, A. (1998) Bacterial energetics and antimicrobial resistance. Drug Resist Updat 1: 227-235.
39. Proctor, R.A., van Langevelde, P., Kristjansson, M., Maslow, J.N., and Arbeit, R.D. (1995) Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin Infect Dis 20: 95-102.
40. Proctor, R.A., Kahl, B., von Eiff, C., Vaudaux, P.E., Lew, D.P., and Peters, G. (1998) Staphylococcal small colony variants have novel mechanisms for antibiotic resistance. Clin Infect Dis 27 (Suppl. 1): S68-S74.
41. Proctor, R.A., von Eiff, C., Kahl, B.C., Becker, K., McNamara, P., Herrmann, M., and Peters, G. (2006) Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4: 295-305.
42. Reams, A.B., and Neidle, E.L. (2003) Genome plasticity in Acinetobacter: new degradative capabilities acquired by the spontaneous amplification of large chromosomal segments. Mol Microbiol 47: 1291-1304.
43. Reams, A.B., Kofoid, E., Savageau, M., and Roth, J.R. (2010) Duplication frequency in a population of Salmonella enterica rapidly approaches steady state with or without recombination. Genetics 184: 1077-1094.
44. Roggenkamp, A., Sing, A., Hornef, M., Brunner, U., Autenrieth, I.B., and Heesemann, J. (1998) Chronic prosthetic hip infection caused by a small-colony variant of Escherichia coli. J Clin Microbiol 36: 2530-2534.
45. Sadowska, B., Bonar, A., von Eiff, C., Proctor, R.A., Chmiela, M., Rudnicka, W., and Rozalska, B. (2002) Characteristics of Staphylococcus aureus, isolated from airways of cystic fibrosis patients, and their small colony variants. FEMS Immunol Med Microbiol 32: 191-197.
46. Schrag, S.J., and Perrot, V. (1996) Reducing antibiotic resistance. Nature 381: 120-121.
47. Shcherbakov, D., Akbergenov, R., Matt, T., Sander, P., Andersson, D.I., and Bottger, E.C. (2010) Directed mutagenesis of Mycobacterium smegmatis 16S rRNA to reconstruct the in-vivo evolution of aminoglycoside resistance in Mycobacterium tuberculosis. Mol Microbiol 77: 830-840.
48. Sonti, R.V., and Roth, J.R. (1989) Role of gene duplications in the adaptation of Salmonella typhimurium to growth on limiting carbon sources. Genetics 123: 19-28.
49. Sun, S., Berg, O.G., Roth, J.R., and Andersson, D.I. (2009) Contribution of gene amplification to evolution of increased antibiotic resistance in Salmonella typhimurium. Genetics 182: 1183-1195.
50. Swingle, E.L. (1935) Studies on small colony variants of staphylococcus aureus. J Bacteriol 29: 467-489.
51. Vesga, O., Groeschel, M.C., Otten, M.F., Brar, D.W., Vann, J.M., and Proctor, R.A. (1996) Staphylococcus aureus small colony variants are induced by the endothelial cell intracellular milieu. J Infect Dis 173: 739-742.
52. Xu, K., Delling, J., and Elliott, T. (1992) The genes required for heme synthesis in Salmonella typhimurium include those encoding alternative functions for aerobic and anaerobic coproporphyrinogen oxidation. J Bacteriol 174: 3953-3963.