Genomic characterization provides new insight into Salmonella phage diversity

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Moreno Switt, Andrea I ^a   Orsi, Renato H ^a   den Bakker, Henk C ^a   Vongkamjan, Kitiya ^a   Altier, Craig ^a   Wiedmann, Martin ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Phage genomics; Salmonella phage

Indexed keywords

ADHESIN; BICOZAMYCIN; CHEMICAL COMPOUND; TELLURITE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DAIRYING; GENE CLUSTER; GENE REARRANGEMENT; GENOME ANALYSIS; MICROBIAL DIVERSITY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; SALMONELLA PHAGE; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; UNITED STATES; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS ISOLATION; VIRUS MORPHOLOGY; VIRUS VIRULENCE;

AMINO ACID SEQUENCE; ANTI-INFECTIVE AGENTS; BACTERIOPHAGES; CLUSTER ANALYSIS; DNA, VIRAL; DRUG RESISTANCE, VIRAL; ENVIRONMENT; GENETIC VARIATION; GENOMICS; MOLECULAR SEQUENCE DATA; POLYMORPHISM, SINGLE NUCLEOTIDE; SALMONELLA; VIRAL PROTEINS;

SALMONELLA;

EID: 84881030007     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-481     Document Type: Article

References (83)

1. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 2010, 50:882-889. 10.1086/650733, 20158401.
2. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 2011, 17:7-15. 3375761, 21192848.
3. Hoelzer K, Moreno Switt AI, Wiedmann M. Animal contact as a source of human non-typhoidal salmonellosis. Vet Res 2011, 42:34. 10.1186/1297-9716-42-34, 3052180, 21324103.
4. Cummings KJ, Warnick LD, Elton M, Gröhn YT, McDonough PL, Siler JD. The effect of clinical outbreaks of salmonellosis on the prevalence of fecal Salmonella shedding among dairy cattle in New York. Foodborne Pathog Dis 2010, 7:815-823. 10.1089/fpd.2009.0481, 3132070, 20353290.
5. Van Kessel JA, Karns JS, Lombard JE, Kopral CA. Prevalence of Salmonella enterica, Listeria monocytogenes, and Escherichia coli virulence factors in bulk tank milk and in-line filters from U.S. dairies. J Food Prot 2011, 74:759-768.
6. [CDC] Center for Disease Control and Prevention Salmonella: annual summary (2009) 2007, Atlanta, GA: CDC, Division of Bacterial and Mycotic Diseases, http://www.cdc.gov/ncezid/dfwed/PDFs/SalmonellaAnnualSummaryTables2009.pdf, [CDC] Center for Disease Control and Prevention.
7. Moreno Switt AI, den Bakker HC, Vongkamjan K, Hoelzer K, Warnick LD, Cummings KJ, Wiedmann M. Salmonella bacteriophage diversity reflects host diversity on dairy farms. Food Microbiol 2013, 36:275-285.
8. Kropinski AM, Sulakvelidze A, Konczy P, Poppe C. Salmonella phages and prophages-genomics and practical aspects. Methods Mol Biol 2007, 394:133-75. 10.1007/978-1-59745-512-1_9, 18363236.
9. Suttle CA. Marine viruses-major players in the global ecosystem. Nat Rev Microbiol 2007, 5:801-12. 10.1038/nrmicro1750, 17853907.
10. Casjens SR, Gilcrease EB, Winn-stapley DA, Schicklmaier P, Schmieger H, Pedulla ML, Ford ME, Houtz JM, Hatfull GF, Hendrix RW. The generalized transducing Salmonella bacteriophage ES18: complete genome sequence and DNA packaging strategy. J Bacteriol 2005, 187:1091-1104. 10.1128/JB.187.3.1091-1104.2005, 545730, 15659686.
11. Weinbauer MG, Rassoulzadegan F. Are viruses driving microbial diversification and diversity?. Environ Microbiol 2004, 6:1-11.
12. Hooton SP, Timms AR, Rowsell J, Wilson R, Connerton IF. Salmonella Typhimurium-specific bacteriophage ΦSH19 and the origins of species specificity in the Vi01-like phage family. Virol J 2011, 8:498. 10.1186/1743-422X-8-498, 3220722, 22047448.
13. Price-Carter M, Roy-Chowdhury P, Pope CE, Paine S, de Lisle GW, Collins DM, Nicol C, Carter PE. The evolution and distribution of phage ST160 within Salmonella enterica serotype Typhimurium. Epidemiol Infect 2011, 139:1262-71. 10.1017/S0950268810002335, 20950514.
14. Santos SB, Kropinski AM, Ceyssens PJ, Ackermann HW, Villegas A, Lavigne R, Krylov VN, Carvalho CM, Ferreira EC, Azeredo J. Genomic and proteomic characterization of the broad host range Salmonella phage PVP-SE1 - The creation of a new phage genus. J Virol 2011, 85:11265-73. 10.1128/JVI.01769-10, 3194984, 21865376.
15. Lee JH, Shin H, Ryu S. Complete genome sequence of Salmonella enterica serovar Typhimurium bacteriophage SPN3UB. J Virol 2012, 86:3404-5. 10.1128/JVI.07226-11, 3302332, 22354944.
16. Shin H, Lee JH, Lim JA, Kim H, Ryu S. Complete genome sequence of Salmonella enterica serovar Typhimurium bacteriophage SPN1S. J Virol 2012, 86:1284-5. 10.1128/JVI.06696-11, 3255854, 22205721.
17. Jacobsen A, Hendriksen RS, Aaresturp FM, Ussery DW, Friis C. The Salmonella enterica pan-genome. Microb Ecol 2011, 62:487-504. 10.1007/s00248-011-9880-1, 3175032, 21643699.
18. Den Bakker HC, Moreno Switt AI, Govoni G, Cummings CA, Ranieri ML, Degoricija L, Hoelzer K, Rodriguez-Rivera LD, Brown S, Bolchacova E, Furtado MR, Wiedmann M. Genome sequencing reveals diversification of virulence factor content and possible host adaptation in distinct subpopulations of Salmonella enterica. BMC Genomics 2011, 12:425. 10.1186/1471-2164-12-425, 3176500, 21859443.
19. Fricke WF, Mammel MK, McDermott PF, Tartera C, White DG, Leclerc JE, Ravel J, Cebula TA. Comparative genomics of 28 Salmonella enterica isolates: evidence for CRISPR-mediated adaptive sublineage evolution. J Bacteriol 2011, 193:3556-68. 10.1128/JB.00297-11, 3133335, 21602358.
20. Lee JH, Shin H, Kim H, Ryu S. Complete genome sequence of Salmonella bacteriophage SPN3US. J Virol 2011, 85:13470-1. 10.1128/JVI.06344-11, 3233126, 22106383.
21. Villegas A, She YM, Kropinski AM, Lingohr EJ, Mazzocco A, Ojha S, Waddell TE, Ackermann HW, Moyles DM, Ahmed R, Johnson RP. The genome and proteome of a virulent Escherichia coli O157:H7 bacteriophage closely resembling Salmonella phage Felix O1. Virol J 2009, 6:41. 10.1186/1743-422X-6-41, 2674420, 19379502.
22. Pope WH, Jacobs-Sera D, Russell DA, et al. Expanding the diversity of mycobacteriophages: insights into genome architecture and evolution. PLoS One 2011, 6:e16329. 10.1371/journal.pone.0016329, 3029335, 21298013.
23. Hatfull GF, Jacobs-Sera D, Lawrence JG, Pope WH, Russell DA, Ko CC, Weber RJ, Patel MC, Germane KL, Edgar RH, Hoyte NN, Bowman CA, Tantoco AT, Paladin EC, Myers MS, Smith AL, Grace MS, Pham TT, O'Brien MB, Vogelsberger AM, Hryckowian AJ, Wynalek JL, Donis-Keller H, Bogel MW, Peebles CL, Cresawn SG, Hendrix RW. Comparative genomic analysis of 60 Mycobacteriophage genomes: genome clustering, gene acquisition, and gene size. J Mol Biol 2010, 397:119-43. 10.1016/j.jmb.2010.01.011, 2830324, 20064525.
24. Cresawn SG, Bogel M, Day N, Jacobs-Sera D, Hendrix RW, Hatfull GF. Phamerator: a bioinformatic tool for comparative bacteriophage genomics. BMC Bioinformatics 2011, 12:395. 10.1186/1471-2105-12-395, 3233612, 21991981.
25. International commitee on virus taxonomy. Virus Taxonomy Virus Taxonomy: 2012 Release (current) http://ictvonline.org/virusTaxonomy.asp?version=2012&bhcp=1, International commitee on virus taxonomy. Virus Taxonomy.
26. Bullas LR, Mostaghimi AR, Arensdorf JJ, Rajadas PT, Zuccarelli AJ. Salmonella phage PSP3, another member of the P2-like phage group. Virology 1992, 188:414.
27. Hoelzer K, Cummings KJ, Wright EM, Rodriguez-Rivera LD, Roof SE, Moreno Switt AI, Dumas N, Root T, Schoonmaker-Bopp DJ, Grohn YT, Siler JD, Warnick LD, Hancock DD, Davis MA, Wiedmann M. Salmonella Cerro isolated over the past twenty years from various sources in the US represent a single predominant pulsed-field gel electrophoresis type. Vet Microbiol 2011, 150:389-93. 10.1016/j.vetmic.2011.01.026, 3095722, 21349663.
28. Wang YC, Chang YC, Chuang HL, Chiu CC, Yeh KS, Chang CC, Hsuan SL, Lin WH, Chen TH. Transmission of Salmonella between swine farms by the housefly (Musca domestica). J Food Prot 2011, 74:1012-6. 10.4315/0362-028X.JFP-10-394, 21669083.
29. Umali DV, Lapuz RR, Suzuki T, Shirota K, Katoh H. Transmission and shedding patterns of Salmonella in naturally infected captive wild roof rats (Rattus rattus) from a Salmonella-contaminated layer farm. Avian Dis 2012, 56:288-94. 10.1637/9911-090411-Reg.1, 22856184.
30. Scholl D, Rogers S, Adhya S, Merril CR. Bacteriophage K1-5 encodes two different tail fiber proteins, allowing it to infect and replicate on both K1 and K5 strains of Escherichia coli. J Virol 2001, 75:2509-15. 10.1128/JVI.75.6.2509-2515.2001, 115872, 11222673.
31. Hatfull GF. Complete genome sequences of 138 mycobacteriophages. J Virol 2012, 86:2382-4. 10.1128/JVI.06870-11, 3302410, 22282335.
32. Shin H, Lee JH, Kim H, Choi Y, Heu S, Ryu S. Receptor diversity and host interaction of bacteriophages infecting Salmonella enterica serovar Typhimurium. PLoS One 2012, 7:e43392. 10.1371/journal.pone.0043392, 3424200, 22927964.
33. Ladero V, García P, Alonso JC, Suárez JE. Interaction of the Cro repressor with the lysis/lysogeny switch of the Lactobacillus casei temperate bacteriophage A2. J Gen Virol 2002, 83:2891-5.
34. Das M, Ganguly T, Chattoraj P, Chanda PK, Bandhu A, Lee CY, Sau S. Purification and characterization of repressor of temperate S. aureus phage phi11. J Biochem Mol Biol 2007, 40:740-8. 10.5483/BMBRep.2007.40.5.740, 17927908.
35. Kazaks A, Dislers A, Lipowsky G, Nikolajeva V, Tars K. Complete Genome Sequence of the Enterobacter cancerogenus Bacteriophage Enc34. J Virol 2012, 86:11403-4. 10.1128/JVI.01954-12, 3457185, 22997422.
36. 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. 10.1186/1743-422X-8-242, 3121705, 21595934.
37. Adriaenssens EM, Ackermann HW, Anany H, Blasdel B, Connerton IF, Goulding D, Griffiths MW, Hooton SP, Kutter EM, Kropinski AM, Lee JH, Maes M, Pickard D, Ryu S, Sepehrizadeh Z, Shahrbabak SS, Toribio AL, Lavigne R. A suggested new bacteriophage genus: " Viunalikevirus" Arch Virol 2012, 157:2035-2046. 10.1007/s00705-012-1360-5, 22707043.
38. Pickard D, Toribio AL, Petty NK, van Tonder A, Yu L, Goulding D, Barrell B, Rance R, Harris D, Wetter M, Wain J, Choudhary J, Thomson N, Dougan G. A conserved acetyl esterase domain targets diverse bacteriophages to the Vi capsular receptor of Salmonella enterica serovar Typhi. J Bacteriol 2010, 192:5746-54. 10.1128/JB.00659-10, 2953684, 20817773.
39. Park M, Lee JH, Shin H, Kim M, Choi J, Kang DH, Heu S, Ryu S. Characterization and comparative genomic analysis of a novel bacteriophage SFP10 simultaneously inhibiting both Salmonella and Escherichia coli O157:H7. Appl Environ Microbiol 2012, 78:58-69. 10.1128/AEM.06231-11, 3255626, 22020516.
40. Whichard JM, Weigt LA, Borris DJ, Li LL, Zhang Q, Kapur V, Pierson FW, Lingohr EJ, She YM, Kropinski AM, Sriranganathan N. Complete genomic sequence of bacteriophage Felix O1. Viruses 2010, 2:710-30. 10.3390/v2030710, 3185647, 21994654.
41. Lehman SM, Kropinski AM, Castle AJ, Svircev AM. Complete genome of the broad-host-range Erwinia amylovora phage phiEa21-4 and its relationship to Salmonella phage Felix O1. Appl Environ Microbiol 2009, 75:2139-47. 10.1128/AEM.02352-08, 2663227, 19181832.
42. Edgell DR, Gibb EA, Belfort M. Mobile DNA elements in T4 and related phages. Virol J 2010, 7:290. 10.1186/1743-422X-7-290, 2988022, 21029434.
43. De Lappe N, Doran G, O'Connor J, O'Hare C, Cormican M. Characterization of bacteriophages used in the Salmonella enterica serovar Enteritidis phage-typing scheme. J Med Microbiol 2009, 58:86-93. 10.1099/jmm.0.000034-0, 19074657.
44. Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM. Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res 1989, 17:4713-30. 10.1093/nar/17.12.4713, 318027, 2546125.
45. Thurber RV. Current insights into phage biodiversity and biogeography. Curr Opin Microbiol 2009, 12:582-7. 10.1016/j.mib.2009.08.008, 19811946.
46. Ceyssens PJ, Miroshnikov K, Mattheus W, Krylov V, Robben J, Noben JP, Vanderschraeghe S, Sykilinda N, Kropinski AM, Volckaert G, Mesyanzhinov V, Lavigne R. Comparative analysis of the widespread and conserved PB1-like viruses infecting Pseudomonas aeruginosa. Environ Microbiol 2009, 11:2874-83. 10.1111/j.1462-2920.2009.02030.x, 19678828.
47. Ceyssens PJ, Glonti T, Kropinski NM, Lavigne R, Chanishvili N, Kulakov L, Lashkhi N, Tediashvili M, Merabishvili M. Phenotypic and genotypic variations within a single bacteriophage species. Virol J 2011, 23:134.
48. The Mycobacterium database Phage Isolation Locations by GPS Coordinates http://phagesdb.org/GPSmap/, The Mycobacterium database.
49. The Mycobacterium database Details for Subcluster A2 Phages http://phagesdb.org/subclusters/A2/, The Mycobacterium database.
50. Casjens SR, Thuman-Commike PA. Evolution of mosaically related tailed bacteriophage genomes seen through the lens of phage P22 virion assembly. Virology 2011, 411:393-415. 10.1016/j.virol.2010.12.046, 21310457.
51. Mmolawa PT, Schmieger H, Heuzenroeder MW. Bacteriophage ST64B, a genetic mosaic of genes from diverse sources isolated from Salmonella enterica serovar Typhimurium DT 64. J Bacteriol 2003, 185:6481-5. 10.1128/JB.185.21.6481-6485.2003, 219385, 14563886.
52. Loś JM, Loś M, We{ogonek}grzyn G. Bacteriophages carrying shiga toxin genes: genomic variations, detection and potential treatment of pathogenic bacteria. Future Microbiol 2011, 6:909-24. 10.2217/fmb.11.70, 21861621.
53. Brüssow H, Canchaya C, Hardt WD. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 2004, 68:560-602. 10.1128/MMBR.68.3.560-602.2004, 515249, 15353570.
54. Stanley TL, Ellermeier CD, Slauch JM. Tissue-specific gene expression identifies a gene in the lysogenic phage Gifsy-1 that affects Salmonella enterica serovar Typhimurium survival in Peyer's patches. J Bacteriol 2000, 182:4406-13. 10.1128/JB.182.16.4406-4413.2000, 94610, 10913072.
55. Mirold S, Rabsch W, Tschäpe H, Hardt WD. Transfer of the Salmonella type III effector sopE between unrelated phage families. J Mol Biol 2001, 312:7-16. 10.1006/jmbi.2001.4950, 11545581.
56. Mirold S, Rabsch W, Rohde M, Stender S, Tschäpe H, Rüssmann H, Igwe E, Hardt WD. Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella Typhimurium strain. Proc Natl Acad Sci USA 1999, 96:9845-50. 10.1073/pnas.96.17.9845, 22298, 10449782.
57. Cardinale CJ, Washburn RS, Tadigotla VR, Brown LM, Gottesman ME, Nudler E. Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. Science 2008, 320:935-8. 10.1126/science.1152763, 18487194.
58. Kohn H, Widger W. The molecular basis for the mode of action of bicyclomycin. Curr Drug Targets Infect Disord 2005, 5:273-95. 10.2174/1568005054880136, 16181146.
59. Laskaris P, Sekine T, Wellington EM. Diversity analysis of Streptomycetes and associated phosphotranspherase genes in soil. PLoS One 2012, 7:e35756. 10.1371/journal.pone.0035756, 3335164, 22540003.
60. Chiang SK, Lou YC, Chen C. NMR solution structure of KP-TerB, a tellurite-resistance protein from Klebsiella pneumoniae. Protein Sci 2008, 17:785-9. 10.1110/ps.073389408, 2271173, 18305192.
61. Johnson TJ, Wannemeuhler YM, Scaccianoce JA, Johnson SJ, Nolan LK. Complete DNA sequence, comparative genomics, and prevalence of an IncHI2 plasmid occurring among extraintestinal pathogenic Escherichia coli isolates. Antimicrob Agents Chemother 2006, 50:3929-33. 10.1128/AAC.00569-06, 1635206, 16940062.
62. Hoiczyk E, Roggenkamp A, Reichenbecher M, Lupas A, Heesemann J. Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J 2000, 19:5989-99. 10.1093/emboj/19.22.5989, 305836, 11080146.
63. Molina-Quiroz RC, Muñoz-Villagrán CM, de la Torre E, Tantaleán JC, Vásquez CC, Pérez-Donoso JM. Enhancing the antibiotic antibacterial effect by sub lethal tellurite concentrations: tellurite and cefotaxime act synergistically in Escherichia coli. PLoS One 2012, 7:e35452. 10.1371/journal.pone.0035452, 3334966, 22536386.
64. Schicklmaier P, Schmieger H. Frequency of generalized transducing phages in natural isolates of the Salmonella Typhimurium complex. Appl Environ Microbiol 1995, 61:1637-40. 167422, 7747978.
65. Sternberg NL, Maurer R. Bacteriophage-mediated generalized transduction in Escherichia coli and Salmonella Typhimurium. Methods Enzymol 1991, 204:18-43.
66. Waddell TE, Franklin K, Mazzocco A, Kropinski AM, Johnson RP. Generalized transduction by lytic bacteriophages. Methods Mol Biol 2009, 501:293-303. 10.1007/978-1-60327-164-6_25, 19066829.
67. Miller ES, Kutter E, Mosig G, Arisaka F, Kunisawa T, Rüger W. Bacteriophage T4 genome. Microbiol Mol Biol Rev 2003, 67:86-156. 10.1128/MMBR.67.1.86-156.2003, 150520, 12626685.
68. Guttman BS, Kutter EM. Bacteriophage genetics, in modern microbial genetics 2002, New York, USA: Edited by U. N. Streips and R. E. Yasbin. John Wiley & Sons, Inc., 2.
69. Casjens SR, Molineux IJ. Short noncontractile tail machines: adsorption and DNA delivery by podoviruses. Adv Exp Med Biol 2012, 726:143-79. 10.1007/978-1-4614-0980-9_7, 22297513.
70. Davidson AR, Cardarelli L, Pell LG, Radford DR, Maxwell KL. Long noncontractile tail machines of bacteriophages. Adv Exp Med Biol 2012, 726:115-42. 10.1007/978-1-4614-0980-9_6, 22297512.
71. Welkos S, Schreiber M, Baer H. Identification of Salmonella with the O-1 bacteriophage. Appl Microbiol 1974, 28:618-22. 186784, 4609209.
72. Sambrook J, Russell DW. Molecular cloning 2001, New York: Cold Spring Harbor Laboratory Press, 3.
73. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008, 18:821-9. 10.1101/gr.074492.107, 2336801, 18349386.
74. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008, 9:75. 10.1186/1471-2164-9-75, 2265698, 18261238.
75. NCBI Prokaryotic Genomes Automatic Annotation Pipeline (PGAAP) http://www.ncbi.nlm.nih.gov/genomes/static/Pipeline.html.
76. Wiki food safety https://confluence.cornell.edu/display/FOODSAFETY/Cornell+Food+Safety+Laboratory+Microbial+Genome+Data.
77. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003, 13:2178-89. 10.1101/gr.1224503, 403725, 12952885.
78. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006, 23:254-67.
79. Krumsiek J, Arnold R, Rattei T. Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 2007, 23:1026-8. 10.1093/bioinformatics/btm039, 17309896.
80. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004, 14:1394-403. 10.1101/gr.2289704, 442156, 15231754.
81. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011, 27:1009-10. 10.1093/bioinformatics/btr039, 3065679, 21278367.
82. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinformatics 2009, 10:421. 10.1186/1471-2105-10-421, 2803857, 20003500.
83. Petty NK, Toribio AL, Goulding D, Foulds I, Thomson N, Dougan G, Salmond GP. A generalized transducing phage for the murine pathogen Citrobacter rodentium. Microbiol 2007, 153:2984-8.