Academia.eduAcademia.edu

Outline

Bacterial Virus Ontology; Coordinating across Databases

Viruses

https://doi.org/10.3390/V9060126

Abstract

Bacterial viruses, also called bacteriophages, display a great genetic diversity and utilize unique processes for infecting and reproducing within a host cell. All these processes were investigated and indexed in the ViralZone knowledge base. To facilitate standardizing data, a simple ontology of viral life-cycle terms was developed to provide a common vocabulary for annotating data sets. New terminology was developed to address unique viral replication cycle processes, and existing terminology was modified and adapted. Classically, the viral life-cycle is described by schematic pictures. Using this ontology, it can be represented by a combination of successive events: entry, latency, transcription/replication, host-virus interactions and virus release. Each of these parts is broken down into discrete steps. For example enterobacteria phage lambda entry is broken down in: viral attachment to host adhesion receptor, viral attachment to host entry receptor, viral genome ejection and viral genome circularization. To demonstrate the utility of a standard ontology for virus biology, this work was completed by annotating virus data in the ViralZone, UniProtKB and Gene Ontology databases.

References (76)

  1. Hershey, A.D.; Chase, M. Independent functions of viral protein and nucleic acid in growth of bacteriophage. J. Gen. Physiol. 1952, 36, 39-56. [CrossRef] [PubMed]
  2. Haq, I.U.; Chaudhry, W.N.; Akhtar, M.N.; Andleeb, S.; Qadri, I. Bacteriophages and their implications on future biotechnology: A review. Virol. J. 2012, 9, 9. [CrossRef] [PubMed]
  3. Henry, M.; Debarbieux, L. Tools from viruses: Bacteriophage successes and beyond. Virology 2012, 434, 151-161. [CrossRef] [PubMed]
  4. Sharan, S.K.; Thomason, L.C.; Kuznetsov, S.G.; Court, D.L. Recombineering: A homologous recombination- based method of genetic engineering. Nat. Protoc. 2009, 4, 206-223. [CrossRef] [PubMed]
  5. Cisek, A.A.; D ąbrowska, I.; Gregorczyk, K.P.; Wy żewski, Z. Phage Therapy in Bacterial Infections Treatment: One Hundred Years after the Discovery of Bacteriophages. Curr. Microbiol. 2017, 74, 277-283. [CrossRef] [PubMed] Viruses 2017, 9, 126 15 of 17
  6. Drulis-Kawa, Z.; Majkowska-Skrobek, G.; Maciejewska, B.; Delattre, A.-S.; Lavigne, R. Learning from bacteriophages-advantages and limitations of phage and phage-encoded protein applications. Curr. Protein Pept. Sci. 2012, 13, 699-722. [CrossRef] [PubMed]
  7. Snyder, J.C.; Bolduc, B.; Young, M.J. 40 Years of archaeal virology: Expanding viral diversity. Virology 2015, 479-480, 369-378. [CrossRef] [PubMed]
  8. Mann, N.H. The third age of phage. PLoS Biol. 2005, 3, e182. [CrossRef] [PubMed]
  9. Wagner, P.L.; Waldor, M.K. Bacteriophage control of bacterial virulence. Infect. Immun. 2002, 70, 3985-3993. [CrossRef] [PubMed]
  10. Jover, L.F.; Effler, T.C.; Buchan, A.; Wilhelm, S.W.; Weitz, J.S. The elemental composition of virus particles: Implications for marine biogeochemical cycles. Nat. Rev. Microbiol. 2014, 12, 519-528. [CrossRef] [PubMed]
  11. Rodriguez-Valera, F.; Martin-Cuadrado, A.-B.; Rodriguez-Brito, B.; Pasić, L.; Thingstad, T.F.; Rohwer, F.; Mira, A. Explaining microbial population genomics through phage predation. Nat. Rev. Microbiol. 2009, 7, 828-836. [CrossRef] [PubMed]
  12. Nelson, D. Phage taxonomy: We agree to disagree. J. Bacteriol. 2004, 186, 7029-7031. [CrossRef] [PubMed]
  13. Hulo, C.; de Castro, E.; Masson, P.; Bougueleret, L.; Bairoch, A.; Xenarios, I.; Le Mercier, P. ViralZone: A knowledge resource to understand virus diversity. Nucleic Acids Res. 2011, 39, 576-582. [CrossRef] [PubMed]
  14. UniProt Consortium. UniProt: A hub for protein information. Nucleic Acids Res. 2015, 43, 204-212.
  15. Ashburner, M.; Ball, C.A.; Blake, J.A.; Botstein, D.; Butler, H.; Cherry, J.M.; Davis, A.P.; Dolinski, K.; Dwight, S.S.; Eppig, J.T.; et al. Gene ontology: Tool for the unification of biology. Nat. Genet. 2000, 25, 25-29. [CrossRef] [PubMed]
  16. Gene Ontology Consortium. The Gene Ontology in 2010: Extensions and refinements. Nucleic Acids Res. 2010, 38, D331-D335.
  17. Masson, P.; Hulo, C.; de Castro, E.; Foulger, R.; Poux, S.; Bridge, A.; Lomax, J.; Bougueleret, L.; Xenarios, I.; Le Mercier, P. An integrated ontology resource to explore and study host-virus relationships. PLoS ONE 2014, 9, e108075. [CrossRef] [PubMed]
  18. Calendar, R. The Bacteriophages, 2th ed.; Oxford University Press: Oxford, UK, 2006.
  19. Toussaint, A.; Lima-Mendez, G.; Leplae, R. PhiGO, a phage ontology associated with the ACLAME database. Res. Microbiol. 2007, 158, 567-571. [CrossRef] [PubMed]
  20. Leiman, P.G.; Shneider, M.M. Contractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 2012, 726, 93-114. [PubMed]
  21. Casjens, S.R.; Molineux, I.J. Short noncontractile tail machines: Adsorption and DNA delivery by podoviruses. Adv. Exp. Med. Biol. 2012, 726, 143-179. [PubMed]
  22. Davidson, A.R.; Cardarelli, L.; Pell, L.G.; Radford, D.R.; Maxwell, K.L. Long noncontractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 2012, 726, 115-142. [PubMed]
  23. Büttner, C.R.; Wu, Y.; Maxwell, K.L.; Davidson, A.R. Baseplate assembly of phage Mu: Defining the conserved core components of contractile-tailed phages and related bacterial systems. Proc. Natl. Acad. Sci. USA 2016, 113, 10174-10179. [CrossRef] [PubMed]
  24. Taylor, N.M.I.; Prokhorov, N.S.; Guerrero-Ferreira, R.C.; Shneider, M.M.; Browning, C.; Goldie, K.N.; Stahlberg, H.; Leiman, P.G. Structure of the T4 baseplate and its function in triggering sheath contraction. Nature 2016, 533, 346-352. [CrossRef] [PubMed]
  25. Holland, S.J.; Sanz, C.; Perham, R.N. Identification and specificity of pilus adsorption proteins of filamentous bacteriophages infecting Pseudomonas aeruginosa. Virology 2006, 345, 540-548. [CrossRef] [PubMed]
  26. Choi, Y.; Shin, H.; Lee, J.-H.; Ryu, S. Identification and characterization of a novel flagellum-dependent Salmonella-infecting bacteriophage, iEPS5. Appl. Environ. Microbiol. 2013, 79, 4829-4837. [CrossRef] [PubMed]
  27. Grahn, A.M.; Daugelavicius, R.; Bamford, D.H. Sequential model of phage PRD1 DNA delivery: Active involvement of the viral membrane. Mol. Microbiol. 2002, 46, 1199-1209. [CrossRef] [PubMed]
  28. Rakonjac, J.; Bennett, N.J.; Spagnuolo, J.; Gagic, D.; Russel, M. Filamentous bacteriophage: Biology, phage display and nanotechnology applications. Curr. Issues Mol. Biol. 2011, 13, 51-76. [PubMed]
  29. Puspurs, A.H.; Trun, N.J.; Reeve, J.N. Bacteriophage Mu DNA circularizes following infection of Escherichia coli. EMBO J. 1983, 2, 345-352. [PubMed]
  30. Mardanov, A.V.; Ravin, N.V. Conversion of linear DNA with hairpin telomeres into a circular molecule in the course of phage N15 lytic replication. J. Mol. Biol. 2009, 391, 261-268. [CrossRef] [PubMed]
  31. Roldan, L.A.; Baker, T.A. Differential role of the Mu B protein in phage Mu integration vs. replication: Mechanistic insights into two transposition pathways. Mol. Microbiol. 2001, 40, 141-155. [CrossRef] [PubMed]
  32. Farruggio, A.P.; Chavez, C.L.; Mikell, C.L.; Calos, M.P. Efficient reversal of phiC31 integrase recombination in mammalian cells. Biotechnol. J. 2012, 7, 1332-1336. [CrossRef] [PubMed]
  33. Pope, W.H.; Bowman, C.A.; Russell, D.A.; Jacobs-Sera, D.; Asai, D.J.; Cresawn, S.G.; Jacobs, W.R.; Hendrix, R.W.; Lawrence, J.G.; Hatfull, G.F. Whole genome comparison of a large collection of mycobacteriophages reveals a continuum of phage genetic diversity. eLife 2015, 4, e06416. [CrossRef] [PubMed]
  34. Labrie, S.J.; Samson, J.E.; Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 2010, 8, 317-327. [CrossRef] [PubMed]
  35. Samson, J.E.; Magadán, A.H.; Sabri, M.; Moineau, S. Revenge of the phages: Defeating bacterial defences. Nat. Rev. Microbiol. 2013, 11, 675-687. [CrossRef] [PubMed]
  36. Roberts, R.J. Restriction and modification enzymes and their recognition sequences. Nucleic Acids Res. 1981, 9, 167-204. [CrossRef]
  37. Studier, F.W. Gene 0.3 of bacteriophage T7 acts to overcome the DNA restriction system of the host. J. Mol. Biol. 1975, 94, 283-295. [CrossRef]
  38. Berkner, K.L.; Folk, W.R. The effects of substituted pyrimidines in DNAs on cleavage by sequence-specific endonucleases. J. Biol. Chem. 1979, 254, 2551-2560. [PubMed]
  39. Dillingham, M.S.; Kowalczykowski, S.C. RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol. Mol. Biol. Rev. 2008, 72, 642-671. [CrossRef] [PubMed]
  40. Lipinska, B.; Rao, A.S.; Bolten, B.M.; Balakrishnan, R.; Goldberg, E.B. Cloning and identification of bacteriophage T4 gene 2 product Gp2 and action of Gp2 on infecting DNA in vivo. J. Bacteriol. 1989, 171, 488-497. [CrossRef] [PubMed]
  41. Murphy, K.C. The lambda Gam protein inhibits RecBCD binding to dsDNA ends. J. Mol. Biol. 2007, 371, 19-24. [CrossRef] [PubMed]
  42. Chopin, M.-C.; Chopin, A.; Bidnenko, E. Phage abortive infection in lactococci: Variations on a theme. Curr. Opin. Microbiol. 2005, 8, 473-479. [CrossRef] [PubMed]
  43. Otsuka, Y.; Yonesaki, T. Dmd of bacteriophage T4 functions as an antitoxin against Escherichia coli LsoA and RnlA toxins. Mol. Microbiol. 2012, 83, 669-681. [CrossRef] [PubMed]
  44. Barrangou, R.; Marraffini, L.A. CRISPR-Cas systems: Prokaryotes upgrade to adaptive immunity. Mol. Cell 2014, 54, 234-244. [CrossRef] [PubMed]
  45. Bondy-Denomy, J.; Pawluk, A.; Maxwell, K.L.; Davidson, A.R. Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 2013, 493, 429-432. [CrossRef] [PubMed]
  46. Seed, K.D.; Lazinski, D.W.; Calderwood, S.B.; Camilli, A. A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 2013, 494, 489-491. [CrossRef] [PubMed]
  47. Bae, B.; Davis, E.; Brown, D.; Campbell, E.A.; Wigneshweraraj, S.; Darst, S.A. Phage T7 Gp2 inhibition of Escherichia coli RNA polymerase involves misappropriation of σ70 domain 1.1. Proc. Natl. Acad. Sci. USA 2013, 110, 19772-19777. [CrossRef] [PubMed]
  48. Souther, A.; Bruner, R.; Elliott, J. Degradation of Escherichia coli chromosome after infection by bacteriophage T4: Role of bacteriophage gene D2a. J. Virol. 1972, 10, 979-984. [PubMed]
  49. Powell, I.B.; Tulloch, D.L.; Hillier, A.J.; Davidson, B.E. Phage DNA synthesis and host DNA degradation in the life cycle of Lactococcus lactis bacteriophage c6A. J. Gen. Microbiol. 1992, 138, 945-950. [CrossRef] [PubMed]
  50. Yano, S.T.; Rothman-Denes, L.B. A phage-encoded inhibitor of Escherichia coli DNA replication targets the DNA polymerase clamp loader. Mol. Microbiol. 2011, 79, 1325-1338. [CrossRef] [PubMed]
  51. Belley, A.; Callejo, M.; Arhin, F.; Dehbi, M.; Fadhil, I.; Liu, J.; McKay, G.; Srikumar, R.; Bauda, P.; Bergeron, D.; et al. Competition of bacteriophage polypeptides with native replicase proteins for binding to the DNA sliding clamp reveals a novel mechanism for DNA replication arrest in Staphylococcus aureus. Mol. Microbiol. 2006, 62, 1132-1143. [CrossRef] [PubMed]
  52. Bondy-Denomy, J.; Qian, J.; Westra, E.R.; Buckling, A.; Guttman, D.S.; Davidson, A.R.; Maxwell, K.L. Prophages mediate defense against phage infection through diverse mechanisms. ISME J. 2016, 10, 2854-2866. [CrossRef] [PubMed]
  53. Berngruber, T.W.; Weissing, F.J.; Gandon, S. Inhibition of superinfection and the evolution of viral latency. J. Virol. 2010, 84, 10200-10208. [CrossRef] [PubMed] Viruses 2017, 9, 126
  54. Braun, V.; Killmann, H.; Herrmann, C. Inactivation of FhuA at the cell surface of Escherichia coli K-12 by a phage T5 lipoprotein at the periplasmic face of the outer membrane. J. Bacteriol. 1994, 176, 4710-4717. [CrossRef] [PubMed]
  55. Lu, M.J.; Henning, U. Superinfection exclusion by T-even-type coliphages. Trends Microbiol. 1994, 2, 137-139.
  56. Abedon, S.T.; Lejeune, J.T. Why bacteriophage encode exotoxins and other virulence factors. Evol. Bioinform. Online 2007, 1, 97-110. [PubMed]
  57. Boyd, E.F.; Brüssow, H. Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol. 2002, 10, 521-529. [CrossRef]
  58. Mann, N.H.; Clokie, M.R.J.; Millard, A.; Cook, A.; Wilson, W.H.; Wheatley, P.J.; Letarov, A.; Krisch, H.M. The genome of S-PM2, a "photosynthetic" T4-type bacteriophage that infects marine Synechococcus strains. J. Bacteriol. 2005, 187, 3188-3200. [CrossRef] [PubMed]
  59. Maluf, N.K.; Gaussier, H.; Bogner, E.; Feiss, M.; Catalano, C.E. Assembly of bacteriophage lambda terminase into a viral DNA maturation and packaging machine. Biochemistry 2006, 45, 15259-15268. [CrossRef] [PubMed]
  60. Zhang, Z.; Kottadiel, V.I.; Vafabakhsh, R.; Dai, L.; Chemla, Y.R.; Ha, T.; Rao, V.B. A promiscuous DNA packaging machine from bacteriophage T4. PLoS Biol. 2011, 9, e1000592. [CrossRef] [PubMed]
  61. Narajczyk, M.; Bara ńska, S.; Wegrzyn, A.; Wegrzyn, G. Switch from theta to sigma replication of bacteriophage lambda DNA: Factors involved in the process and a model for its regulation. Mol. Genet. Genom. 2007, 278, 65-74. [CrossRef] [PubMed]
  62. Salas, M.; Holguera, I.; Redrejo-Rodríguez, M.; de Vega, M. DNA-binding proteins essential for protein-primed bacteriophage Φ29 DNA replication. Front. Mol. Biosci. 2016, 3, 37. [CrossRef] [PubMed]
  63. Hulo, C.; Masson, P.; Le Mercier, P.; Toussaint, A. A structured annotation frame for the transposable phages: A new proposed family "Saltoviridae" within the Caudovirales. Virology 2015, 477, 155-163. [CrossRef] [PubMed]
  64. Shapiro, J.A. Molecular model for the transposition and replication of bacteriophage Mu and other transposable elements. Proc. Natl. Acad. Sci. USA 1979, 76, 1933-1937. [CrossRef] [PubMed]
  65. Lundström, K.H.; Bamford, D.H.; Palva, E.T.; Lounatmaa, K. Lipid-containing bacteriophage PR4: Structure and life cycle. J. Gen. Virol. 1979, 43, 583-592. [CrossRef] [PubMed]
  66. Johnson, M.D.; Mindich, L. Plasmid-directed assembly of the lipid-containing membrane of bacteriophage phi 6. J. Bacteriol. 1994, 176, 4124-4132. [CrossRef] [PubMed]
  67. Young, R. Phage lysis: Three steps, three choices, one outcome. J. Microbiol. Seoul Korea 2014, 52, 243-258. [CrossRef] [PubMed]
  68. Young, R. Phage lysis: Do we have the hole story yet? Curr. Opin. Microbiol. 2013, 16, 790-797. [CrossRef] [PubMed]
  69. Zheng, Y.; Struck, D.K.; Young, R. Purification and functional characterization of phiX174 lysis protein E. Biochemistry 2009, 48, 4999-5006. [CrossRef] [PubMed]
  70. Karnik, S.; Billeter, M. The lysis function of RNA bacteriophage Qbeta is mediated by the maturation (A2) protein. EMBO J. 1983, 2, 1521-1526. [PubMed]
  71. Marvin, D.A.; Symmons, M.F.; Straus, S.K. Structure and assembly of filamentous bacteriophages. Prog. Biophys. Mol. Biol. 2014, 114, 80-122. [CrossRef] [PubMed]
  72. Poddar, S.K.; Cadden, S.P.; Das, J.; Maniloff, J. Heterogeneous progeny viruses are produced by a budding enveloped phage. Intervirology 1985, 23, 208-221. [CrossRef] [PubMed]
  73. Burge, S.; Kelly, E.; Lonsdale, D.; Mutowo-Muellenet, P.; McAnulla, C.; Mitchell, A.; Sangrador-Vegas, A.; Yong, S.-Y.; Mulder, N.; Hunter, S. Manual GO annotation of predictive protein signatures: The InterPro approach to GO curation. Database J. Biol. Databases Curation 2012, 2012. [CrossRef] [PubMed]
  74. Pedruzzi, I.; Rivoire, C.; Auchincloss, A.H.; Coudert, E.; Keller, G.; de Castro, E.; Baratin, D.; Cuche, B.A.; Bougueleret, L.; Poux, S.; et al. HAMAP in 2015: Updates to the protein family classification and annotation system. Nucleic Acids Res. 2015, 43, D1064-D1070. [CrossRef] [PubMed]
  75. Delattre, H.; Souiai, O.; Fagoonee, K.; Guerois, R.; Petit, M.-A. Phagonaute: A web-based interface for phage synteny browsing and protein function prediction. Virology 2016, 496, 42-50. [CrossRef] [PubMed]
  76. Category: CACAO-GONUTS. Available online: https://gowiki.tamu.edu/wiki/index.php/Category: CACAO (accessed on 16 May 2017).