Polymorphic mutation frequencies of clinical and environmental Stenotrophomonas maltophilia populations

Applied and Environmental Microbiology

Volumn 76, Issue 6, 2010, Pages 1746-1758

  Turrientes, María Carmen ^a,b   Baquero, María Rosario ^c   Sánchez, María Blanca ^d   Valdezate, Sylvia ^e   Escudero, Esther ^a   Berg, Gabrielle ^f   Cantón, Rafael ^a,b   Baquero, Fernando ^a,b   Galán, Juan Carlos ^a,b   Martínez, José Luis ^a,d  

^a HOSPITAL RAMÓN Y CAJAL   (Spain)

^b CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^c UNIVERSIDAD ALFONSO X EL SABIO   (Spain)

^d CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^e INSTITUTO DE SALUD CARLOS III   (Spain)

^f GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POPULATION; BACTERIAL SPECIES; CLINICAL ENVIRONMENTS; COMPLEMENTATION; IN-SILICO; MODAL VALUES; MUTATION FREQUENCY; MUTS PROTEIN; RESISTANT MUTANTS; SECOND ORDERS; SELECTION PROCESS; STENOTROPHOMONAS MALTOPHILIA; SUSCEPTIBLE POPULATION; WILD TYPES;

BACTERIOLOGY; ORGANIC ACIDS;

AMINO ACIDS;

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; PROTEIN MUTS; RIFAMPICIN;

AMINO ACID; ANTIBIOTIC RESISTANCE; BACTERIUM; BIOASSAY; DETECTION METHOD; MUTATION; POLYMORPHISM; PROTEIN;

ANTIBIOTIC RESISTANCE; ARTICLE; GENETIC COMPLEMENTATION; GENETIC POLYMORPHISM; GENETICS; GRAM NEGATIVE INFECTION; ISOLATION AND PURIFICATION; MICROBIOLOGY; MUTATION; STENOTROPHOMONAS MALTOPHILIA;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; ENVIRONMENTAL MICROBIOLOGY; GENETIC COMPLEMENTATION TEST; GRAM-NEGATIVE BACTERIAL INFECTIONS; MUTATION; MUTS DNA MISMATCH-BINDING PROTEIN; POLYMORPHISM, GENETIC; RIFAMPIN; STENOTROPHOMONAS MALTOPHILIA;

BACTERIA (MICROORGANISMS); STENOTROPHOMONAS MALTOPHILIA;

EID: 77749304009     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02817-09     Document Type: Article

References (81)

1. Aisenberg, G., K. V. Rolston, B. F. Dickey, D. P. Kontoyiannis, I. I. Raad, and A. Safdar. 2007. Stenotrophomonas maltophilia pneumonia in cancer patients without traditional risk factors for infection, 1997-2004. Eur. J. Clin. Microbiol. Infect. Dis. 26:13-20.
2. Alonso, A., and J. L. Martinez. 2000. Cloning and characterization of SmeDEF, a novel multidrug efflux pump from Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 44:3079-3086.
3. Alonso, A., and J. L. Martinez. 2001. Expression of multidrug efflux pump SmeDEF by clinical isolates of Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 45:1879-1881.
4. Alonso, A., and J. L. Martinez. 1997. Multiple antibiotic resistance in Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 41:1140-1142.
5. Alonso, A., F. Rojo, and J. L. Martinez. 1999. Environmental and clinical isolates of Pseudomonas aeruginosa show pathogenic and biodegradative properties irrespective of their origin. Environ. Microbiol. 1:421-430.
6. Alonso, A., P. Sanchez, and J. L. Martinez. 2000. Stenotrophomonas maltophilia D457R contains a cluster of genes from gram-positive bacteria involved in antibiotic and heavy metal resistance. Antimicrob. Agents Chemother. 44:1778-1782.
7. Anisimova, M., and O. Gascuel. 2006. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 55:539-552.
8. Atlas, R. M. 1993. Handbook of microbiological media. CRC Press, Boca Raton FL.
9. Avison, M. B., C. S. Higgins, C. J. von Heldreich, P. M. Bennett, and T. R. Walsh. 2001. Plasmid location and molecular heterogeneity of the L1 and L2 beta-lactamase genes of Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 45:413-419.
10. Baquero, M. R., A. I. Nilsson, M. C. Turrientes, D. Sandvang, J. C. Galan, J. L. Martinez, N. Frimodt-Moller, F. Baquero, and D. I. Andersson. 2004. Polymorphic mutation frequencies in Escherichia coli: emergence of weak mutators in clinical isolates. J. Bacteriol. 186:5538-5542.
11. Berg, G., L. Eberl, and A. Hartmann. 2005. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ. Microbiol. 7:1673-1685.
12. Berg, G., N. Roskot, and K. Smalla. 1999. Genotypic and phenotypic relationships between clinical and environmental isolates of Stenotrophomonas maltophilia. J. Clin. Microbiol. 37:3594-3600.
13. Binks, P. R., S. Nicklin, and N. C. Bruce. 1995. Degradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) by Stenotrophomonas maltophilia PB1. Appl. Environ. Microbiol. 61:1318-1322.
14. Bragonzi, A., M. Paroni, A. Nonis, N. Cramer, S. Montanari, J. Rejman, C. Di Serio, G. Doring, and B. Tummler. 2009. Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am. J. Respir. Crit. Care Med. 180:138-145.
15. Burke, V., J. O. Robinson, C. J. Richardson, and C. S. Bundell. 1991. Longitudinal studies of virulence factors of Pseudomonas aeruginosa in cystic fibrosis. Pathology 23:145-148.
16. Chopra, I., A. J. O'Neill, and K. Miller. 2003. The role of mutators in the emergence of antibiotic-resistant bacteria. Drug Resist. Updat. 6:137-145.
17. Crossman, L. C., V. C. Gould, J. M. Dow, G. S. Vernikos, A. Okazaki, M. Sebaihia, D. Saunders, C. Arrowsmith, T. Carver, N. Peters, E. Adlem, A. Kerhornou, A. Lord, L. Murphy, K. Seeger, R. Squares, S. Rutter, M. A. Quail, M. A. Rajandream, D. Harris, C. Churcher, S. D. Bentley, J. Parkhill, N. R. Thomson, and M. B. Avison. 2008. The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol. 9:R74.
18. Crum, N. F., G. C. Utz, and M. R. Wallace. 2002. Stenotrophomonas maltophilia endocarditis. Scand. J. Infect. Dis. 34:925-927.
19. del Campo, R., M. I. Morosini, E. G. de la Pedrosa, A. Fenoll, C. Munoz-Almagro, L. Maiz, F. Baquero, and R. Canton. 2005. Population structure, antimicrobial resistance, and mutation frequencies of Streptococcus pneumoniae isolates from cystic fibrosis patients. J. Clin. Microbiol. 43:2207-2214.
20. de Lorenzo, V., L. Eltis, B. Kessler, and K. N. Timmis. 1993. Analysis of Pseudomonas gene products using lacIq/Ptrp-lac plasmids and transposons that confer conditional phenotypes. Gene 123:17-24.
21. de Lorenzo, V., and K. N. Timmis. 1994. Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol. 235:386-405.
22. De Soyza, A., A. McDowell, L. Archer, J. H. Dark, S. J. Elborn, E. Mahenthiralingam, K. Gould, and P. A. Corris. 2001. Burkholderia cepacia complex genomovars and pulmonary transplantation outcomes in patients with cystic fibrosis. Lancet 358:1780-1781.
23. Denamur, E., G. Lecointre, P. Darlu, O. Tenaillon, C. Acquaviva, C. Sayada, I. Sunjevaric, R. Rothstein, J. Elion, F. Taddei, M. Radman, and I. Matic. 2000. Evolutionary implications of the frequent horizontal transfer of mismatch repair genes. Cell 103:711-721.
24. Dungan, R. S., S. R. Yates, and W. T. Frankenberger, Jr. 2003. Transformations of selenate and selenite by Stenotrophomonas maltophilia isolated from a seleniferous agricultural drainage pond sediment. Environ. Microbiol. 5:287-295.
25. Fegan, M., P. Francis, A. C. Hayward, G. H. Davis, and J. A. Fuerst. 1990. Phenotypic conversion of Pseudomonas aeruginosa in cystic fibrosis. J. Clin. Microbiol. 28:1143-1146.
26. Foweraker, J. E., C. R. Laughton, D. F. Brown, and D. Bilton. 2005. Phenotypic variability of Pseudomonas aeruginosa in sputa from patients with acute infective exacerbation of cystic fibrosis and its impact on the validity of antimicrobial susceptibility testing. J. Antimicrob. Chemother. 55:921-927.
27. Gaddis, G. M., and M. L. Gaddis. 1990. Introduction to biostatistics, part 5: statistical inference techniques for hypothesis testing with nonparametric data. Ann. Emerg. Med. 19:1054-1059.
28. Galan, J. C., M. C. Turrientes, M. R. Baquero, M. Rodriguez-Alcayna, J. Martinez-Amado, J. L. Martinez, and F. Baquero. 2007. Mutation rate is reduced by increased dosage of mutL gene in Escherichia coli K-12. FEMS Microbiol. Lett. 275:263-269.
29. Gould, V. C., and M. B. Avison. 2006. SmeDEF-mediated antimicrobial drug resistance in Stenotrophomonas maltophilia clinical isolates having defined phylogenetic relationships. J. Antimicrob. Chemother. 57:1070-1076.
30. Gould, V. C., A. Okazaki, and M. B. Avison. 2006. Beta-lactam resistance and beta-lactamase expression in clinical Stenotrophomonas maltophilia isolates having defined phylogenetic relationships. J. Antimicrob. Chemother. 57: 199-203.
31. Gould, V. C., A. Okazaki, R. A. Howe, and M. B. Avison. 2004. Analysis of sequence variation among smeDEF multi drug efflux pump genes and flanking DNA from defined 16S rRNA subgroups of clinical Stenotrophomonas maltophilia isolates. J. Antimicrob. Chemother. 54:348-353.
32. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
33. Gutierrez, O., C. Juan, J. L. Perez, and A. Oliver. 2004. Lack of association between hypermutation and antibiotic resistance development in Pseudomonas aeruginosa isolates from intensive care unit patients. Antimicrob. Agents Chemother. 48:3573-3575.
34. Horst, J. P., T. H. Wu, and M. G. Marinus. 1999. Escherichia coli mutator genes. Trends Microbiol. 7:29-36.
35. Hugh, R., and E. Ryschenkow. 1961. Pseudomonas maltophilia, an alcaligenes-like species. J. Gen. Microbiol. 26:123-132.
36. Jain, M., D. Ramirez, R. Seshadri, J. F. Cullina, C. A. Powers, G. S. Schulert, M. Bar-Meir, C. L. Sullivan, S. A. McColley, and A. R. Hauser. 2004. Type III secretion phenotypes of Pseudomonas aeruginosa strains change during infection of individuals with cystic fibrosis. J. Clin. Microbiol. 42:5229-5237.
37. Kai, M., U. Effmert, G. Berg, and B. Piechulla. 2007. Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch. Microbiol. 187:351-360.
38. Kohler, T., A. Buckling, and C. van Delden. 2009. Cooperation and virulence of clinical Pseudomonas aeruginosa populations. Proc. Natl. Acad. Sci. U. S. A. 106:6339-6344.
39. Lambert, T., M. C. Ploy, F. Denis, and P. Courvalin. 1999. Characterization of the chromosomal aac(6′)-Iz gene of Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 43:2366-2371.
40. Lamers, M. H., A. Perrakis, J. H. Enzlin, H. H. Winterwerp, N. de Wind, and T. K. Sixma. 2000. The crystal structure of DNA mismatch repair protein MutS binding to a G x T mismatch. Nature 407:711-717.
41. LeClerc, J. E., B. Li, W. L. Payne, and T. A. Cebula. 1996. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274: 1208-1211.
42. Li, X. Z., L. Zhang, G. A. McKay, and K. Poole. 2003. Role of the acetyltransferase AAC(6′)-Iz modifying enzyme in aminoglycoside resistance in Stenotrophomonas maltophilia. J. Antimicrob. Chemother. 51:803-811.
43. Li, X. Z., L. Zhang, and K. Poole. 2002. SmeC, an outer membrane multidrug efflux protein of Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 46:333-343.
44. Looney, W. J. 2005. Role of Stenotrophomonas maltophilia in hospital-acquired infection. Br. J. Biomed. Sci. 62:145-154.
45. Mann, H. B., and D. R. Whitney. 1947. On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Statist. 18:50-60.
46. Mao, E. F., L. Lane, J. Lee, and J. H. Miller. 1997. Proliferation of mutators in a cell population. J. Bacteriol. 179:417-422.
47. Martin, D., M. Schurr, M. Mudd, J. Govan, B. Holloway, and V. Deretic. 1993. Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc. Natl. Acad. Sci. U. S. A. 90:8377-8381.
48. Martinez, J. L., and F. Baquero. 2002. Interactions among strategies associated with bacterial infection: pathogenicity, epidemicity, and antibiotic resistance. Clin. Microbiol. Rev. 15:647-679.
49. Martinez-Solano, L., M. D. Macia, A. Fajardo, A. Oliver, and J. L. Martinez. 2008. Chronic Pseudomonas aeruginosa infection in chronic obstructive pulmonary disease. Clin. Infect. Dis. 47:1526-1533.
50. Martins-Pinheiro, M., R. S. Galhardo, C. Lage, K. M. Lima-Bessa, K. A. Aires, and C. F. Menck. 2004. Different patterns of evolution for duplicated DNA repair genes in bacteria of the Xanthomonadales group. BMC Evol. Biol. 4:29.
51. Matic, I., M. Radman, F. Taddei, B. Picard, C. Doit, E. Bingen, E. Denamur, and J. Elion. 1997. Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science 277:1833-1834.
52. Mena, A., E. E. Smith, J. L. Burns, D. P. Speert, S. M. Moskowitz, J. L. Perez, and A. Oliver. 2008. Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalyzed by hypermutation. J. Bacteriol. 190:7910-7917.
53. Miller, J. H. 1996. Spontaneous mutators in bacteria: insights into pathways of mutagenesis and repair. Annu. Rev. Microbiol. 50:625-643.
54. Morales, G., L. Wiehlmann, P. Gudowius, C. van Delden, B. Tummler, J. L. Martinez, and F. Rojo. 2004. Structure of Pseudomonas aeruginosa populations analyzed by single nucleotide polymorphism and pulsed-field gel electrophoresis genotyping. J. Bacteriol. 186:4228-4237.
55. Natrajan, G., M. H. Lamers, J. H. Enzlin, H. H. Winterwerp, A. Perrakis, and T. K. Sixma. 2003. Structures of Escherichia coli DNA mismatch repair enzyme MutS in complex with different mismatches: a common recognition mode for diverse substrates. Nucleic Acids Res. 31:4814-4821.
56. Navas, A., G. Cobas, M. Talavera, J. A. Ayala, J. A. Lopez, and J. L. Martinez. 2007. Experimental validation of Haldane's hypothesis on the role of infection as an evolutionary force for metazoans. Proc. Natl. Acad. Sci. U. S. A. 104:13728-13731.
57. Obmolova, G., C. Ban, P. Hsieh, and W. Yang. 2000. Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature 407:703-710.
58. Okazaki, A., and M. B. Avison. 2007. Aph(3′)-IIc, an aminoglycoside resistance determinant from Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 51:359-360.
59. Oliver, A., F. Baquero, and J. Blazquez. 2002. The mismatch repair system (mutS, mutL and uvrD genes) in Pseudomonas aeruginosa: molecular characterization of naturally occurring mutants. Mol. Microbiol. 43:1641-1650.
60. Oliver, A., R. Canton, P. Campo, F. Baquero, and J. Blazquez. 2000. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288:1251-1254.
61. Prunier, A. L., B. Malbruny, M. Laurans, J. Brouard, J. F. Duhamel, and R. Leclercq. 2003. High rate of macrolide resistance in Staphylococcus aureus strains from patients with cystic fibrosis reveals high proportions of hypermutable strains. J. Infect. Dis. 187:1709-1716.
62. Renders, N., H. Verbrugh, and A. Van Belkum. 2001. Dynamics of bacterial colonisation in the respiratory tract of patients with cystic fibrosis. Infect. Genet. Evol. 1:29-39.
63. Ribbeck-Busch, K., A. Roder, D. Hasse, W. de Boer, J. L. Martinez, M. Hagemann, and G. Berg. 2005. A molecular biological protocol to distinguish potentially human pathogenic Stenotrophomonas maltophilia from plant-associated Stenotrophomonas rhizophila. Environ. Microbiol. 7:1853-1858.
64. Richardson, A. R., Z. Yu, T. Popovic, and I. Stojiljkovic. 2002. Mutator clones of Neisseria meningitidis in epidemic serogroup A disease. Proc. Natl. Acad. Sci. U. S. A. 99:6103-6107.
65. Rocha, E. P., J. M. Smith, L. D. Hurst, M. T. Holden, J. E. Cooper, N. H. Smith, and E. J. Feil. 2006. Comparisons of dN/dS are time dependent for closely related bacterial genomes. J. Theor. Biol. 239:226-235.
66. Roman, F., R. Canton, M. Perez-Vazquez, F. Baquero, and J. Campos. 2004. Dynamics of long-term colonization of respiratory tract by Haemophilus influenzae in cystic fibrosis patients shows a marked increase in hypermutable strains. J. Clin. Microbiol. 42:1450-1459.
67. Sanchez, M. B., A. Hernandez, J. M. Rodriguez-Martinez, L. Martinez-Martinez, and J. L. Martinez. 2008. Predictive analysis of transmissible quinolone resistance indicates Stenotrophomonas maltophilia as a potential source of a novel family of Qnr determinants. BMC Microbiol. 8:148.
68. Sanchez, M. B., and J. L. Martinez. 2010. SmQnr contributes to intrinsic resistance to quinolones of Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 54:580-581.
69. Sanchez, P., A. Alonso, and J. L. Martinez. 2004. Regulatory regions of smeDEF in Stenotrophomonas maltophilia strains expressing different amounts of the multidrug efflux pump SmeDEF. Antimicrob. Agents Chemother. 48:2274-2276.
70. Sixma, T. K. 2001. DNA mismatch repair: MutS structures bound to mismatches. Curr. Opin. Struct. Biol. 11:47-52.
71. Smith, E. E., D. G. Buckley, Z. Wu, C. Saenphimmachak, L. R. Hoffman, D. A. D'Argenio, S. I. Miller, B. W. Ramsey, D. P. Speert, S. M. Moskowitz, J. L. Burns, R. Kaul, and M. V. Olson. 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. U. S. A. 103:8487-8492.
72. Spicuzza, L., C. Sciuto, G. Vitaliti, G. Di Dio, S. Leonardi, and M. La Rosa. 2008. Emerging pathogens in cystic fibrosis: ten years of follow-up in a cohort of patients. Eur. J. Clin. Microbiol. Infect. Dis. 28:191-195.
73. Tachibana, S., N. Kuba, F. Kawai, J. A. Duine, and M. Yasuda. 2003. Involvement of a quinoprotein (PQQ-containing) alcohol dehydrogenase in the degradation of polypropylene glycols by the bacterium Stenotrophomonas maltophilia. FEMS Microbiol. Lett. 218:345-349.
74. Tavare, S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on mathematics in the life sciences, vol. 17, p. 57-86. American Mathematical Society, Providence, RI.
75. Tenaillon, O., F. Taddei, M. Radmian, and I. Matic. 2001. Second-order selection in bacterial evolution: selection acting on mutation and recombination rates in the course of adaptation. Res. Microbiol. 152:11-16.
76. Tenaillon, O., B. Toupance, H. Le Nagard, F. Taddei, and B. Godelle. 1999. Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics 152:485-493.
77. Valdezate, S., A. Vindel, L. Maiz, F. Baquero, H. Escobar, and R. Canton. 2001. Persistence and variability of Stenotrophomonas maltophilia in cystic fibrosis patients, Madrid, 1991-1998. Emerg. Infect. Dis. 7:113-122.
78. Vila, J., and J. L. Martinez. 2008. Clinical impact of the over-expression of efflux pump in nonfermentative gram-negative bacilli, development of efflux pump inhibitors. Curr. Drug Targets 9:797-807.
79. Wang, W. S., C. P. Liu, C. M. Lee, and F. Y. Huang. 2004. Stenotrophomonas maltophilia bacteremia in adults: four years' experience in a medical center in northern Taiwan. J. Microbiol. Immunol. Infect. 37:359-365.
80. Wilder, C. N., G. Allada, and M. Schuster. 2009. Instantaneous withinpatient diversity of Pseudomonas aeruginosa quorum-sensing populations from cystic fibrosis lung infections. Infect. Immun. 77:5631-5639.
81. Wu, P. S., C. Y. Lu, L. Y. Chang, P. R. Hsueh, P. I. Lee, J. M. Chen, C. Y. Lee, P. C. Chan, P. Y. Chang, T. T. Yang, and L. M. Huang. 2006. Stenotrophomonas maltophilia bacteremia in pediatric patients, a 10-year analysis. J. Microbiol. Immunol. Infect. 39:144-149.