Isolation and characterization of numerous novel phages targeting diverse strains of the ubiquitous and opportunistic pathogen Achromobacter xylosoxidans

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Wittmann, Johannes ^a   Dreiseikelmann, Brigitte ^b   Rohde, Christine ^a   Rohde, Manfred ^c   Sikorski, Johannes ^a  

^a LEIBNIZ INSTITUTE DSMZ GERMAN COLLECTION OF MICROORGANISMS AND CELL CULTURES   (Germany)

^b BIELEFELD UNIVERSITY   (Germany)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; AMPICILLIN; BACITRACIN; CEFALOTIN; CEFAZOLIN; CEFOTAXIME; CEFTRIAXONE; CHLORAMPHENICOL; CLINDAMYCIN; COLISTIN; DOXYCYCLINE; ERYTHROMYCIN; GENTAMICIN; IMIPENEM; KANAMYCIN; LINCOMYCIN; MEZLOCILLIN; NEOMYCIN; NITROFURANTOIN; NORFLOXACIN; OFLOXACIN; OXACILLIN; PENICILLIN G; PIPEMIDIC ACID; PIPERACILLIN PLUS TAZOBACTAM; POLYMYXIN B; TETRACYCLINE; TICARCILLIN; UNINDEXED DRUG; VANCOMYCIN;

ACHROMOBACTER XYLOSOXIDANS; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIOPHAGE; BACTERIUM ISOLATION; ELECTRON MICROSCOPY; GERMANY; MICROARRAY ANALYSIS; MICROBIAL DIVERSITY; MICROBIAL MORPHOLOGY; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; RESTRICTION MAPPING; UNINDEXED SEQUENCE; WASTE WATER TREATMENT PLANT;

ACHROMOBACTER DENITRIFICANS; ANTI-BACTERIAL AGENTS; BLOTTING, SOUTHERN; CAUDOVIRALES; DRUG RESISTANCE, BACTERIAL; GERMANY; MICROARRAY ANALYSIS; MICROSCOPY, ELECTRON; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; SPECIES SPECIFICITY;

EID: 84893876396     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086935     Document Type: Article

References (77)

1. Yabuuchi E, Oyama A (1971) Achromobacter xylosoxidans n. sp. from human ear discharge. Jpn J Microbiol 15: 477-481.
2. Busse HJ, Auling G (2005) Genus II. Achromobacter Yabuuchi and Yano 1981, 477VP emend. Yabuuchi, Kawamura, Kosako and Ezaki 1998a, 1083. In: Brenner DJ, Krieg NR, Staley JT, editors. Bergey's manual of systematic bacteriology. New York: Springer Verlag. 658-662.
3. Spear JB, Fuhrer J, Kirby BD (1988) Achromobacter xylosoxidans (Alcaligenes xylosoxidans subsp. xylosoxidans) bacteremia associated with a well-water source: case report and review of the literature. J Clin Microbiol 26: 598-599. (Pubitemid 18062132)
4. Reverdy ME, Freney J, Fleurette J, Coulet M, Surgot M, et al. (1984) Nosocomial colonization and infection by Achromobacter xylosoxidans. J Clin Microbiol 19: 140-143. (Pubitemid 14183564)
5. Ho YN, Mathew DC, Hsiao SC, Shih CH, Chien MF, et al. (2012) Selection and application of endophytic bacterium Achromobacter xylosoxidans strain F3B for improving phytoremediation of phenolic pollutants. J Hazard Mater 219-220: 43-49.
6. Jha P, Kumar A (2009) Characterization of novel plant growth promoting endophytic bacterium Achromobacter xylosoxidans from wheat plant. Microb Ecol 58: 179-188.
7. Ma Y, Rajkumar M, Freitas H (2009) Inoculation of plant growth promoting bacterium Achromobacter xylosoxidans strain Ax10 for the improvement of copper phytoextraction by Brassica juncea. J Environ Manage 90: 831-837.
8. Jencova V, Strnad H, Chodora Z, Ulbrich P, Hickey WJ, et al. (2004) Chlorocatechol catabolic enzymes from Achromobacter xylosoxidans A8. International Biodeterioration & Biodegradation 54: 175-181. (Pubitemid 39122981)
9. Jencova V, Strnad H, Chodora Z, Ulbrich P, Vlcek C, et al. (2008) Nucleotide sequence, organization and characterization of the (halo)aromatic acid catabolic plasmid pA81 from Achromobacter xylosoxidans A8. Res Microbiol 159: 118-127.
10. Strnad H, Ridl J, Paces J, Kolar M, Vlcek C, et al. (2011) Complete genome sequence of the haloaromatic acid-degrading bacterium Achromobacter xylosoxidans A8. J Bacteriol 193: 791-792.
11. Lambiase A, Catania MR, Del Pezzo M, Rossano F, Terlizzi V, et al. (2011) Achromobacter xylosoxidans respiratory tract infection in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis 30: 973-980.
12. Razvi S, Quittell L, Sewall A, Quinton H, Marshall B, et al. (2009) Respiratory microbiology of patients with cystic fibrosis in the United States, 1995 to 2005. Chest 136: 1554-1560.
13. Ahmed MS, Nistal C, Jayan R, Kuduvalli M, Anijeet HK (2009) Achromobacter xylosoxidans, an emerging pathogen in catheter-related infection in dialysis population causing prosthetic valve endocarditis: a case report and review of literature. Clin Nephrol 71: 350-354.
14. van Hal S, Stark D, Marriott D, Harkness J (2008) Achromobacter xylosoxidans subsp. xylosoxidans prosthetic aortic valve infective endocarditis and aortic root abscesses. J Med Microbiol 57: 525-527. (Pubitemid 351537031)
15. Behrens-Muller B, Conway J, Yoder J, Conover CS (2012) Investigation and control of an outbreak of Achromobacter xylosoxidans bacteremia. Infect Control Hosp Epidemiol 33: 180-184.
16. Tena D, Carranza R, Barbera JR, Valdezate S, Garrancho JM, et al. (2005) Outbreak of long-term intravascular catheter-related bacteremia due to Achromobacter xylosoxidans subspecies xylosoxidans in a hemodialysis unit. Eur J Clin Microbiol Infect Dis 24: 727-732. (Pubitemid 41752068)
17. Manckoundia P, Mazen E, Coste AS, Somana S, Marilier S, et al. (2011) A case of meningitis due to Achromobacter xylosoxidans denitrificans 60 years after a cranial trauma. Med Sci Monit 17: CS63-65.
18. Park JH, Song NH, Koh JW (2012) Achromobacter xylosoxidans keratitis after contact lens usage. Korean J Ophthalmol 26: 49-53.
19. Reddy AK, Garg P, Shah V, Gopinathan U (2009) Clinical, microbiological profile and treatment outcome of ocular infections caused by Achromobacter xylosoxidans. Cornea 28: 1100-1103.
20. Tena D, Gonzalez-Praetorius A, Perez-Balsalobre M, Sancho O, Bisquert J (2008) Urinary tract infection due to Achromobacter xylosoxidans: report of 9 cases. Scand J Infect Dis 40: 84-87.
21. Davies JC, Rubin BK (2007) Emerging and unusual gram-negative infections in cystic fibrosis. Semin Respir Crit Care Med 28: 312-321. (Pubitemid 46982062)
22. Ridderberg W, Bendstrup KE, Olesen HV, Jensen-Fangel S, Norskov-Lauritsen N (2011) Marked increase in incidence of Achromobacter xylosoxidans infections caused by sporadic acquisition from the environment. J Cyst Fibros 10: 466-469.
23. Ridderberg W, Wang M, Norskov-Lauritsen N (2012) Multilocus sequence analysis of isolates of Achromobacter from patients with cystic fibrosis reveals infecting species other than Achromobacter xylosoxidans. J Clin Microbiol 50: 2688-2694.
24. Vu-Thien H, Darbord JC, Moissenet D, Dulot C, Dufourcq JB, et al. (1998) Investigation of an outbreak of wound infections due to Alcaligenes xylosoxidans transmitted by chlorhexidine in a burns unit. Eur J Clin Microbiol Infect Dis 17: 724-726. (Pubitemid 29218996)
25. Festini F, Taccetti G, Mannini C, Campana S, Mergni G, et al. (2007) Patient risk of contact with respiratory pathogens from inanimate surfaces in a cystic fibrosis outpatient clinic. A prospective study over a four-year period. Pediatr Pulmonol 42: 779-784. (Pubitemid 47580804)
26. Reina J, Antich M, Siquier B, Alomar P (1988) Nosocomial outbreak of Achromobacter xylosoxidans associated with a diagnostic contrast solution. J Clin Pathol 41: 920-921.
27. Olshtain-Pops K, Block C, Temper V, Hidalgo-Grass C, Gross I, et al. (2011) An outbreak of achromobacter xylosoxidans associated with ultrasound gel used during transrectal ultrasound guided prostate biopsy. J Urol 185: 144-147.
28. Aisenberg G, Rolston KV, Safdar A (2004) Bacteremia caused by Achromobacter and Alcaligenes species in 46 patients with cancer (1989-2003). Cancer 101: 2134-2140. (Pubitemid 39425391)
29. Duggan JM, Goldstein SJ, Chenoweth CE, Kauffman CA, Bradley SF (1996) Achromobacter xylosoxidans bacteremia: report of four cases and review of the literature. Clin Infect Dis 23: 569-576. (Pubitemid 26304509)
30. Martino P, Micozzi A, Venditti M, Gentile G, Girmenia C, et al. (1990) Catheter-related right-sided endocarditis in bone marrow transplant recipients. Rev Infect Dis 12: 250-257. (Pubitemid 20118649)
31. Olson DA, Hoeprich PD (1982) Postoperative infection of an aortic prosthesis with Achromobacter xylosoxidans. West J Med 136: 153-157.
32. Fleming A (1980) Classics in infectious diseases: on the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenzae by Alexander Fleming, Reprinted from the British Journal of Experimental Pathology 10: 226-236, 1929. Rev Infect Dis 2: 129-139.
33. Rolston KV, Messer M (1990) The in-vitro susceptibility of Alcaligenes denitrificans subsp. xylosoxidans to 40 antimicrobial agents. J Antimicrob Chemother 26: 857-860.
34. Yamamoto M, Nagao M, Hotta G, Matsumura Y, Matsushima A, et al. (2012) Molecular characterization of IMP-type metallo-beta-lactamases among multi-drug-resistant Achromobacter xylosoxidans. J Antimicrob Chemother 67: 2110-2113.
35. Cooper MA, Shlaes D (2011) Fix the antibiotics pipeline. Nature 472: 32.
36. Walker RD, Thornsberry C (1998) Decrease in antibiotic susceptibility or increase in resistance? J Antimicrob Chemother 41: 1-4. (Pubitemid 28064242)
37. Levesque R, Letarte R, Pechere JC (1983) Comparative study of the beta-lactamase activity found in Achromobacter. Can J Microbiol 29: 819-826.
38. Bador J, Amoureux L, Blanc E, Neuwirth C (2013) Innate aminoglycoside resistance of Achromobacter xylosoxidans is due to AxyXY-OprZ, an RND-type multidrug efflux pump. Antimicrob Agents Chemother 57: 603-605.
39. D'Herelle F (2007) On an invisible microbe antagonistic toward dysenteric bacilli: brief note by Mr. F. D'Herelle, presented by Mr. Roux. 1917. Res Microbiol 158: 553-554.
40. Borysowski J, Lobocka M, Miedzybrodzki R, Weber-Dabrowska B, Gorski A (2011) Potential of bacteriophages and their lysins in the treatment of MRSA: current status and future perspectives. BioDrugs 25: 347-355.
41. Chan BK, Abedon ST, Loc-Carrillo C (2013) Phage cocktails and the future of phage therapy. Future Microbiol 8: 769-783.
42. Pirnay J-P, Verbeken G, Rose T, Jennes S, Zizi M, et al. (2012) Introducing yesterday's phage therapy in today's medicine. Future Virology 7: 379-390.
43. Jones PT, Pretorius GHJ (1981) Achromobacter sp. 2 Phage a3: A Physical Characterization. J gen Virol 55: 275-281.
44. Thomson JA, Woods DR (1974) Bacteriophages and cryptic lysogeny in Achromobacter. J Gen Virol 22: 153-157.
45. Ackermann HW, DuBow MS (2000) Myoviridae, Siphoviridae, Podoviridae. In: Van Regenmortel HV, Fauquet CM, Bishop DHL, editors. Virus Taxonomy: Classification and Nomenclature of Viruses : Seventh Report of the International Committee on Taxonomy of Viruses:: Academic Press. 69-109.
46. Capparelli R, Parlato M, Borriello G, Salvatore P, Iannelli D (2007) Experimental phage therapy against Staphylococcus aureus in mice. Antimicrob Agents Chemother 51: 2765-2773. (Pubitemid 47206211)
47. Guenther S, Huwyler D, Richard S, Loessner MJ (2009) Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl Environ Microbiol 75: 93-100.
48. O'Flaherty S, Ross RP, Coffey A (2009) Bacteriophage and their lysins for elimination of infectious bacteria. FEMS Microbiol Rev 33: 801-819.
49. Chhibber S, Kaur T, Sandeep K (2013) Co-therapy using lytic bacteriophage and linezolid: effective treatment in eliminating methicillin resistant Staphylococcus aureus (MRSA) from diabetic foot infections. PLoS One 8: e56022.
50. Merabishvili M, De Vos D, Verbeken G, Kropinski AM, Vandenheuvel D, et al. (2012) Selection and characterization of a candidate therapeutic bacteriophage that lyses the Escherichia coli O104:H4 strain from the 2011 outbreak in Germany. PLoS One 7: e52709.
51. Traglia GM, Almuzara M, Merkier AK, Adams C, Galanternik L, et al. (2012) Achromobacter xylosoxidans: an emerging pathogen carrying different elements involved in horizontal genetic transfer. Curr Microbiol 65: 673-678.
52. Mazaheri Nezhad Fard R, Barton MD, Heuzenroeder MW (2011) Bacteriophage-mediated transduction of antibiotic resistance in enterococci. Letters in Applied Microbiology 52: 559-564.
53. Woods DR, Thomson JA (1975) Unstable generalized transduction in Achromobacter. J Gen Microbiol 88: 86-92.
54. Karumidze N, Kusradze I, Rigvava S, Goderdzishvili M, Rajakumar K, et al. (2013) Isolation and characterisation of lytic bacteriophages of Klebsiella pneumoniae and Klebsiella oxytoca. Curr Microbiol 66: 251-258.
55. Rigvava S, Tchgkonia I, Jgenti D, Dvalidze T, Carpino J, et al. (2013) Comparative analysis of the biological and physical properties of Enterococcus faecalis bacteriophage vB-EfaS-GEC-EfS-3 and Streptococcus mitis bacteriophage vB-SmM-GEC-SmitisM-2. Can J Microbiol 59: 18-21.
56. Seal BS (2013) Characterization of bacteriophages virulent for Clostridium perfringens and identification of phage lytic enzymes as alternatives to antibiotics for potential control of the bacterium. Poult Sci 92: 526-533.
57. Ackermann HW (2001) Frequency of morphological phage descriptions in the year 2000. Brief review. Arch Virol 146: 843-857.
58. Zivin R, Zehring W, Rothman-Denes LB (1981) Transcriptional map of bacteriophage N4: Location and polarity of N4 RNAs. Journal of Molecular Biology 152: 335-356. (Pubitemid 12163833)
59. Fouts DE, Klumpp J, Bishop-Lilly KA, Rajavel M, Willner KM, et al. (2013) Whole genome sequencing and comparative genomic analyses of two Vibrio cholerae O139 Bengal-specific Podoviruses to other N4-like phages reveal extensive genetic diversity. Virol J 10: 165.
60. Hatfull GF (2008) Bacteriophage genomics. Curr Opin Microbiol 11: 447-453.
61. Garbe J, Wesche A, Bunk B, Kazmierczak M, Selezska K, et al. (2010) Characterization of JG024, a pseudomonas aeruginosa PB1-like broad host range phage under simulated infection conditions. BMC Microbiol 10: 301.
62. Alemayehu D, Casey PG, McAuliffe O, Guinane CM, Martin JG, et al. (2012) Bacteriophages phiMR299-2 and phiNH-4 can eliminate Pseudomonas aeruginosa in the murine lung and on cystic fibrosis lung airway cells. MBio 3: e00029-00012.
63. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN, editor. Mammalian Protein Metabolism New York: Academic Press. 21-132.
64. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution 28: 2731-2739.
65. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
66. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG (2004) eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186: 1518-1530. (Pubitemid 38248742)
67. Haubold B, Hudson RR (2000) LIAN 3.0: detecting linkage disequilibrium in multilocus data. Linkage Analysis. Bioinformatics 16: 847-848.
68. Vaas LA, Sikorski J, Michael V, Goker M, Klenk HP (2012) Visualization and curve-parameter estimation strategies for efficient exploration of phenotype microarray kinetics. PLoS One 7: e34846.
69. Vaas LA, Sikorski J, Hofner B, Fiebig A, Buddruhs N, et al. (2013) opm: an R package for analysing OmniLog(R) phenotype microarray data. Bioinformatics 29: 1823-1824.
70. Kindt R, Coe R (2005) Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies.
71. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. (2013) vegan: Community Ecology Package. R package version 2.0-8.
72. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50: 346-363.
73. Herberich E, Sikorski J, Hothorn T (2010) A robust procedure for comparing multiple means under heteroscedasticity in unbalanced designs. PLoS One 5: e9788.
74. García P, Madera C, Martínez B, Rodríguez A (2007) Biocontrol of Staphylococcus aureus in curd manufacturing processes using bacteriophages. International Dairy Journal 17: 1232-1239.
75. Beilstein F, Dreiseikelmann B (2006) Bacteriophages of freshwater Brevundimonas vesicularis isolates. Res Microbiol 157: 213-219.
76. Valentine RC, Shapiro BM, Stadtman ER (1968) Regulation of glutamine synthetase. XII. Electron microscopy of the enzyme from Escherichia coli. Biochemistry 7: 2143-2152.
77. Capparelli R, Nocerino N, Lanzetta R, Silipo A, Amoresano A, et al. (2010) Bacteriophage-resistant Staphylococcus aureus mutant confers broad immunity against staphylococcal infection in mice. PLoS One 5: e11720.