The host-range, genomics and proteomics of Escherichia coli O157:H7 bacteriophage rV5

Virology Journal

Roger P Johnson⁴  Erika J Lingohr⁴  John Yates⁵  Amanda Mazzocco⁴  Rafiq Ahmed⁷  Hans-Wolfgang Ackermann⁶  Kristyn Franklin⁴  Juncai Meng¹  Tom Waddell²  Andrew M Kropinski³ 

[1] Merck Research Laboratories, 126E Lincoln Avenue, Rahway, NJ, 07065, USA;Abbott Point of Care, 185 Corkstown Road, Ottawa, ON, K2H 8V4, Canada;Department of Molecular and Cellular Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada;Public Health Agency of Canada, Laboratory for Foodborne Diseases, 110 Stone Road West, Guelph, ON N1G 3W4, Canada;The Scripps Research Institute, Department of Cell Biology, Proteomic Mass Spectrometry Laboratory, 10550 North Torrey Pines Road, La Jolla, CA, 92037, USA;Département de Microbiologie-infectiologie et immunologie, Faculté de médecine, Université Laval, Québec, QC, G1K 7P4, Canada;Enteric Diseases Program, National Microbiology Laboratory, Public Health Agency of Canada, 1015 Arlington Street, Winnipeg, MB, R3E 3R2, Canada

关键词: Tail spike;    Pyrosequencing;    Bioinformatics;    Proteomics;    Genomics;    Myoviridae;    Phage ecology;    Phage evolution;    E. coli O157:H7;   

Others  :  1151343
DOI  :  10.1186/1743-422X-10-76

 received in 2012-06-12, accepted in 2013-02-28,  发布年份 2013

【 摘 要 】

Background

Bacteriophages (phages) have been used extensively as analytical tools to type bacterial cultures and recently for control of zoonotic foodborne pathogens in foods and in animal reservoirs.

Methods

We examined the host range, morphology, genome and proteome of the lytic E. coli O157 phage rV5, derived from phage V5, which is a member of an Escherichia coli O157:H7 phage typing set.

Results

Phage rV5 is a member of the Myoviridae family possessing an icosahedral head of 91 nm between opposite apices. The extended tail measures 121 x 17 nm and has a sheath of 44 x 20 nm and a 7 nm-wide core in the contracted state. It possesses a 137,947 bp genome (43.6 mol%GC) which encodes 233 ORFs and six tRNAs. Until recently this virus appeared to be phylogenetically isolated with almost 70% of its gene products ORFans. rV5 is closely related to coliphages Delta and vB-EcoM-FY3, and more distantly related to Salmonella phages PVP-SE1 and SSE-121, Cronobacter sakazakii phage vB_CsaM_GAP31, and coliphages phAPEC8 and phi92. A complete shotgun proteomic analysis was carried out on rV5, extending what had been gleaned from the genomic analyses. Host range studies revealed that rV5 is active against several other E. coli.

【 授权许可】

   
2013 Kropinski et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Bolton DJ: Verocytotoxigenic (Shiga toxin-producing) Escherichia coli: virulence factors and pathogenicity in the farm to fork paradigm. Foodborne Pathog Dis 2011, 8:357-365.
• [2]Karmali MA: Host and pathogen determinants of verocytotoxin-producing Escherichia coli-associated hemolytic uremic syndrome. Kidney Int Suppl 2009, 112:S4-S7.
• [3]Stanford K, McAllister TA, Niu YD, Stephens TP, Mazzocco A, Waddell TE, Johnson RP: Oral delivery systems for encapsulated bacteriophages targeted at Escherichia coli O157:H7 in feedlot cattle. J Food Prot 2010, 73:1304-1312.
• [4]Niu YD, Stanford K, Kropinski AM, Ackermann HW, Johnson RP, She YM, Ahmed R, Villegas A, McAllister TA: Genomic, proteomic and physiological characterization of a T5-like bacteriophage for control of Shiga toxin-producing Escherichia coli O157:H7. PLoS One 2012, 7:e34585.
• [5]Kutter EM, Skutt-Kakaria K, Blasdel B, el-Shibiny A, Castano A, Bryan D, Kropinski AM, Villegas A, Ackermann HW, Toribio AL, Pickard D, Anany H, Callaway T, Brabban AD: Characterization of a ViI-like phage specific to Escherichia coli O157:H7. Virol J 2011, 8:430. BioMed Central Full Text
• [6]Ahmed R, Bopp C, Borczyk A, Kasatiya S: Phage-typing scheme for Escherichia coli O157:H7. J Infect Dis 1987, 155:806-809.
• [7]Viazis S, Akhtar M, Feirtag J, Brabban AD, Diez-Gonzalez F: Isolation and characterization of lytic bacteriophages against enterohaemorrhagic Escherichia coli. J Appl Microbiol 2011, 110:1323-1331.
• [8]Ronner AB, Cliver DO: Isolation and characterization of a coliphage specific form Escherichia coli O157:H7. J Food Prot 1990, 53:944-947.
• [9]Liao WC, Ng WV, Lin IH, Syu WJ, Liu TT, Chang CH: T4-Like genome organization of the Escherichia coli O157:H7 lytic phage AR1. J Virol 2011, 85:6567-6578.
• [10]López-Cuevas O, Castro-Del CN, Léon-Felix J, González-Robles A, Chaidez C: Characterization of bacteriophages with a lytic effect on various Salmonella serotypes and Escherichia coli O157:H7. Can J Microbiol 2011, 57:1042-1051.
• [11]Dini C, De Urraza PJ: Isolation and selection of coliphages as potential biocontrol agents of enterohemorrhagic and Shiga toxin-producing E. coli (EHEC and STEC) in cattle. J Appl Microbiol 2010, 109:873-887.
• [12]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.
• [13]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.
• [14]Kannan P, Yong HY, Reiman L, Cleaver C, Patel P, Bhagwat AA: Bacteriophage-based rapid and sensitive detection of Escherichia coli O157:H7 isolates from ground beef. Foodborne Pathog Dis 2010, 7:1551-1558.
• [15]McAllister TA, Stanford K, Bach SJ: Monitoring and migration of E. coli O157:H7 in commercial dairies. Advances in Dairy Technology 2005, 17:227-246.
• [16]O’Flynn G, Ross RP, Fitzgerald GF, Coffey A: Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl Environ Microbiol 2004, 70:3417-3424.
• [17]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.
• [18]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.
• [19]Goodridge L, Chen J, Griffiths M: Development and characterization of a fluoresecent-bacteriophage assay for detection of Escherichia coli O157:H7. Appl Environ Microbiol 1999, 65:1397-1404.
• [20]Perry LL, SanMiguel P, Minocha U, Terekhov AI, Shroyer ML, Farris LA, Bright N, Reuhs BL, Applegate BM: Sequence analysis of Escherichia coli O157:H7 bacteriophage ϕV10 and identification of a phage-encoded immunity protein that modifies the O157 antigen. FEMS Microbiol Lett 2009, 292:182-186.
• [21]Hendrix RW, Casjens SR: Myoviridae, Siphoviridae, Podoviridae. In Virus Taxonomy. VIIIth Report of the International Committee on Taxonomy of Viruses. Edited by Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA. New York: Elsevier Academic Press; 2005:43-47.
• [22]Morita M, Tanji Y, Mizoguchi K, Akitsu T, Kijima N, Unno H: Characterization of a virulent bacteriophage specific for Escherichia coli O157:H7 and analysis of its cellular receptor and two tail fiber genes. FEMS Microbiol Lett 2002, 211:77-83.
• [23]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 enterica and Escherichia coli O157:H7. Appl Environ Microbiol 2012, 78:58-69.
• [24]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.
• [25]Tanji Y, Shimada T, Yoichi M, Miyanaga K, Hori K, Unno H: Towards a rational control of Escherichia coli O157:H7 by a phage cocktail. Appl Microbiol Biotechnol 2004, 64:270-274.
• [26]Kropinski AM, Lingohr EJ, Moyles DM, Ojha S, Mazzocco A, She YM, Bach SJ, Rozema EA, Stanford K, McAllister TA, Johnson RP: Endemic bacteriophages: a cautionary tale for evaluation of bacteriophage therapy and other interventions for infection control in animals. J Virol 2012, 9:207. BioMed Central Full Text
• [27]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. BioMed Central Full Text
• [28]Lavigne R, Darius P, Summer EJ, Seto D, Mahadevan P, Nilsson AS, Ackermann H-W, Kropinski AM: Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol 2009, 9:224. BioMed Central Full Text
• [29]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.
• [30]Kropinski AM, Lingohr EJ, Moyles DM, Chibeu A, Mazzocco A, Franklin K, Villegas A, Ahmed R, She YM, Johnson RP: Escherichia coli O157:H7 typing phage V7 is a T4-like virus. J Virol 2012, 86:10246-12.
• [31]Kropinski AM, Kovalyova IV, Billington SJ, Butts BD, Patrick AN, Guichard JA, Hutson SM, Sydlaske AD, Day KR, Falk DR, McConnell MR: The genome of ε15, a serotype-converting, Group E1 Salmonella enterica-specific bacteriophage. Virology 2007, 369:234-244.
• [32]Waddell TE, Mazzocco A, Pacan J, Johnson R, Ahmed R, Poppe C, Khakhria C: Use of bacteriophages to control Escherichia coli O157 infections in cattle. United States Patent No 2002, 6:485,902.
• [33]Waddell T, Mazzocco A, Johnson R, Pacan J, Campbell S, Perets A, MacKinnon J, Holtslander B, Poppe C, Gyles C: Control of Escherichia coli O157:H7 infection of calves by bacteriophages. 1st edition. Kyoto, Japan: Fourth International International Symposium and Workshop on Shiga toxin (verocytotoxin)-producing Escherichia coli (VTEC 2000); 2000:1-2.
• [34]Ochman H, Selander RK: Standard reference strains of Escherichia coli from natural populations. J Bacteriol 1984, 157:690-693.
• [35]Lior H: Classification of Escherichia coli. In Escherichia coli in Domestic Animals and Humans. Edited by Gyles CL. Wallingford, UK: CAB International; 1994:31-72.
• [36]Kropinski AM: Sequence of the genome of the temperate, serotype-converting, Pseudomonas aeruginosa bacteriophage D3. J Bacteriol 2000, 182:6066-6074.
• [37]Lowe TM, Eddy SR: tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25:955-964.
• [38]Laslett D, Canback B: ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 2004, 32:11-16.
• [39]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: creation of a new phage genus. J Virol 2011, 85:11265-11273.
• [40]Sonnhammer ELL, von Heijne G, Krogh A: A hidden Markov model for predicting transmembrane helices in protein sequences. In Proceedings of the Sixth International Conference on Intelligent Systems for Molecular Biology. Edited by Glasgow J, Littlejohn T, Major F, Lathrop R, Sankoff D, Sensen C. Menlo Park, CA: AAAI Press; 1998:175-182.
• [41]Kall L, Krogh A, Sonnhammer EL: A combined transmembrane topology and signal peptide prediction method. J Mol Biol 2004, 338:1027-1036.
• [42]Miller EC, Kutter E, Mosig G, Arisaka F, Kunisawa T, Rüger W: Bacteriophage T4 genome. Microbiol Mol Biol Rev 2003, 67:86-156.
• [43]Bailey TL, Elkan C: The value of prior knowledge in discovering motifs with MEME. ISMB 1995, 3:21-29.
• [44]Kassavetis GA, Butler ET, Roulland D, Chamberlin MJ: Bacteriophage SP6-specific RNA polymerase. II. Mapping of SP6 DNA and selective in vitro transcription. J Biol Chem 1982, 257:5779-5788.
• [45]Geiduschek EP, Kassavetis GA: Transcription of the T4 late genes. Virol J 2010, 7:288. BioMed Central Full Text
• [46]Lundin D, Torrents E, Poole AM, Sjoberg BM: RNRdb, a curated database of the universal enzyme family ribonucleotide reductase, reveals a high level of misannotation in sequences deposited to Genbank. BMC Genomics 2009, 10:589. BioMed Central Full Text
• [47]Kropinski AM, Lingohr EJ, Ackermann HW: The genome sequence of enterobacterial phage 7–11, which possesses an unusually elongated head. Arch Virol 2011, 156:149-151.
• [48]Morello E, Saussereau E, Maura D, Huerre M, Touqui L, Debarbieux L: Pulmonary bacteriophage therapy on Pseudomonas aeruginosa cystic fibrosis strains: first steps towards treatment and prevention. PLoS One 2011, 6:e16963.
• [49]Shin H, Lee JH, Kim Y, Ryu S: Complete genome sequence of Cronobacter sakazakii bacteriophage CR3. J Virol 2012, 86:6367-6368.
• [50]Grigoriev A: Analyzing genomes with cumulative skew diagrams. Nucleic Acids Res 1998, 26:2286-2290.
• [51]Lobry JR, Lobry C: Evolution of DNA base composition under no-strand-bias conditions when the substitution rates are not constant. Mol Biol Evol 1999, 16:719-723.
• [52]Lobry JR: Genomic landscapes. Microbiology Today 1999, 26:164-165.
• [53]Grigoriev A: Strand-specific compositional asymmetries in double-stranded DNA viruses. Virus Res 1999, 60:1-19.
• [54]Hildebrand A, Remmert M, Biegert A, Soding J: Fast and accurate automatic structure prediction with HHpred. Proteins 2009, 77(Suppl 9):128-132.
• [55]Kostyuchenko VA, Leiman PG, Chipman PR, Kanamaru S, van Raaij MJ, Arisaka F, Mesyanzhinov VV, Rossmann MG: Three-dimensional structure of bacteriophage T4 baseplate. Nat Struct Biol 2003, 10:688-693.
• [56]Pearson WR, Wood T, Zhang Z, Miller W: Comparison of DNA sequences with protein sequences. Genomics 1997, 46:24-36.
• [57]Lupas A: Predicting coiled-coil regions in proteins. Curr Opin Struct Biol 1997, 7:388-393.
• [58]Lupas A, Van DM, Stock J: Predicting coiled coils from protein sequences. Science 1991, 252:1162-1164.
• [59]Schwarzer D, Buettner FF, Browning C, Nazarov S, Rabsch W, Bethe A, Oberbeck A, Bowman VD, Stummeyer K, Muhlenhoff M, Leiman PG, Gerardy-Schahn R: A multivalent adsorption apparatus explains the broad host range of phage phi92: a comprehensive genomic and structural analysis. J Virol 2012, 86:10384-10398.
• [60]Mikkonen M, Alatossava T: A group I intron in the terminase gene of Lactobacillus delbrueckii subsp. lactis phage LL-H. Microbiology 1995, 141:2183-2190.
• [61]Young R: Bacteriophage lysis: mechanism and regulation. Microbiol Rev 1992, 56:430-481.
• [62]Grundling A, Bläsi U, Young R: Biochemical and genetic evidence for three transmembrane domains in the class I holin, lambda S. J Biol Chem 2000, 275:769-776.
• [63]Young R, Bläsi U: Holins: form and function in bacteriophage lysis. FEMS Microbiol Rev 1995, 17:191-205.
• [64]Pickard D, Thomson NR, Baker S, Wain J, Pardo M, Goulding D, Hamlin N, Choudhary J, Threfall J, Dougan G: Molecular characterization of the Salmonella enterica serovar Typhi Vi-typing bacteriophage E1. J Bacteriol 2008, 190:2580-2587.
• [65]The National Microbiology Laboratory (NML) andCentre for Food-borne Environmental and Zoonotic Infectious Diseases (CFEZID) PHAoC, Provincial Public Health Microbiology Laboratories: 2009 Annual Summary of Laboratory Surveillance Data, Including Serotype and Phage Types Tables for 2007–2009, NESP and NML. : ; 2009. http://www.nml-lnm.gc.ca/NESP-PNSME/surveillance-2009-eng.html webcite
• [66]Viscardi M, Perugini AG, Auriemma C, Capuano F, Morabito S, Kim KP, Loessner MJ, Iovane G: Isolation and characterisation of two novel coliphages with high potential to control antibiotic-resistant pathogenic Escherichia coli (EHEC and EPEC). Int J Antimicrob Agents 2008, 31:152-157.
• [67]Fischer D, Eisenberg D: Finding families for genomic ORFans. Bioinformatics 1999, 15:759-762.
• [68]Yin Y, Fischer D: Identification and investigation of ORFans in the viral world. BMC Genomics 2008, 9:24. BioMed Central Full Text
• [69]Truncaite L, Simoliunas E, Zajanckauskaite A, Kaliniene L, Mankeviciute R, Staniulis J, Klausa V, Meskys R: Bacteriophage vB_EcoM_FV3: a new member of “rV5-like viruses”. Arch Virol 2012, 157:2431-2435.
• [70]Tsonos J, Adriaenssens EM, Klumpp J, Hernalsteens JP, Lavigne R, De GH: Complete genome sequence of the novel Escherichia coli phage phAPEC8. J Virol 2012, 86:13117-13118.
• [71]Abbasifar R, Kropinski AM, Sabour PM, Ackermann HW, Alanis VA, Abbasifar A, Griffiths MW: Genome sequence of Cronobacter sakazakii myovirus vB_CsaM_GAP31. J Virol 2012, 86:13830-13831.
• [72]Ceyssens PJ, Brabban A, Rogge L, Lewis MS, Pickard D, Goulding D, Dougan G, Noben JP, Kropinski A, Kutter E, Lavigne R: Molecular and physiological analysis of three Pseudomonas aeruginosa phages belonging to the “N4-like viruses”. Virology 2010, 405:26-30.
• [73]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, 11:2874-2883.
• [74]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, 8:134. BioMed Central Full Text
• [75]Lavigne R, Seto D, Mahadevan P, Ackermann H-W, Kropinski AM: Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Res Microbiol 2008, 159:406-414.
• [76]Pedulla ML, Ford ME, Houtz JM, Karthikeyan T, Wadsworth C, Lewis JA, Jacobs-Sera D, Falbo J, Gross J, Pannunzio NR, Brucker W, Kumar V, Kandasamy J, Keenan L, Bardarov S, Kriakov J, Lawrence JG, Jacobs WR Jr, Hendrix RW, Hatfull GF: Origins of highly mosaic mycobacteriophage genomes. Cell 2003, 113:171-182.
• [77]Darling AE, Mau B, Perna NT: progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010, 5:e11147.
• [78]Voelker R, Sulakvelidze A, Ackermann HW: Spontaneous tail length variation in a Salmonella myovirus. Virus Res 2005, 114:164-166.
• [79]Yamamoto KR, Alberts BM, Benzinger R, Lawhorne L, Treiber G: Rapid bacteriophage sedimentation in the presence of polyethylene glycol and its application to large-scale virus purification. Virology 1970, 40:734-744.
• [80]Sambrook J, Russell DW: Molecular Cloning: A Laboratory Manual. 3rd edition. Cold Spring Harbor, New York: Cold Spring Harbor Press; 2001.
• [81]Lingohr E, Frost S, Johnson RP: Determination of bacteriophage genome size by pulsed-field gel electrophoresis. Methods Mol Biol 2009, 502:19-25.
• [82]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
• [83]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, 25:3389-4022.
• [84]Soding J, Biegert A, Lupas AN: The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 2005, 33:W244-W248.
• [85]Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH: CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 2011, 39:D225-D229.
• [86]Derbyshire MK, Lanczycki CJ, Bryant SH, Marchler-Bauer A: Annotation of functional sites with the Conserved Domain Database. Database 2012. 2012:bar058
• [87]Macke TJ, Ecker DJ, Gutell RR, Gautheret D, Case DA, Sampath R: RNAMotif, an RNA secondary structure definition and search algorithm. Nucleic Acids Res 2001, 29:4724-4735.
• [88]Zuker M, Zuker M: Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003, 31:3406-3415.
• [89]Bailey TL, Elkan C: Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Menlo Park, CA USA: AAAI Press; 1994:28-36.
• [90]Zafar N, Mazumder R, Seto D: CoreGenes: a computational tool for identifying and cataloging “core” genes in a set of small genomes. BMC Bioinforma 2002, 3:12. BioMed Central Full Text
• [91]Kropinski AM, Borodovsky M, Carver TJ, Cerdeno-Tarraga AM, Darling A, Lomsadze A, Mahadevan P, Stothard P, Seto D, Van DG, Wishart DS: In silico identification of genes in bacteriophage DNA. Methods Mol Biol 2009, 502:57-89.
• [92]Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O: Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008, 36:W465-W469.
• [93]Washburn MP, Wolters D, Yates JR III, Washburn MP, Wolters D, Yates JR: Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 2001, 19:242-247.
• [94]Tabb DL, McDonald WH, Yates JR III, Tabb DL, McDonald WH, Yates JR: DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J Proteome Res 2002, 1:21-26.