Skip to main content
Log in

Isolation, characterization, and comparative genomic analysis of vB_PlaM_Pd22F, a new bacteriophage of the family Myoviridae

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

The use of phage and phage-based products for the prevention and treatment of bee disease is one of the promising natural alternatives to chemical or antibiotic treatments in beekeeping. A novel lysogenic bacteriophage, phage Pd22F (vB_PlaM_Pd22F), was isolated from Paenibacillus dendritiformis by the prophage induction method. This phage, which is capable of infecting Paenibacillus larvae and P. dendritiformis strains, was characterized by microbiological and comparative genomic analysis. Transmission electron microscopy images showed that phage Pd22F had the morphology of a myovirus. Whole-genome sequencing results showed that vB_Pla M_Pd22F has an 86,388-bp linear dsDNA genome with a GC content of 50.68%. This genome has 124 coding sequences (CDSs), 53% of which encode functionally unknown proteins and 57 of which encode proteins that show similarity to known proteins. In addition, one tRNA gene was found. The phage Pd22F genome does not contain any antimicrobial resistance genes. The similarity between the genome sequence of phage Pd22F and the whole genome sequences of other Paenibacillus phages available in the NCBI Virus Database was found to be below 50% (42%), indicating that phage Pd22F differs greatly from previously characterized phages at the DNA level. The results of comparative genomics and phylogenetic analysis revealed that Pd22F is a new phage belonging to the family Myoviridae, order Caudovirales. This is the first report of genomic and morphological characterization of a Paenibacillus dendritiformis prophage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Genersch E (2010) American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. J Invertebr Pathol 103:S10–S19. https://doi.org/10.1016/j.jip.2009.06.015

    Article  PubMed  Google Scholar 

  2. Ingham CJ, Ben Jacob E (2008) Swarming and complex pattern formation in Paenibacillus vortex studied by imaging and tracking cells. BMC Microbiol 8:36. https://doi.org/10.1186/1471-2180-8-36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Be’er A, Strain SK, Hernandez RA, Ben-Jacob E, Florin EL (2013) Periodic reversals in Paenibacillus dendritiformis swarming. J Bacteriol 195:2709–2717. https://doi.org/10.1128/JB.00080-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Forsgren E (2010) European foulbrood in honey bees. J Invertebr Pathol 103(Suppl 1):S5-9. https://doi.org/10.1016/j.jip.2009.06.016

    Article  PubMed  Google Scholar 

  5. Bailey L, Ball BV (1991) Honey bee pathology, 2nd edn. Academic Press, London

    Google Scholar 

  6. White G (1912) The cause of European foulbrood. US Department of Agriculture Bureau of Entomology; Circular no. 157

  7. Gaggìa F, Baffoni L, Stenico V, Alberoni D, Buglione E, Lilli A, Di Gioia D, Porrini C (2015) Microbial investigation on honey bee larvae showing atypical symptoms of European foulbrood. Bull Insectol 68(2):321–327

    Google Scholar 

  8. Erler S, Lewkowski O, Poehlein A, Forsgren E (2018) The curious case of Achromobacter eurydice, a Gram-variable pleomorphic bacterium associated with European foulbrood disease in honeybees. Microb Ecol 75(1):1–6. https://doi.org/10.1007/s00248-017-1007-x

    Article  CAS  PubMed  Google Scholar 

  9. Lapidot D, Dror R, Vered E, Mishli O, Levy D, Helman Y (2015) Disease protection and growth promotion of potatoes (Solanum tuberosum L.) by Paenibacillus dendritiformis. Plant Pathol 64:545–551. https://doi.org/10.1111/ppa.12285

    Article  Google Scholar 

  10. Hubenova Y, Hubenova E, Mitov M (2020) Electroactivity of the Gram-positive bacterium Paenibacillus dendritiformis MA-72. Bioelectrochemistry 136:107632. https://doi.org/10.1016/j.bioelechem.2020.107632

    Article  CAS  PubMed  Google Scholar 

  11. Wittebole X, De Roock S, Opal SM (2014) A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence 5(1):226–235. https://doi.org/10.4161/viru.25991

    Article  PubMed  Google Scholar 

  12. Chanishvili N (2016) Bacteriophages as therapeutic and prophylactic means: summary of the Soviet and Post Soviet Experiences. Curr Drug Deliv 13:309–323. https://doi.org/10.2174/156720181303160520193946

    Article  CAS  PubMed  Google Scholar 

  13. Myelnikov D (2018) An alternative cure: the adoption and survival of phage therapy in the USSR, 1922–1955. J Hist Med Allied Sci 73:385–411. https://doi.org/10.1093/jhmas/jry024

    Article  PubMed  PubMed Central  Google Scholar 

  14. Lin DM, Koskella B, Lin HC (2017) Phage therapy: an alternative to antibiotics in the age of multi-drug resistance. World J Gastrointest Pharmacol Therap 8(3):162–173. https://doi.org/10.4292/wjgpt.v8.i3.162

    Article  Google Scholar 

  15. Oliveira A, Melo LDR, Kropinski AM, Azeredo J (2013) Complete genome sequence of the broad-host-range Paenibacillus larvae phage phiIBB_Pl23. Genome Announc 1(5):e00438-e513. https://doi.org/10.1128/genomeA.00438-13

    Article  PubMed  PubMed Central  Google Scholar 

  16. Carson S, Bruff E, DeFoor W, Dums J, Groth A, Hatfield T, Iyer A, Joshi K, McAdams S, Miles D, Miller D, Oufkir A, Raynor B, Riley S, Roland S, Rozier H, Talley S, Miller ES (2015) Genome sequences of six Paenibacillus larvae Siphoviridae phages. Genome Announc 3(3):e00101-e115. https://doi.org/10.1128/genomeA.00101

    Article  PubMed  PubMed Central  Google Scholar 

  17. Beims H, Wittmann J, Bunk B, Spröer C, Rohde C, Günther G, Rohde M, von der Ohe W, Steinert M (2015) Paenibacillus larvae-directed bacteriophage HB10c2 and its application in American foulbrood-affected honey bee larvae. Appl Environ Microbiol 81:5411–5419. https://doi.org/10.1128/AEM.00804-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Tsourkas PK, Yost D, Krohn A, Leblanc L, Zhang A, Stamereilers C, Amy PS (2015) Complete genome sequences of nine phages capable of infecting Paenibacillus larvae, the causative agent of American foulbrood disease of honeybees. Genome Announc 3(5):e01120-e1215. https://doi.org/10.1128/genomeA.01120-15

    Article  PubMed  PubMed Central  Google Scholar 

  19. Walker JK, Merrill BD, Berg JA, Dhalai A, Dingman DW, Fajardo CP, Graves K, Hill HL, Hilton JA, Imahara C, Knabe BK, Mangohig J, Monk J, Mun H, Payne AM, Salisbury A, Stamereilers C, Velez K, Ward AT, Breakwell DP, Grose JH, Hope S, Tsourkas PK (2018) Complete genome sequences of Paenibacillus larvae phages BN12, Dragolir, Kiel007, Leyra, Likha, Pagassa, PBL1c, and Tadhana. Genome Announc 6:e01602-e1617. https://doi.org/10.1128/genomeA.01602-17

    Article  PubMed  PubMed Central  Google Scholar 

  20. Ribeiro HG, Melo LDR, Oliveira H, Boon M, Lavigne R, Noben JP, Azeredo J, Oliveira A (2019) Characterization of a new Podovirus infecting Paenibacillus larvae. Sci Rep 9:20355. https://doi.org/10.1038/s41598-019-56699-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Stamereilers C, Fajardo CP, Walker JK, Mendez KN, Castro-Nallar E, Grose JH, Hope S, Tsourkas PK (2018) Genomic Analysis of 48 Paenibacillus larvae Bacteriophages. Viruses 10(7):377. https://doi.org/10.3390/v10070

    Article  PubMed Central  Google Scholar 

  22. Tsourkas PK (2020) Paenibacillus larvae bacteriophages: obscure past, promising future. Microbial Genomics 6(2):e000329. https://doi.org/10.1099/mgen.0.000329

    Article  CAS  PubMed Central  Google Scholar 

  23. Pınarbaş M, Alpay Karaoğlu S (2017) Characterization and antibiotic sensitiveness of gram positive bacteri̇a isolated from American foulbrood suspect bee (Apis mellifera) and bee products, with genetic di̇versity of Paenibacillus larvae isolates. Recep Tayyip Erdogan University, Graduate School of Natural and Applied Sciences, Department of Biology, 117s

  24. Karali M and Alpay Karaoglu S (2019) Investigation of bacteriophage/bacteriocin presence and host width in Paenibacillus dendritiformis isolates. Recep Tayyip Erdogan University, Graduate School of Natural and Applied Sciences, Department of Biology, 61s

  25. Vallat B, Edwards S, O’Neill B (2012) Manuel of diagnostic tests and vaccines for terrestrial animals. OIE 1:365–380

    Google Scholar 

  26. De Graaf DC, Alippi AM, Antúnez K, Aronstein KA, Budge G, De Koker D, De Smet L, Dingman DW, Evans JD, Foster LJ, Fünfhaus A, Garcia-Gonzalez E, Gregorc A, Human H, Murray KD, Nguyen BK, Poppinga L, Spivak M, Van Engelsdorp D, Wilkins S, Genersch E (2013) Standard methods for American foulbrood research. J Apicultural Res. https://doi.org/10.3896/IBRA.1.52.1.11

    Article  Google Scholar 

  27. Bakonyi T, Derakhshifar I, Grabensteiner E, Nowotny N (2003) Development and evaluation of PCR assays for the detection of Paenibacillus larvae in honey samples: comparison with isolation and biochemical characterization. Appl Environ Microbiol 6:1504–1510. https://doi.org/10.1128/AEM.69.3.1504-1510.2003

    Article  CAS  Google Scholar 

  28. Halebian S, Harris B, Finegold SM, Rolfe RD (1981) Rapid method that aids in distinguishing Gram-positive from Gram-negative anaerobic bacteria. J Clin Microbiol 13(3):444–448. https://doi.org/10.1128/jcm.13.3.444-448.1981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Rohde M (2011) Microscopy, taxonomy of prokaryotes. Methods Microbiol 38:61–100. https://doi.org/10.1016/B978-0-12-387730-7.00004-8

    Article  CAS  Google Scholar 

  30. Sambrook J, Fritsch ER, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  31. Dobbelaere W, de Graaf DC, Peeters JE (2001) Development of a fast and reliable diagnostic method for American foulbrood disease (Paenibacillus larvae subsp. larvae) using a 16S rRNA gene based PCR. Apidologie 32(4):363–370. https://doi.org/10.1051/apido:2001136

    Article  CAS  Google Scholar 

  32. Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55(3):541–555. https://doi.org/10.1016/j.mimet.2003.08.009

    Article  CAS  PubMed  Google Scholar 

  33. Rivas R, Velázquez E, Zurdo-Piñeiro JL, Mateos PF, Martínez Molina E (2004) Identification of microorganisms by PCR amplification and sequencing of a universal amplified ribosomal region present in both prokaryotes and eukaryotes. J Microbiol Methods 56(3):413–426. https://doi.org/10.1016/j.mimet.2003.11.007

    Article  CAS  PubMed  Google Scholar 

  34. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

    Article  CAS  PubMed  Google Scholar 

  35. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol Biol Evol 9:678–687. https://doi.org/10.1093/oxfordjournals.molbev.a040752

    Article  CAS  PubMed  Google Scholar 

  37. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x

    Article  PubMed  Google Scholar 

  38. Muniesa M, Jofre J (2007) The contribution of induction of temperate phages to the numbers of free somatic coliphages in waters is not significant. FEMS Microbiol Lett 270:272–276. https://doi.org/10.1111/j.1574-6968.2007.00676.x

    Article  CAS  PubMed  Google Scholar 

  39. Dingman DW, Bakhiet N, Field CC, Stahly DP (1984) Isolation of two bacteriophages from Bacillus larvae, PBL1 and PBL0.5, and partial characterization of PBL1. J Gen Virol 65:1101–1105. https://doi.org/10.1099/0022-1317-65-6-1101

    Article  PubMed  Google Scholar 

  40. Bradley DE (1967) Ultrastructure of bacteriophage and bacteriocins. Bacteriol Rev 31(4):230–314. https://doi.org/10.1128/br.31.4.230-314.1967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hershey AD, Dove W (1983) Introduction to lambda. In: Hendrix RW, Roberts JW, Stahl WF, Weisberg RA (eds) Lambda II. Cold Spring Harbor, Cold Spring Harbor Laboratory, pp 3–20

    Google Scholar 

  42. Roberts JW, Devoret R (1983) Lysogenic induction. In: Hendrix RW, Roberts JW, Stahl FW, Weisberg RA (eds) Lambda II. Cold Spring Harbor, Cold Spring Harbor Laboratory, pp 123–144

    Google Scholar 

  43. Kiliç AO, Pavlova SI, Alpay S, Kiliç SS, Tao L (2001) Comparative study of vaginal Lactobacillus phages isolated from women in the United States and Turkey: prevalence, morphology, host range, and DNA homology. Clin Diagn Lab Immunol 8(1):31–39. https://doi.org/10.1128/CDLI.8.1.31-39.2001

    Article  PubMed  PubMed Central  Google Scholar 

  44. Hurst CJ, Reynolds KA (2002) Chapter 48: sampling viruses from soil. In: Hurst CJ, Crawford RL, Knudsen GR, McInerney MJ, Stetzenbach DL (eds) Manual of environmental microbiology, 2nd edn. American Society for Microbiology Press, Washington DC, pp 527–534

    Google Scholar 

  45. Santos SB, Carvalho CM, Sillankorva S, Nicolau A, Ferreira EC, Azeredo J (2009) The use of antibiotics to improve phage detection and enumeration by the double-layer agar technique. BMC Microbiol 9:148. https://doi.org/10.1186/1471-2180-9-148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Kim M, Ryu S (2011) Characterization of a T5-like coliphage, SPC35, and differential development of resistance to SPC35 in Salmonella enterica serovar typhimurium and Escherichia coli. Appl Environ Microbiol 77(6):2042–2050. https://doi.org/10.1128/AEM.02504-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Fauquet C, Mayo MA, Maniloff J, Desselberger U, Ball LA (2005) Virus taxonomy. In: Eighth report of the international committee on the taxonomy of viruses. Elsevier Academic Press, San Diego, CA

  48. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680a0

    Article  CAS  PubMed  Google Scholar 

  49. Pickard DJ (2009) Preparation of bacteriophage lysates and pure DNA. Methods Mol Biol 502:3–9. https://doi.org/10.1007/978-1-60327-565-1_1

    Article  CAS  PubMed  Google Scholar 

  50. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477. https://doi.org/10.1089/cmb.2012.0021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Wick RR, Judd LM, Gorrie CL, Holt KE (2017) Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 13(6):e1005595. https://doi.org/10.1371/journal.pcbi.1005595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2014) The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 42(Database issue):D206–D214. https://doi.org/10.1093/nar/gkt1226

    Article  CAS  PubMed  Google Scholar 

  53. Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679. https://doi.org/10.1093/bioinformatics/btm009

    Article  CAS  PubMed  Google Scholar 

  54. Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform 11:119. https://doi.org/10.1186/1471-2105-11-119

    Article  CAS  Google Scholar 

  55. Borodovsky M, Lomsadze A (2011) Gene identification in prokaryotic genomes, phages, metagenomes, and EST sequences with GeneMarkS suite. Curr Protoc Bioinform 4(5):1–17. https://doi.org/10.1002/0471250953.bi0405

    Article  Google Scholar 

  56. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomason JA, Stevens R, Vonstein V, Wattam AR, Xia F (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:8365. https://doi.org/10.1038/srep08365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402. https://doi.org/10.1093/nar/25.17.3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  59. Laslett D, Canback B (2004) ARAGORN, A program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32(1):11–16. https://doi.org/10.1093/nar/gkh152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Garneau JR, Depardieu F, Fortier LC, Bikard D, Monot M (2017) PhageTerm: a tool for fast and accurate determination of phage termini and packaging mechanism using next-generation sequencing data. Sci Rep 7(1):8292. https://doi.org/10.1038/s41598-017-07910-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Stothard P, Wishart DS (2005) Circular genome visualization and exploration using CGView. Bioinformatics 21(4):537–539. https://doi.org/10.1093/bioinformatics/bti054

    Article  CAS  PubMed  Google Scholar 

  62. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305(3):567–580. https://doi.org/10.1006/jmbi.2000.4315

    Article  CAS  PubMed  Google Scholar 

  63. Nishimura Y, Yoshida T, Kuronishi M, Uehara H, Ogata H, Goto S (2017) ViPTree: the viral proteomic tree server. Bioinformatics 33(15):2379–2380. https://doi.org/10.1093/bioinformatics/btx157

    Article  CAS  PubMed  Google Scholar 

  64. Lopes A, Tavares P, Petit MA, Guérois R, Zinn-Justin S (2014) Automated classification of tailed bacteriophages according to their neck organization. BMC Genom 15:1027. https://doi.org/10.1186/1471-2164-15-1027

    Article  CAS  Google Scholar 

  65. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

  66. Ronquist F, Huelsenbeck JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574. https://doi.org/10.1093/bioinformatics/btg180

    Article  CAS  PubMed  Google Scholar 

  67. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67(5):901–904. https://doi.org/10.1093/sysbio/syy032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Rambaut A (2012) FigTree 1.4.0 software. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh

  70. Kropinski AM, Prangishvili D, Lavigne R (2009) Position paper: the creation of a rational scheme for the nomenclature of viruses of Bacteria and Archaea. Environ Microbiol 11:2775–2777. https://doi.org/10.1111/j.1462-2920.2009.01970.x

    Article  PubMed  Google Scholar 

  71. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy Server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, New Jersey, pp 571–607

    Chapter  Google Scholar 

  72. Wu Y (2012) Unwinding and rewinding: double faces of helicase? J Nucleic Acids 140601:1–15. https://doi.org/10.1155/2012/140601

    Article  CAS  Google Scholar 

  73. Fuller-Pace FV, Ali S (2008) The DEAD box RNA helicases p68 (Ddx5) and p72 (Ddx17): novel transcriptional co-regulators. Biochem Soc Trans 36(Pt 4):609–612. https://doi.org/10.1042/BST0360609

    Article  CAS  PubMed  Google Scholar 

  74. Schütz P, Karlberg T, van den Berg S, Collins R, Lehtiö L, Högbom M, Holmberg-Schiavone L, Tempel W, Park HW, Hammarström M, Moche M, Thorsell AG, Schüler H (2010) Comparative structural analysis of human DEAD-box RNA helicases. PLoS ONE 5(9):e12791. https://doi.org/10.1371/journal.pone.0012791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Edgell DR, Belfort M, Shub DA (2000) Barriers to intron promiscuity in bacteria. J Bacteriol 182(19):5281–5289. https://doi.org/10.1128/JB.182.19.5281-5289.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Chapot-Chartier MP (2014) Interactions of the cell-wall glycopolymers of lactic acid bacteria with their bacteriophages. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00236

    Article  PubMed  PubMed Central  Google Scholar 

  77. Wang IN, Smith DL, Young R (2002) Holins: the protein clocks of bacteriophage infections. Annu Rev Microbiol 54:799–825. https://doi.org/10.1146/annurev.micro.54.1.799

    Article  Google Scholar 

  78. Stark W, Boocock MR, Sherratt DJ (1992) Catalysis by site-specific recombinases. Trends Genet 8:432–439

    Article  CAS  PubMed  Google Scholar 

  79. Hatfull GF, Hendrix RW (2011) Bacteriophages and their genomes. Curr Opin Virol 1:298–303. https://doi.org/10.1016/j.coviro.2011.06.009

    Article  CAS  PubMed  Google Scholar 

  80. Duffy C, Feiss M (2002) The large subunit of bacteriophage lambda’s terminase plays a role in DNA translocation and packaging termination. J Mol Biol 316(3):547–561. https://doi.org/10.1006/jmbi.2001.5368

    Article  CAS  PubMed  Google Scholar 

  81. Cepko LCS, Garling EE, Dinsdale MJ, Scott WP, Bandy L, Nice T, Faber-Hammond J, Mellies JL (2020) Myoviridae phage PDX kills enteroaggregative Escherichia coli without human microbiome dysbiosis. J Med Microbiol 69(2):309–323. https://doi.org/10.1099/jmm.0.001162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. McSpadden GBB (2004) Ecology of Bacillus and Paenibacillus spp. in agricultural systems. Phytopathology 94(11):1252–1258. https://doi.org/10.1094/PHYTO.2004.94.11.1252

    Article  Google Scholar 

  83. Ruiu L (2020) Plant-Growth-Promoting Bacteria (PGPB) against Insects and Other Agricultural Pests. Agronomy 10(6):861. https://doi.org/10.3390/agronomy10060861

    Article  CAS  Google Scholar 

  84. Sirota-Madi A, Olender T, Helman Y, Ingham C, Brainis I, Roth D, Hagi E, Brodsky L, Leshkowitz D, Galatenko V, Nikolaev V, Mugasimangalam RC, Bransburg-Zabary S, Gutnick DL, Lancet D, Ben-Jacob E (2010) Genome sequence of the pattern forming Paenibacillus vortex bacterium reveals potential for thriving in complex environments. BMC Genom 11:710. https://doi.org/10.1186/1471-2164-11-710

    Article  CAS  Google Scholar 

  85. Dowah ASA, Clokie MRJ (2018) Review of the nature, diversity and structure of bacteriophage receptor binding proteins that target Gram-positive bacteria. Biophys Rev 10:535–542. https://doi.org/10.1007/s12551-017-0382-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. De Jonge PA, Nobrega FL, Brouns SJ, Dutilh BE (2019) Molecular and evolutionary determinants of bacteriophage host range. Trends Microbiol 27:51–63. https://doi.org/10.1016/j.tim.2018.08.006

    Article  CAS  PubMed  Google Scholar 

  87. Merrill BD, Grose JH, Breakwell DP, Burnett SH (2014) Characterization of Paenibacillus larvae bacteriophages and their genomic relationships to firmicute bacteriophages. BMC Genom 15(1):745. https://doi.org/10.1186/1471-2164-15-745

    Article  Google Scholar 

  88. Delesalle VA, Tanke NT, Vill AC, Krukonis GP (2016) Testing hypotheses for the presence of tRNA genes in mycobacteriophage genomes. Bacteriophage 6(3):e1219441. https://doi.org/10.1080/21597081.2016.121944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Sharaf A, Oborník M, Hammad A, El-Afifi S, Marei E (2018) Characterization and comparative genomic analysis of virulent and temperate Bacillus megaterium bacteriophages. Peer J 6:e5687. https://doi.org/10.7717/peerj.5687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Merrill BD, Ward AT, Grose JH, Hope S (2016) Software-based analysis of bacteriophage genomes, physical ends, and packaging strategies. BMC Genom 17(1):679. https://doi.org/10.1186/s12864-016-3018-2

    Article  Google Scholar 

  91. Grose JH, Jensen GL, Burnett SH, Breakwell DP (2014) Correction: genomic comparison of 93 Bacillus phages reveals 12 clusters, 14 singletons and remarkable diversity. BMC Genom 15(1):1184. https://doi.org/10.1186/1471-2164-15-1184

    Article  Google Scholar 

  92. Thorpe HM, Smith MC (1998) In vitro site-specific integration of bacteriophage DNA catalyzed by a recombinase of the resolvase/invertase family. Proc Natl Acad Sci USA 95(10):5505–5510. https://doi.org/10.1073/pnas.95.10.5505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Rezaei Javan R, Ramos-Sevillano E, Akter A, Brown J, Brueggemann AB (2019) Prophages and satellite prophages are widespread in Streptococcus and may play a role in pneumococcal pathogenesis. Nat Commun 10(1):4852. https://doi.org/10.1038/s41467-019-12825-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Rocker A, Meinhart A (2016) Type II toxin: Antitoxin systems. More than small selfish entities? Curr Genet 62(2):287–290. https://doi.org/10.1007/s00294-015-0541-7

    Article  CAS  PubMed  Google Scholar 

  95. Van Melderen L (2010) Toxin-antitoxin systems: why so many, what for? Curr Opin Microbiol 13(6):781–785. https://doi.org/10.1016/j.mib.2010.10.006

    Article  CAS  PubMed  Google Scholar 

  96. Yamaguchi Y, Inouye M (2011) Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat Rev Microbiol 9(11):779–790. https://doi.org/10.1038/nrmicro2651

    Article  CAS  PubMed  Google Scholar 

  97. Wang X, Lord DM, Cheng HY, Osbourne DO, Hong SH, Sanchez-Torres V, Quiroga C, Zheng K, Herrmann T, Peti W, Benedik MJ, Page R, Wood TK (2012) A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS. Nat Chem Biol 8:855–861. https://doi.org/10.1038/nchembio.1062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Page R, Peti W (2016) Toxin-antitoxin systems in bacterial growth arrest and persistence. Nat Chem Biol 12:208–214. https://doi.org/10.1038/nchembio.2044

    Article  CAS  PubMed  Google Scholar 

  99. Yao J, Guo Y, Wang P, Zeng Z, Li B, Tang K, Liu X, Wang X (2018) Type II toxin/antitoxin system ParESO/CopASO stabilizes prophage CP4So in Shewanella oneidensis. Environ Microbiol 20(3):1224–1239. https://doi.org/10.1111/1462-2920.14068

    Article  CAS  PubMed  Google Scholar 

  100. Breitbart M, Miyake JH, Rohwer F (2004) Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol Lett 236:249–256. https://doi.org/10.1016/j.femsle.2004.05.042

    Article  CAS  PubMed  Google Scholar 

  101. Chow CET, Fuhrman JA (2012) Seasonality and monthly dynamics of marine Myovirus communities. Environ Microbiol 14(8):2171–2183. https://doi.org/10.1111/j.1462-2920.2012.02744.x

    Article  PubMed  Google Scholar 

  102. Wommack KE, Nasko DJ, Chopyk J, Sakowski EG (2015) Counts and sequences, observations that continue to change our understanding of viruses in nature. J Microbiol 53:181–192. https://doi.org/10.1007/s12275-015-5068-6

    Article  CAS  PubMed  Google Scholar 

  103. Rohwer F, Edwards R (2002) The Phage Proteomic Tree: a genome-based taxonomy for phage. J Bacteriol 184:4529–4535. https://doi.org/10.1128/JB.184.16.4529-4535.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Sullivan MB, Coleman M, Weigele P, Rohwer F, Chisholm SW (2005) Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3:e144. https://doi.org/10.1371/journal.pbio.0030144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Hambly E, Tetart F, Desplats C, Wilson WH, Krisch HM, Mann NH (2001) A conserved genetic module that encodes the major virion components in both the coliphage T4 and the marine cyanophage S-PM2. Proc Natl Acad Sci USA 98(20):11411–11416. https://doi.org/10.1073/pnas.191174498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Hsiao CL, Black LW (1978) Head morphogenesis of bacteriophage T4. III. The role of g20 in DNA packaging. Virology 91(1):15–25. https://doi.org/10.1016/0042-6822(78)90351-3

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Sincere thanks to Bayram Toraman of Karadeniz Technical University for providing advice on bioinformatics application. Thanks to Dr. Cantekin Dursun of Recep Tayyip Erdoğan University for providing help on the phylogenetic tree of phages. We thank Elif Sevim and Müberra Pinarbaş for their technical comments and assistance in the study.

Funding

This study was financially supported by the RTEU Scientific Research Projects (RTEU-FBA-2017-807).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study's conception and design. Material preparation, experimental studies, data collection, evaluation of results, and interpretation of bioinformatic analysis were performed by Arif Bozdeveci and Şengül Alpay Karaoğlu. The main draft of the article was written by Arif Bozdeveci and Şengül Alpay Karaoğlu, and all authors contributed to and commented on the main draft of the article. All authors read and approved the final version of the manuscript.

Corresponding author

Correspondence to Şengül Alpay Karaoğlu.

Ethics declarations

Conflict of interest

The authors have no financial conflicts of interest to declare.

Additional information

Handling Editor: Tim Skern.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bozdeveci, A., Karali, M., Akpinar, R. et al. Isolation, characterization, and comparative genomic analysis of vB_PlaM_Pd22F, a new bacteriophage of the family Myoviridae. Arch Virol 167, 1269–1284 (2022). https://doi.org/10.1007/s00705-022-05429-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-022-05429-3

Navigation