Characterization of a ViI-like Phage Specific to Escherichia coli O157:H7

Virology Journal

Andrew D Brabban⁵  Todd Callaway⁷  Hany Anany^1,10  Derek Pickard⁹  Ana L Toribio⁹  Hans-Wolfgang Ackermann¹  Andre Villegas⁶  Andrew M Kropinski²  Daniel Bryan⁵  Anna Castano⁸  Ayman El-Shibiny³  Bob Blasdel⁴  Kyobi Skutt-Kakaria⁵  Elizabeth M Kutter⁵ 

[1] Department of Microbiology, Faculty of Medicine, Laval University, Quebec, QC, Canada;Department of Molecular & Cellular Biology, University of Guelph, ON, Canada;Faculty of Environmental Agricultural Sciences, Suez Canal University, Egypt;Department of Microbiology, The Ohio State University, Columbus, OH;The Evergreen State College, Olympia, WA, USA;Laboratory for Foodborne Zoonoses, Public Health Agency of Canada, Guelph, ON, Canada;USDA Agricultural Station, College Station, TX, USA;Department of Pediatric Neurology, University of Colorado Children's Hospital, Denver, CO;The Wellcome Trust Sanger Institute, Genome Campus, Hinxton, England, UK;Microbiology Department, Ain Shams University, Cairo, Egypt

关键词: T4 core genes;    tail spike;    O157 antigen;    Vi antigen;    bioinformatics;    proteome;    genome;    phage ecology;    phage evolution;    hydroxymethyluracil;    E. coli O157:H7;   

Others  :  1156137
DOI  :  10.1186/1743-422X-8-430

 received in 2011-08-04, accepted in 2011-09-07,  发布年份 2011

【 摘 要 】

Phage vB_EcoM_CBA120 (CBA120), isolated against Escherichia coli O157:H7 from a cattle feedlot, is morphologically very similar to the classic phage ViI of Salmonella enterica serovar Typhi. Until recently, little was known genetically or physiologically about the ViI-like phages, and none targeting E. coli have been described in the literature. The genome of CBA120 has been fully sequenced and is highly similar to those of both ViI and the Shigella phage AG3. The core set of structural and replication-related proteins of CBA120 are homologous to those from T-even phages, but generally are more closely related to those from T4-like phages of Vibrio, Aeromonas and cyanobacteria than those of the Enterobacteriaceae. The baseplate and method of adhesion to the host are, however, very different from those of either T4 or the cyanophages. None of the outer baseplate proteins are conserved. Instead of T4's long and short tail fibers, CBA120, like ViI, encodes tail spikes related to those normally seen on podoviruses. The 158 kb genome, like that of T4, is circularly permuted and terminally redundant, but unlike T4 CBA120 does not substitute hmdCyt for cytosine in its DNA. However, in contrast to other coliphages, CBA120 and related coliphages we have isolated cannot incorporate ³H-thymidine (³H-dThd) into their DNA. Protein sequence comparisons cluster the putative "thymidylate synthase" of CBA120, ViI and AG3 much more closely with those of Delftia phage φW-14, Bacillus subtilis phage SPO1, and Pseudomonas phage YuA, all known to produce and incorporate hydroxymethyluracil (hmdUra).

【 授权许可】

   
2011 Kutter et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】

• [1]Abuladze T, Li M, Menetrez MY, Dean T, Senecal A, Sulakvelidze A: Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157:H7. Appl Environ Microbiol 2008, 74:6230-6238.
• [2]Atterbury RJ: Bacteriophage biocontrol in animals and meat products. Microb Biotechnol 2009, 2:601-612.
• [3]Mahony J, Mauliffe O, Ross RP, van Sinderen D: Bacteriophages as biocontrol agents of food pathogens. Current Opinion in Biotechnology 2011, 22:157-163.
• [4]Parviz S, Griffiths MW: Bacteriophages in the Control of Food- and Water-borne Pathogens. Washington, DC: ASM Press; 2010.
• [5]Rees CE, Dodd CE: Phage for rapid detection and control of bacterial pathogens in food. Adv Appl Microbiol 2006, 59:159-186.
• [6]Sulakvelidze A, Barrow P: Phage therapy in animals and agribusiness. In Bacteriophages: biology and applications. Edited by Kutter E, Sulakvelidse A. Washington, D.C.: CRC Press; 2005:335-380.
• [7]Bach SA, McAllistera TA, Veirab DM, Gannonc VPJ, Holley RA: Effect of bacteriophage DC22 on Escherichia coli O157:H7 in an artificial rumen system (Rusitec) and inoculated sheep. Anim Res 2003, 52:89-101.
• [8]Callaway TR, Edrington TS, Brabban AD, Anderson RC, Rossman ML, Engler MJ, Carr MA, Genovese KJ, Keen JE, Looper ML, et al.: Bacteriophage isolated from feedlot cattle can reduce Escherichia coli O157:H7 populations in ruminant gastrointestinal tracts. Foodborne Pathog Dis 2008, 5:183-191.
• [9]Johnson RP, Gyles CL, Huff WE, Ojha S, Huff GR, Rath NC, Donoghue AM: Bacteriophages for prophylaxis and therapy in cattle, poultry, and pigs. Anim Health Res Rev 2008, 9:201-215.
• [10]Kudva IT, Jelacic S, Tarr PI, Youderian P, Hovde CJ: Biocontrol of Escherichia coli O157 with O157-specific bacteriophages. Appl Environ Microbiol 1999, 65:3767-3773.
• [11]Loc Carrillo C, Atterbury RJ, El-Shibiny A, Connerton PL, Dillon E, Scott A, Connerton IF: Bacteriophage Therapy To Reduce Campylobacter jejuni Colonization of Broiler Chickens. Appl Environ Microbiol 2005, 71:6554-6563.
• [12]Raya RR, Oot RA, Moore-Maley B, Wieland S, Callaway TR, Kutter EM, Brabban AD: Naturally resident and exogenously applied T4-like and T5-like bacteriophages can reduce Escherichia coli O157:H7 levels in sheep guts. Bacteriophage 2011, 1:15-24.
• [13]Raya RR, Varey P, Oot RA, Dyen MR, Callaway TR, Edrington TS, Kutter EM, Brabban AD: Isolation and characterization of a new T-even bacteriophage, CEV1, and determination of its potential to reduce Escherichia coli O157:H7 levels in sheep. Appl Environ Microbiol 2006, 72:6405-6410.
• [14]Sheng H, Knecht HJ, Kudva IT, Hovde CJ: Application of bacteriophages to control intestinal Escherichia coli O157:H7 levels in ruminants. Appl Environ Microbiol 2006, 72:5359-5366.
• [15]El-Shibiny A, Scott A, Timms A, Metawea Y, Connerton P, Connerton I: Application of a group II Campylobacter bacteriophage to reduce strains of Campylobacter jejuni and Campylobacter coli colonizing broiler chickens. J Food Prot 2009, 72:733-740.
• [16]Niu YD, McAllister TA, Xu Y, Johnson RP, Stephens TP, Stanford K: Prevalence and impact of bacteriophages on the presence of Escherichia coli O157:H7 in feedlot cattle and their environment. Appl Environ Microbiol 2009, 75:1271-1278.
• [17]Callaway TR, Edrington TS, Brabban AD, Keen JE, Anderson RC, Rossman ML, Engler MJ, Genovese KJ, Gwartney BL, Reagan JO, et al.: Fecal prevalence of Escherichia coli O157, Salmonella, Listeria, and Bacteriophage Infecting E. coli O157:H7 in feedlot cattle in the Southern Plains region of the United States. Foodborne Pathog Dis 2006, 3:234-244.
• [18]Oot RA, Raya RR, Callaway TR, Edrington TS, Kutter EM, Brabban AD: Prevalence of Escherichia coli O157 and O157:H7-infecting bacteriophages in feedlot cattle feces. Lett Appl Microbiol 2007, 45:445-453.
• [19]Ackermann HW, Berthiaume L, Kasatiya SS: Ultrastructure of Vi phages I to VII of Salmonella typhi. Can J Microbiol 1970, 16:411-413.
• [20]Pickard D, Toribio AL, Petty NK, van Tonder A, Yu L, Goulding D, Barrell B, Rance R, Harris D, Wetter M, et al.: A conserved acetyl esterase domain targets diverse bacteriophages to the Vi capsular receptor of Salmonella enterica serovar Typhi. J Bacteriol 2010, 192:5746-5754.
• [21]Boyce P, Setlow RB: Simple method of increasing the incorporation of thymidine into the DNAQ of E. coli. Biochim Biophys Acta 1962, 61:618-620.
• [22]Anany H, Lingohr EJ, Villegas A, Ackermann HW, She YM, Griffiths MW, Kropinski AM: A Shigella boydii bacteriophage which resembles Salmonella phage ViI. Virol J 2011, 8:242. BioMed Central Full Text
• [23]Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J: ACT: the Artemis Comparison Tool. Bioinformatics 2005, 21:3422-3423.
• [24]Karam JD, Drake JW, Kreuzer KN, Mosig G, Hall DH, Eiserling FA, Black LW, Spicer EK, Kutter E, Carlson C, Miller ES: Molecular biology of bacteriophage T4. Washington, D.C.: ASM Press; 1994.
• [25]Leiman PG, Arisaka F, van Raaij MJ, Kostyuchenko VA, Aksyuk AA, Kanamaru S, Rossmann MG: Morphogenesis of the T4 tail and tail fibers. Virol J 2010, 7:355. BioMed Central Full Text
• [26]Mathews CK, Kutter E, Mosig G, Berget PB: Bacteriophage T4. Washington, D.C.: ASM Press; 1983.
• [27]Miller ES, Heidelberg JF, Eisen JA, Nelson WC, Durkin AS, Ciecko A, Feldblyum TV, White O, Paulsen IT, Nierman WC, et al.: Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4-related bacteriophage. J Bacteriol 2003, 185:5220-5233.
• [28]Petrov VM, Ratnayaka S, Nolan JM, Miller ES, Karam JD: Genomes of the T4-related bacteriophages as windows on microbial genome evolution. Virol J 2010, 7:292. BioMed Central Full Text
• [29]Geiduschek EP, Kassavetis GA: Transcription of the T4 late genes. Virol J 2010, 7:288. BioMed Central Full Text
• [30]Clokie MR, Millard AD, Mann NH: T4 genes in the marine ecosystem: studies of the T4-like cyanophages and their role in marine ecology. Virol J 2010, 7:291. BioMed Central Full Text
• [31]Hoet PP, Coene MM, Cocito CG: Replication cycle of Bacillus subtilis hydroxymethyluracil-containing phages. Annu Rev Microbiol 1992, 46:95-116.
• [32]Stewart CR, Casjens SR, Cresawn SG, Houtz JM, Smith AL, Ford ME, Peebles CL, Hatfull GF, Hendrix RW, Huang WM, Pedulla ML: The genome of Bacillus subtilis bacteriophage SPO1. J Mol Biol 2009, 388:48-70.
• [33]Kropinski AM, Bose RJ, Warren RA: 5-(4-Aminobutylaminomethyl)uracil, an unusual pyrimidine from the deoxyribonucleic acid of bacteriophage phiW-14. Biochemistry 1973, 12:151-157.
• [34]Maltman KL, Neuhard J, Warren RA: 5-[(Hydroxymethyl)-O-pyrophosphoryl]uracil, an intermediate in the biosynthesis of alpha-putrescinylthymine in deoxyribonucleic acid of bacteriophage phi W-14. Biochemistry 1981, 20:3586-3591.
• [35]Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL, et al.: The Pfam protein families database. Nucleic Acids Res 2004, 32:D138-141.
• [36]Walter M, Fiedler C, Grassl R, Biebl M, Rachel R, Hermo-Parrado XL, Llamas-Saiz AL, Seckler R, Miller S, van Raaij MJ: Structure of the receptor-binding protein of bacteriophage det7: a podoviral tail spike in a myovirus. J Virol 2008, 82:2265-2273.
• [37]Craigie J, Yen CH: The demonstration of types of B. typhosus by means of preparations of Type II Vi phage: The stability and Epidemiological significance of V form types of B. typhosus. Canadian Public Health Journal 1938, 29:484-496.
• [38]Desranleau JM: Progress in the treatment of typhoid fever with Vi bacteriophages. Can J Public Health 1949, 40:473-478.
• [39]Werquin M, Ackermann HW, Levesque RC: A Study of 33 Bacteriophages of Rhizobium meliloti. Appl Environ Microbiol 1988, 54:188-196.
• [40]Ackermann HW, Brochu G, Emadi Konjin HP: Classification of Acinetobacter phages. Arch Virol 1994, 135:345-354.
• [41]Lin NT, Chiou PY, Chang KC, Chen LK, Lai MJ: Isolation and characterization of phi AB2: a novel bacteriophage of Acinetobacter baumannii. Res Microbiol 2010, 161:308-314.
• [42]Sullivan MB, Huang KH, Ignacio-Espinoza JC, Berlin AM, Kelly L, Weigele PR, DeFrancesco AS, Kern SE, Thompson LR, Young S, et al.: Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol 2010, 12:3035-3056.
• [43]Chibani-Chennoufi S, Sidoti J, Bruttin A, Dillmann ML, Kutter E, Qadri F, Sarker SA, Brussow H: Isolation of Escherichia coli bacteriophages from the stool of pediatric diarrhea patients in Bangladesh. J Bacteriol 2004, 186:8287-8294.
• [44]Kutter E, Gachechiladze K, Poglazov A, Marusich E, Shneider M, Aronsson P, Napuli A, Porter D, Mesyanzhinov V: Evolution of T4-related phages. Virus Genes 1995, 11:285-297.
• [45]Nolan JM, Petrov V, Bertrand C, Krisch HM, Karam JD: Genetic diversity among five T4-like bacteriophages. Virol J 2006, 3:30. BioMed Central Full Text
• [46]Petrov VM, Nolan JM, Bertrand C, Levy D, Desplats C, Krisch HM, Karam JD: Plasticity of the gene functions for DNA replication in the T4-like phages. J Mol Biol 2006, 361:46-68.
• [47]Kropinski AM, Warren RA: Isolation and properties of a Pseudomonas acidovorans bacteriophage. J Gen Virol 1970, 6:85-93.
• [48]Young R, Wang I-N: Phage Lysis. In The Bacteriophages. Edited by Calendar R. Oxford University Press; 2006:104-125. 2nd
• [49]Morley TJ, Willis LM, Whitfield C, Wakarchuk WW, Withers SG: A New Sialidase Mechanism. Journal of Biological Chemistry 2009, 284:17404-17410.
• [50]Leiman PG, Battisti AJ, Bowman VD, Stummeyer K, Muhlenhoff M, Gerardy-Schahn R, Scholl D, Molineux IJ: The structures of bacteriophages K1E and K1-5 explain processive degradation of polysaccharide capsules and evolution of new host specificities. J Mol Biol 2007, 371:836-849.
• [51]Peleg A, Shifrin Y, Ilan O, Nadler-Yona C, Nov S, Koby S, Baruch K, Altuvia S, Elgrably-Weiss M, Abe CM, et al.: Identification of an Escherichia coli operon required for formation of the O-antigen capsule. J Bacteriol 2005, 187:5259-5266.
• [52]Shifrin Y, Peleg A, Ilan O, Nadler C, Kobi S, Baruch K, Yerushalmi G, Berdichevsky T, Altuvia S, Elgrably-Weiss M, et al.: Transient shielding of intimin and the type III secretion system of enterohemorrhagic and enteropathogenic Escherichia coli by a group 4 capsule. J Bacteriol 2008, 190:5063-5074.
• [53]Samuel G, Hogbin JP, Wang L, Reeves PR: Relationships of the Escherichia coli O157, O111, and O55 O-antigen gene clusters with those of Salmonella enterica and Citrobacter freundii, which express identical O antigens. J Bacteriol 2004, 186:6536-6543.
• [54]Hinton DM: Transcriptional control in the prereplicative phase of T4 development. Virol J 2010, 7:289. BioMed Central Full Text
• [55]Liebig HD, Ruger W: Bacteriophage T4 early promoter regions. Consensus sequences of promoters and ribosome-binding sites. J Mol Biol 1989, 208:517-536.
• [56]Kashlev M, Nudler E, Goldfarb A, White T, Kutter E: Bacteriophage T4 Alc protein: a transcription termination factor sensing local modification of DNA. Cell 1993, 75:147-154.
• [57]Kutter EM, Bradley D, Schenck R, Guttman BS, Laiken R: Bacteriophage T4 alc gene product: general inhibitor of transcription from cytosine-containing DNA. J Virol 1981, 40:822-829.
• [58]Paddison P, Abedon ST, Dressman HK, Gailbreath K, Tracy J, Mosser E, Neitzel J, Guttman B, Kutter E: The roles of the bacteriophage T4 r genes in lysis inhibition and fine-structure genetics: a new perspective. Genetics 1998, 148:1539-1550.
• [59]Ramanculov E, Young R: An ancient player unmasked: T4 rI encodes a t-specific antiholin. Mol Microbiol 2001, 41:575-583.
• [60]Tran TA, Struck DK, Young R: The T4 RI antiholin has an N-terminal signal anchor release domain that targets it for degradation by DegP. J Bacteriol 2007, 189:7618-7625.
• [61]Kutter E: Phage Host Range and Efficiency of Plating. In Bacteriophages. Volume 501. Edited by Clokie MRJ. Kropinski AM: Humana Press; 2009::141-149. Methods in Molecular Biology
• [62]Ochman H, Selander RK: Standard reference strains of Escherichia coli from natural populations. J Bacteriol 1984, 157:690-693.
• [63]Carlson K: Appendix: working with bacteriophages: common techniques and methodological approaches. In Bacteriophages: biology and applications. Edited by Kutter E, Sulakvelidse A. Washington, D.C.: CRC Press; 2005:437-494.
• [64]Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B: Artemis: sequence visualization and annotation. Bioinformatics 2000, 16:944-945.
• [65]Koski LB, Gray MW, Lang BF, Burger G: AutoFACT: an automatic functional annotation and classification tool. BMC Bioinformatics 2005, 6:151. BioMed Central Full Text
• [66]Carver T, Berriman M, Tivey A, Patel C, Bohme U, Barrell BG, Parkhill J, Rajandream MA: Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 2008, 24:2672-2676.
• [67]Coggill P, Finn RD, Bateman A: Identifying Protein Domains with the Pfam Database. In Current Protocols in Bioinformatics. John Wiley & Sons, Inc.; 2002.
• [68]Shine J, Dalgarno L: Determinant of cistron specificity in bacterial ribosomes. Nature 1975, 254:34-38.
• [69]Kropinski AM, Borodovsky M, Carver TJ, Cerdeno-Tarraga AM, Darling A, Lomsadze A, Mahadevan P, Stothard P, Seto D, Van Domselaar G, Wishart DS: In silico identification of genes in bacteriophage DNA. Methods Mol Biol 2009, 502:57-89.
• [70]Zafar N, Mazumder R, Seto D: CoreGenes: a computational tool for identifying and cataloging "core" genes in a set of small genomes. BMC Bioinformatics 2002, 3:12. BioMed Central Full Text
• [71]Krogh A, Larsson B, von Heijne G, Sonnhammer EL: Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001, 305:567-580.
• [72]Laslett D, Canback B: ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 2004, 32:11-16.
• [73]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
• [74]Pearson WR, Lipman DJ: Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 1988, 85:2444-2448.