Functional and comparative genome analysis of novel virulent actinophages belonging to Streptomyces flavovirens
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
PubMed
28257628
PubMed Central
PMC5336643
DOI
10.1186/s12866-017-0940-7
PII: 10.1186/s12866-017-0940-7
Knihovny.cz E-zdroje
- Klíčová slova
- Bacteriophage, Biological stability, Comparative genomics, NGS, Whole genome sequence,
- MeSH
- bakteriofágy genetika izolace a purifikace patogenita fyziologie MeSH
- biologická evoluce MeSH
- chlorid hořečnatý farmakologie MeSH
- chlorid sodný farmakologie MeSH
- chloridy farmakologie MeSH
- DNA virů izolace a purifikace MeSH
- fylogeneze MeSH
- genom virový genetika fyziologie MeSH
- genomika MeSH
- hostitelská specificita MeSH
- otevřené čtecí rámce genetika MeSH
- půda MeSH
- půdní mikrobiologie MeSH
- sekvence aminokyselin MeSH
- sekvence nukleotidů MeSH
- sekvenční analýza DNA MeSH
- sekvenční homologie nukleových kyselin MeSH
- sloučeniny zinku farmakologie MeSH
- Streptomyces virologie MeSH
- virion MeSH
- virové geny MeSH
- virové plášťové proteiny genetika MeSH
- virové proteiny genetika MeSH
- vysoce účinné nukleotidové sekvenování metody MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Egypt MeSH
- Názvy látek
- chlorid hořečnatý MeSH
- chlorid sodný MeSH
- chloridy MeSH
- DNA virů MeSH
- půda MeSH
- sloučeniny zinku MeSH
- virové plášťové proteiny MeSH
- virové proteiny MeSH
- zinc chloride MeSH Prohlížeč
BACKGROUND: Next Generation Sequencing (NGS) technologies provide exciting possibilities for whole genome sequencing of a plethora of organisms including bacterial strains and phages, with many possible applications in research and diagnostics. No Streptomyces flavovirens phages have been sequenced to date; there is therefore a lack in available information about S. flavovirens phage genomics. We report biological and physiochemical features and use NGS to provide the complete annotated genomes for two new strains (Sf1 and Sf3) of the virulent phage Streptomyces flavovirens, isolated from Egyptian soil samples. RESULTS: The S. flavovirens phages (Sf1 and Sf3) examined in this study show higher adsorption rates (82 and 85%, respectively) than other actinophages, indicating a strong specificity to their host, and latent periods (15 and 30 min.), followed by rise periods of 45 and 30 min. As expected for actinophages, their burst sizes were 1.95 and 2.49 virions per mL. Both phages were stable and, as reported in previous experiments, showed a significant increase in their activity after sodium chloride (NaCl) and magnesium chloride (MgCl2.6H2O) treatments, whereas after zinc chloride (ZnCl2) application both phages showed a significant decrease in infection. The sequenced phage genomes are parts of a singleton cluster with sizes of 43,150 bp and 60,934 bp, respectively. Bioinformatics analyses and functional characterizations enabled the assignment of possible functions to 19 and 28 putative identified ORFs, which included phage structural proteins, lysis components and metabolic proteins. Thirty phams were identified in both phages, 10 (33.3%) of them with known function, which can be used in cluster prediction. Comparative genomic analysis revealed significant homology between the two phages, showing the highest hits among Sf1, Sf3 and the closest Streptomyces phage (VWB phages) in a specific 13Kb region. However, the phylogenetic analysis using the Major Capsid Protein (MCP) sequences highlighted that the isolated phages belong to the BG Streptomyces phage group but are clearly separated, representing a novel sub-cluster. CONCLUSION: The results of this study provide the first physiological and genomic information for S. flavovirens phages and will be useful for pharmaceutical industries based on S. flavovirens and future phage evolution studies.
Botany and Microbiology Department Faculty of Science Helwan University Ain Helwan Cairo 11970 Egypt
Central Lab of Organic Agriculture Agricultural Research Center Giza 12619 Egypt
Genetic Department Faculty of Agriculture Ain Shams University Cairo 11241 Egypt
Institute of Biosciences and Bioresources of Italy 90129 Palermo Italy
Institute of Parasitology Biology Centre Czech Academy of Sciences 37005 České Budějovice Czechia
Microbiology Department Faculty of Agriculture Ain Shams University Cairo 11241 Egypt
Zobrazit více v PubMed
Klumpp J, Fouts DE, Sozhamannan S. Next generation sequencing technologies and the changing landscape of phage genomics. Bacteriophage. 2012;2(3):190–9. doi: 10.4161/bact.22111. PubMed DOI PMC
Sandmeier H. Acquisition and rearrangement of sequence motifs in the evolution of bacteriophage tail fibres. Mol Microbiol. 1994;12(3):343–50. doi: 10.1111/j.1365-2958.1994.tb01023.x. PubMed DOI
Juhala RJ, Ford ME, Duda RL, et al. Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol. 2000;299:27–51. doi: 10.1006/jmbi.2000.3729. PubMed DOI
Hendrix RW, Smith MCM, Burns RN, et al. Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proc Natl Acad Sci U S A. 1999;96:2192–7. doi: 10.1073/pnas.96.5.2192. PubMed DOI PMC
Hendrix RW. Bacteriophage genomics. Current Opinion in Microbiol. 2003;6:506–11. doi: 10.1016/j.mib.2003.09.004. PubMed DOI
Bradley SG, Ritzi D. Electron microscopical studies of actinophage multiplication. J Gen Virol. 1967;1(3):285–90. PubMed
Bull AT, Ward AC, Goodfellow M. Search and discovery strategies for biotechnology: the paradigm shift. Microbiol Mol Biol Rev. 2000;64:573–606. doi: 10.1128/MMBR.64.3.573-606.2000. PubMed DOI PMC
Ipek KD. Actinophages as indicators of actinomycete taxa in marine environments. Antonie Van Leeuwenhoek. 2005;87:19–28. doi: 10.1007/s10482-004-6535-y. PubMed DOI
Korn-Wendish F, Schneider J. Phage typing-a useful tool in actinomycete systematics. Gene. 1992;115:243–7. doi: 10.1016/0378-1119(92)90565-7. PubMed DOI
Williams ST, Locci R, Beswick A, et al. Detection and identification of novel actinomycetes. Res Microbiol. 1993;144(8):653–6. doi: 10.1016/0923-2508(93)90069-E. PubMed DOI
Ackerman HW, Berthiaume L, Jones LA. New actinophage species. InterVirology. 1985;23:121–30. doi: 10.1159/000149602. PubMed DOI
Othman BA, Askora AA, Awny NM, et al. Virulent Bacteriophages for Streptomyces griseoflsvus Isolated from Soil. Pak J Biotechnol. 2008;5:109–18.
Ashelford KE, Day MJ, Bailey MJ, et al. In situ population dynamics of bacterial viruses in a terrestrial environment. Appl Environ Microbiol. 1999;65:169–74. PubMed PMC
Ashelford KE, Day MJ, Fry JC. Elevated Abundance of Bacteriophage Infecting Bacteria in Soil. Appl Environ Microbiol. 2003;69(1):285–9. doi: 10.1128/AEM.69.1.285-289.2003. PubMed DOI PMC
Chater KF, Hopwood DA, Kieser T, et al. Gene cloning in Streptomyces. Curr Top Microbiol Immunol. 1982;96:69–95. PubMed
Harris JE, Chater KF, Bruton CJ, et al. The restriction mapping of c gene deletions in Streptomyces bacteriophage 4C31 and their use in cloning vector development. Gene. 1983;22(2–3):167–74. doi: 10.1016/0378-1119(83)90100-2. PubMed DOI
Oliver K. Grundwissen Pharmazeutische Biotechnologie. Vieweg + Teubner Verlag: Wiesbaden; 2002.
Satinder KB, Gurpreet SD, Carlos RS. Biotransformation of Waste Biomass into High Value Biochemicals. New York, NY: Springer New York; 2014.
Eisenstein M. Oxford Nanopore announcement sets sequencing sector abuzz. Nat Biotechnol. 2012;30:295–6. doi: 10.1038/nbt0412-295. PubMed DOI
Srivatsan A, Han Y, Peng J, et al. High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet 2008, doi:10.1371/journal.pgen.1000139. PubMed PMC
Hatfull GF. Bacteriophage genomics. Curr Opin Microbiol. 2008;11:447–53. doi: 10.1016/j.mib.2008.09.004. PubMed DOI PMC
Marei EM, Elbaz RM. Isolation and Molecular Characterization of Three Virulent Actinophages Specific for Streptomyces flavovirens. J Virol Res. 2013;2:12–17.
Lanning S, Williams ST. Methods for the direct isolation and enumeration of actinophages in soil. J Gen Microbiol. 1982;128:2063–71.
Dowding JE. Characterization of a bacteriophage virulent for Streptomyces coelicolor A3(2) J Gen Microbiol. 1973;76:163–176. doi: 10.1099/00221287-76-1-163. PubMed DOI
ADAMS MH. Methods of study of bacterial viruses. Methods in Med Research. 1950;2:1–73.
Paunikar WN, Sanmukh SG, Ghosh TK. Effect of metal ions and chemical solvents on the adsorption of Salmonella phage on Salmonella choleraesuis subspecies indica. Int J of Pharma and Biosci. 2012;3(1):181–190.
Adams MH. Bacteriophages. New York: Interscience; 1959.
Kieser T, Bibb MJ, Buttner MJ, et al. Practical Streptomyces Genetics. Norwich: The John Innes Foundation; 2000.
Lohsem M, Bolger AM, Nagel A, et al. RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res 2012, doi:10.1093/nar/gks540. PubMed PMC
Schatz MC, Phillippy AM, Shneiderman B, et al. Hawkeye: an interactive visual analytics tool for genome assemblies. Genome Biology 2007, doi:10.1186/gb-2007-8-3-r34. PubMed PMC
Hatfull GF, Jacobs-Sera D, Lawrence JG, et al. Comparative genomic analysis of sixty mycobacteriophage genomes: Genome clustering, gene acquisition and gene size. J Mol Biol. 2010;397(1):119–43. doi: 10.1016/j.jmb.2010.01.011. PubMed DOI PMC
Dobbins AT, George M, Jr, Basham DA, et al. Complete Genomic Sequence of the Virulent Salmonella Bacteriophage SP6. J Bacteriol. 2004;186(7):1933–44. doi: 10.1128/JB.186.7.1933-1944.2004. PubMed DOI PMC
Cresawn SG, Bogel M, Day N, et al. Phamerator: a bioinformatic tool for comparative bacteriophage genomics. BMC Bioinformatics. 2011;12:395. doi: 10.1186/1471-2105-12-395. PubMed DOI PMC
Altschul SF, Gish W, Miller W, et al. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI
Darling AE, Mau B, Perna NT. ProgressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010, doi:10.1371/journal.pone.0011147. PubMed PMC
Krzywinski M, Schein J, Birol I, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19(9):1639–45. doi: 10.1101/gr.092759.109. PubMed DOI PMC
Darzentas N. Circoletto: visualizing sequence similarity with Circos. Bioinformatics. 2010;26(20):2620–1. doi: 10.1093/bioinformatics/btq484. PubMed DOI
Kearse M, et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC
Anné J, Van Mellaert L, Decock B, et al. Further biological and molecular characterization of actinophage VWB. J Gen Microbiol. 1990;136:1365–1372. doi: 10.1099/00221287-136-7-1365. PubMed DOI
Pringsulaka O, Chvanich S, Doi K, et al. Characteristics and Distribution of Actinophages Isolated from Thai Soil Samples. Sci Asia. 2004;30:223–230. doi: 10.2306/scienceasia1513-1874.2004.30.223. DOI
AlKhazindar M, Sayed ETA, Khalil MS, et al. Isolation and Characterization of Two Phages Infecting Streptomyces scabies. Res J Pharm, Biol Chem Sci. 2016;7(2):1351–1363.
Binetti A, Quiberoni A, Reinheimer J. Phage adsorption to Streptococcus thermophilus. Influence of environmental factors and characterization of cell-receptors. Food Res Int. 2002;35:73–83. doi: 10.1016/S0963-9969(01)00121-1. DOI
Quiberoni A, Guglielmotti D, Binetti A, et al. Characterization of three Lactobacillus delbrueckii sub sp. bulgaricus phages and the physiochemical analysis of phage adsorption. J Appl Microbiol. 2004;96:340–351. doi: 10.1046/j.1365-2672.2003.02147.x. PubMed DOI
Robert B, Charles PJ. Characterization of the effect of aluminum metal on poliovirus. J of Indus Microbiol. 1988;3:33–38. doi: 10.1007/BF01569440. DOI
Brudno M, Do CB, Cooper GM, et al. NISC Comparative sequencing program LAGAN and multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res. 2003;13(4):721–31. doi: 10.1101/gr.926603. PubMed DOI PMC
Casjen SR, Thuman-Commike PA. Evolution of mosaically related bacteriophage genomes seen through the lens of phage P22 virion assembly. Virology. 2011;411:393–415. doi: 10.1016/j.virol.2010.12.046. PubMed DOI
Hendrix RW, Lawrence JG, Hatfull GF, et al. The origins and ongoing evolution of viruses. Trends Microbiol. 2000;8(11):504–8. doi: 10.1016/S0966-842X(00)01863-1. PubMed DOI
Petrovski S, Tillett D, Seviour RJ. Genome sequences and characterization of the Gordonia phages GTE5 and GRU1 and their use as potential biocontrol agents. Appl Environ Microbiol. 2012;78:42–7. doi: 10.1128/AEM.05584-11. PubMed DOI PMC
Rohwer F, Edwards R. The phage proteomic tree: a genome-based taxonomy of phage. J Bacteriol. 2002;184:4529–5. doi: 10.1128/JB.184.16.4529-4535.2002. PubMed DOI PMC
Marchler-Bauer A, Derbyshire MK, Gonzales NR, et al. CDD: NCBI's conserved domain database. Nucleic Acids Res. 2015;43(Database issue):222–6. doi: 10.1093/nar/gku1221. PubMed DOI PMC
Van Dessel W, Van Mellaert L, Liesegang H, et al. Complete genomic nucleotide sequence and analysis of the temperate bacteriophage VWB. J Anne Virology. 2005;331:325–37. doi: 10.1016/j.virol.2004.10.028. PubMed DOI
Grande L, Michelacci V, Tozzoli R, et al. Whole genome sequence comparison of vtx2-converting phages from Enteroaggregative Haemorrhagic Escherichia coli strains. BMC Genomics. 2014 PubMed PMC
Leon-Velarde CG, Kropinski AM, Chen S, et al. Complete genome sequence of bacteriophage vB_YenP_AP5 which infects Yersinia enterocolitica of serotype O:3. Virol J. 2014 PubMed PMC
Schouler C, Ehrlich SD, Chopin MC. Sequence and organization of the lactococcal prolate-headed bIL67 phage genome. Microbiology. 1994;140:3061–9. doi: 10.1099/13500872-140-11-3061. PubMed DOI
Ford ME, Sarkis GJ, Belanger AE, et al. Genome structure of mycobacteriophage D29: implications for phage evolution. J Mol Biol. 1998;279(1):143–64. doi: 10.1006/jmbi.1997.1610. PubMed DOI
Kropinski AM, Kovalyova IV, Billington SJ, et al. The genome of epsilon15, a serotype-converting, Group E1 Salmonella enterica-specific bacteriophage. Virology. 2007;369(2):234–44. doi: 10.1016/j.virol.2007.07.027. PubMed DOI PMC
Katsura I. Structure and inherent properties of the bacteriophage lambda head shell. VI. DNA-packaging-defective mutants in the major capsid protein. J Mol Biol. 1989;205(2):397–405. doi: 10.1016/0022-2836(89)90350-1. PubMed DOI
Lurz R, Orlova EV, Günther D, et al. Structural organisation of the head-to-tail interface of a bacterial virus. J Mol Biol. 2001;310(5):1027–37. doi: 10.1006/jmbi.2001.4800. PubMed DOI
Gual A, Camacho AG, Alonso JC. Functional analysis of the terminase large subunit, G2P, of Bacillus subtilis bacteriophage SPP1. J Biol Chem. 2000;275(45):35311–9. doi: 10.1074/jbc.M004309200. PubMed DOI
Noirot-Gros MF, Velten M, Yoshimura M, et al. Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis. Proc Natl Acad Sci U S A. 2006;103(7):2368–73. doi: 10.1073/pnas.0506914103. PubMed DOI PMC
Hayashi M, Ogura Y, Harry EJ, et al. Bacillus subtilis YabA is involved in determining the timing and synchrony of replication initiation. FEMS Microbiol Lett. 2005;247(1):73–9. doi: 10.1016/j.femsle.2005.04.028. PubMed DOI
Luscombe NM, Austin SE, Berman HM, et al. An overview of the structures of protein-DNA complexes. Genome Biol 2000, doi:10.1186/gb-2000-1-1-reviews001. PubMed PMC
Dutta R, Inouye M. GHKL, An emergent ATPase/kinase superfamily. Trends Biochem Sci. 2000;25(1):24–8. doi: 10.1016/S0968-0004(99)01503-0. PubMed DOI
Hvorup RN, Winnen B, Chang AB, et al. The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur J Biochem. 2003;270(5):799–813. doi: 10.1046/j.1432-1033.2003.03418.x. PubMed DOI
Satoh A, Wang Y, Malsam J, et al. Golgin-84 is a rab1 binding partner involved in Golgi structure. Traffic. 2003;4(3):153–61. doi: 10.1034/j.1600-0854.2003.00103.x. PubMed DOI PMC
Bruner SD, Norman DP, Verdine GL. Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA. Nature. 2000;403(6772):859–66. doi: 10.1038/35002510. PubMed DOI
Ibrahim H, Wilusz J, Wilusz CJ. RNA recognition by 3’-to-5’ exonucleases: the substrate perspective. Biochim Biophys Acta. 2008;1779(4):256–65. doi: 10.1016/j.bbagrm.2007.11.004. PubMed DOI PMC
Aravind L, Makarova KS, Koonin EV. SURVEY AND SUMMARY: holliday junction resolvases and related nucleases: identification of new families, phyletic distribution and evolutionary trajectories. Nucleic Acids Res. 2000;28(18):3417–32. doi: 10.1093/nar/28.18.3417. PubMed DOI PMC
Ku WY, Liu YW, Hsu YC, et al. The zinc ion in the HNH motif of the endonuclease domain of colicin E7 is not required for DNA binding but is essential for DNA hydrolysis. Nucleic Acids Res. 2002;30(7):1670–8. doi: 10.1093/nar/30.7.1670. PubMed DOI PMC
Cheng X, Zhang X, Pflugrath JW, et al. The structure of bacteriophage T7 lysozyme, a zinc amidase and an inhibitor of T7 RNA polymerase. Proc Natl Acad Sci U S A. 1994;91(9):4034–8. doi: 10.1073/pnas.91.9.4034. PubMed DOI PMC
Petrovski S, Seviour RJ, Tillett D. Genome characterization of the polyvalent lytic bacteriophage GTE2 with the potential for biocontrol of Gordonia, Rhodococcus and Nocardia stabilized foams in activated sludge plants. Appl Environ Microbiol. 2011;77(12):3923–9. doi: 10.1128/AEM.00025-11. PubMed DOI PMC
Petrovski S, Dyson ZA, Seviour RJ, et al. Small but sufficient: the Rhodococcus phage RRH1 has the smallest known Siphoviridae genome at 14.2 kb. J Virol. 2012;86:358–63. doi: 10.1128/JVI.05460-11. PubMed DOI PMC
Smith KC, Castro-Nallar E, Fisher JNB, et al. Phage cluster relationships identified through single gene analysis. BMC Genomics. 2013;14:410. doi: 10.1186/1471-2164-14-410. PubMed DOI PMC
Sullivan MB, Coleman ML, Quinlivan V, et al. Portal protein diversity and phage ecology. Environ Microbiol. 2008;10(10):2810–23. doi: 10.1111/j.1462-2920.2008.01702.x. PubMed DOI PMC
Hooton SP, Timms AR, Rowsell J, et al. Salmonella Typhimurium-specific bacteriophage FSH19 and the origins of species specificity in the Vi01-like phage family. Virol J. 2011;8:498. doi: 10.1186/1743-422X-8-498. PubMed DOI PMC
Dziarski R, Gupta D. Protein family review The peptidoglycan recognition proteins (PGRPs) Genome Biol. 2006;7:232. doi: 10.1186/gb-2006-7-8-232. PubMed DOI PMC
Aravind L, Anantharaman V, Balaji S, et al. The many faces of the helix-turn-helix domain: Transcription regulation and beyond. FEMS Microbiol Rev. 2005;29:231–62. doi: 10.1016/j.fmrre.2004.12.008. PubMed DOI
Wendt JL, Feiss M. A fragile lattice: replacing bacteriophage E’s head stability gene D with the shp gene of phage 21 generates the Mg2 + −dependent virus, E shp. Virology. 2004;326:41–6. doi: 10.1016/j.virol.2004.05.024. PubMed DOI
Clark AJ, Inwood W, Cloutier T, Dhillon TS. Nucleotide sequence of coliphage HK620 and the evolution of lambdoid phages. J Mol Biol. 2001;311:657–79. doi: 10.1006/jmbi.2001.4868. PubMed DOI
Canchaya C, Fournous G, Chibani-Chennoufi S, Dillmann ML, Brussow H. Phage as agents of lateral gene transfer. Curr Opin Microbiol. 2003;6:417–424. doi: 10.1016/S1369-5274(03)00086-9. PubMed DOI
Recktenwald J, Schmidt H. The nucleotide sequence of Shiga toxin (Stx) 2e-encoding phage phiP27 is not related to other Stx phage genomes, but the modular genetic structure is conserved. Infect Immun. 2002;70:1896–908. doi: 10.1128/IAI.70.4.1896-1908.2002. PubMed DOI PMC
Dekel-Bird NP, Avrani S, Sabehi G, Pekarsky I, Marston MF, Kirzner S, Lindell D. Diversity and evolutionary relationships of T7-like podoviruses infecting marine cyanobacteria. Environ Microbiol. 2013;15:1476–91. doi: 10.1111/1462-2920.12103. PubMed DOI
Lawrence JG, Hatfull GF, Hendrix RW. Imbroglios of viral taxonomy: genetic exchange and failings of phenetic approaches. J Bacteriol. 2002;184:4891–4905. doi: 10.1128/JB.184.17.4891-4905.2002. PubMed DOI PMC
Lima-Mendez G, Van Helden J, Toussaint A, Leplae R. Reticulate representation of evolutionary and functional relationships between phage genomes. Mol Biol Evol. 2008;25:762–77. doi: 10.1093/molbev/msn023. PubMed DOI