Abstract
Stenotrophomonas maltophilia (Sm), with most of the isolates being resistant to multidrugs, is an opportunistic bacterium causing nosocomial infections. In this study, a novel virulent Sm phage, Smp14, was characterized. Electron microscopy showed that Smp14 resembled members of Myoviridae and adsorbed to poles of the host cells during infection. It lysed 37 of 87 clinical Sm isolates in spot test, displayed a latent period of ca. 20 min, and had a burst size of ca. 150. Its genome (estimated to be 160 kb by PFGE), containing m4C and two unknown modified bases other than m5C and m6A as identified by HPLC, resisted to digestion with many restriction endonucleases except MseI. These properties indicate that it is a novel Sm phage distinct from the previously reported phiSMA5 which has a genome of 250 kb digestible with various restriction enzymes. Sequencing of a 16 kb region revealed 12 ORFs encoding structural proteins sharing 15–45% identities with the homologues from T4-type phages. SDS-PAGE displayed 20 virion proteins, with the most abundant one being the 39 kDa major capsid protein (gp23), which had the N-terminal 52 amino acids removed. Phylogenetic analysis based on gp23 classified Smp14 into a novel single-membered T4-type subgroup.
References
Ackermann HW (2001) Frequency of morphological phage descriptions in the year 2000. Arch Virol 146:843–857
Ackermann HW (2003) Bacteriophage observations and evolution. Res Microbiol 154:245–251
Aznar R, Alcaide E (1992) Siderophores and related outer membrane proteins produced by pseudomonads isolated from eels and freshwater. FEMS Microbiol Lett 77:269–275
Baek JE, Jung EY, Kim HJ, Lee GW, Hahm JR, Kang KR, Chang SH (2004) Stenotrophomonas maltophilia infection in patients receiving continuous ambulatory peritoneal dialysis. Korean J Intern Med 19:104–108
Ballestero S, Virseda I, Escobar H, Suarez L, Baquero F (1995) Stenotrophomonas maltophilia in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis 14:728–729
Byrne M, Kropinski AM (2005) The genome of the Pseudomonas aeruginosa generalized transducing bacteriophage F116. Gene 346:187–194
Chang HC, Chen CR, Lin JW, Shen GH, Chang KM, Tseng YH, Weng SF (2005) Isolation and characterization of novel giant Stenotrophomonas maltophilia phage phiSMA5. Appl Environ Microbiol 71:1387–1393
Chibani-Chennoufi S, Canchaya C, Bruttin A, Brussow H (2004) Comparative genomics of the T4-Like Escherichia coli phage JS98: implications for the evolution of T4 phages. J Bacteriol 186:8276–8286
Crowlesmith I, Schindler M, Osborn MJ (1978) Bacteriophage P22 is not a likely probe for zones of adhesion between the inner and outer membranes of Salmonella typhimurium. J Bacteriol 135:259–269
Desplats C, Dez C, Tetart F, Eleaume H, Krisch HM (2002) Snapshot of the genome of the pseudo-T-even bacteriophage RB49. J Bacteriol 184:2789–2804
Ehrlich M, Wilson GG, Kuo KC, Gehrke CW (1987) N4-methylcytosine as a minor base in bacterial DNA. J Bacteriol 169:939–943
Filee J, Tetart F, Suttle CA, Krisch HM (2005) Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere. Proc Natl Acad Sci USA 102:12471–12476
Fisher MC, Long SS, Roberts EM, Dunn JM, Balsara RK (1981) Pseudomonas maltophilia bacteremia in children undergoing open heart surgery. Jama 246:1571–1574
Foschino R, Perrone F, Galli A (1995) Characterization of two virulent Lactobacillus fermentum bacteriophages isolated from sour dough. J Appl Bacteriol 79:677–683
Hagemann M, Hasse D, Berg G (2006) Detection of a Phage Genome Carrying a Zonula Occludens like Toxin Gene (zot) in clinical isolates of Stenotrophomonas maltophilia. Arch Microbiol 185:449–458
Hauben L, Vauterin L, Moore ER, Hoste B, Swings J (1999) Genomic diversity of the genus Stenotrophomonas. Int J Syst Bacteriol 49:1749–1760
Hausmann C, Clowes RC (1971) ColB2-K77, a fertility-repressed F-like factor. J Bacteriol 107:900–906
Hugh R (1981) Pseudomonas maltophilia sp. nov., nom. rev. Int J Syst Bacteriol 31:195
Isobe T, Black LW, Tsugita A (1976) Protein cleavage during virus assembly: a novel specificity of assembly dependent cleavage in bacteriophage T4. Proc Natl Acad Sci USA 73:4205–4209
Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405
Juhnke ME, Mathre DE, Sands DC (1987) Identification and Characterization of Rhizosphere-ompetent bacteria of wheat. Appl Environ Microbiol 53:2793–2799
Kim CK, Gentile DM, Sproul OJ (1980) Mechanism of ozone inactivation of bacteriophage f2. Appl Environ Microbiol 39:210–218
Kim JH, Kim SW, Kang HR, Bae GB, Park JH, Nam EJ, Kang YM, Lee JM, Kim NS (2002) Two episodes of Stenotrophomonas maltophilia endocarditis of prosthetic mitral valve: report of a case and review of the literature. J Korean Med Sci 17:263–265
Koike M, Iida K (1971) Effect of polymyxin on the bacteriophage receptors of the cell walls of gram-negative bacteria. J Bacteriol 108:1402–1411
Kumar V, Balaji S, Gomathi NS, Venkatesan P, Sekar G, Jayasankar K, Narayanan PR (2007) Phage cocktail to control the exponential growth of normal flora in processed sputum specimens grown overnight in liquid medium for rapid TB diagnosis. J Microbiol Methods 68:536–542
Lambert T, Ploy MC, Denis F, Courvalin P (1999) Characterization of the chromosomal aac(6′)-Iz gene of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 43:2366–2371
Li XZ, Zhang L, McKay GA, Poole K (2003) Role of the acetyltransferase AAC(6′)-Iz modifying enzyme in aminoglycoside resistance in Stenotrophomonas maltophilia. J Antimicrob Chemother 51:803–811
Mesyanzhinov VV, Leiman PG, Kostyuchenko VA, Kurochkina LP, Miroshnikov KA, Sykilinda NN, Shneider MM (2004) Molecular architecture of bacteriophage T4. Biochemistry (Mosc) 69:1190–1202
Miller ES, Kutter E, Mosig G, Arisaka F, Kunisawa T, Ruger W (2003) Bacteriophage T4 genome. Microbiol Mol Biol Rev 67:86–156
Muder RR, Harris AP, Muller S, Edmond M, Chow JW, Papadakis K, Wagener MW, Bodey GP, Steckelberg JM (1996) Bacteremia due to Stenotrophomonas (Xanthomonas) maltophilia: a prospective, multicenter study of 91 episodes. Clin Infect Dis 22:508–512
Nolan JM, Petrov V, Bertrand C, Krisch HM, Karam JD (2006) Genetic diversity among five T4-like bacteriophages. Virol J 3:30
Page RD (1996) Tree view: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Pajunen M, Kiljunen S, Skurnik M (2000) Bacteriophage phiYeO3–12, specific for Yersinia enterocolitica serotype O:3, is related to coliphages T3 and T7. J Bacteriol 182:5114–5120
Palleroni NJ, Bradbury JF (1993) Stenotrophomonas, a new bacterial genus for Xanthomonas maltophilia (Hugh 1980) Swings et al. 1983. Int J Syst Bacteriol 43:606–609
Roilides E, Butler KM, Husson RN, Mueller BU, Lewis LL, Pizzo PA (1992) Pseudomonas infections in children with human immunodeficiency virus infection. Pediatr Infect Dis J 11:547–553
Ryter A, Shuman H, Schwartz M (1975) Intergration of the receptor for bacteriophage lambda in the outer membrane of Escherichia coli: coupling with cell division. J Bacteriol 122:295–301
Skerker JM, Shapiro L (2000) Identification and cell cycle control of a novel pilus system in Caulobacter crescentus. Embo J 19:3223–3234
Smirnova TA, Netyksa EM, Minenkova IB, Smirnov BB, Azizbekian RR (1979) [Electron microscopic study of the interaction between phages and Bacillus thuringiensis cells]. Mikrobiologiia 48:880–886
Sommer JM, Newton A (1988) Sequential regulation of developmental events during polar morphogenesis in Caulobacter crescentus: assembly of pili on swarmer cells requires cell separation. J Bacteriol 170:409–415
Spencer J, Clarke AR, Walsh TR (2001) Novel mechanism of hydrolysis of therapeutic beta-lactams by Stenotrophomonas maltophilia L1 metallo-beta-lactamase. J Biol Chem 276:33638–33644
Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW (2005) Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3:790–806
Tosi M, Anderson DL (1973) Antigenic properties of bacteriophage phi 29 structural proteins. J Virol 12:1548–1559
Vartivarian S, Anaissie E, Bodey G, Sprigg H, Rolston K (1994) A changing pattern of susceptibility of Xanthomonas maltophilia to antimicrobial agents: implications for therapy. Antimicrob Agents Chemother 38:624–627
Vartivarian SE, Papadakis KA, Anaissie EJ (1996) Stenotrophomonas (Xanthomonas) maltophilia urinary tract infection. A disease that is usually severe and complicated. Arch Intern Med 156:433–435
Wang WS, Liu CP, Lee CM, Huang FY (2004) Stenotrophomonas maltophilia bacteremia in adults: four years’ experience in a medical center in northern Taiwan. J Microbiol Immunol Infect 37:359–365
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Communicated by Jorge Membrillo-Hernández.
Chiy-Rong Chen and Ching-Hsuan Lin contributed equally.
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Chen, CR., Lin, CH., Lin, JW. et al. Characterization of a novel T4-type Stenotrophomonas maltophilia virulent phage Smp14. Arch Microbiol 188, 191–197 (2007). https://doi.org/10.1007/s00203-007-0238-5
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DOI: https://doi.org/10.1007/s00203-007-0238-5