1887

Microbial Genomics logo

Volume 6, Issue 2

bacteriophages: obscure past, promising future Open Access

Abstract

is a Gram-positive, spore-forming bacterium that is the causative agent of American foulbrood (AFB), the most devastating bacterial disease of the honeybee. is antibiotic resistant, complicating treatment efforts. Bacteriophages that target are rapidly emerging as a promising treatment. The first phages were isolated in the 1950s, but as was not antibiotic resistant at the time, interest in them remained scant. Interest in phages has grown rapidly since the first phage genome was sequenced in 2013. Since then, the number of sequenced phage genomes has reached 48 and is set to grow further. All sequenced phages encode a conserved -acetylmuramoyl--alanine amidase that is responsible for cleaving the peptidoglycan cell wall of . All phages also encode either an integrase, excisionase or Cro/CI, indicating that they are temperate. In the last few years, several studies have been published on using phages and the phage amidase as treatments for AFB. Studies were conducted on infected larvae and also on hives in the field. The phages have a prophylactic effect, preventing infection, and also a curative effect, helping resolve infection. phages have a narrow range, lysing only , and are unable to lyse even related species. phages thus appear to be safe to use and effective as treatment for AFB, and interest in them in the coming years will continue to grow.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): American foulbrood , Amidase , bacteriophage , genomics , honeybee and Paenibacillus larvae
© 2020 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000329
2020-01-28
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/2/mgen000329.html?itemId=/content/journal/mgen/10.1099/mgen.0.000329&mimeType=html&fmt=ahah

References

  1. Genersch E. American foulbrood in honeybees and its causative agent, Paenibacillus larvae . J Invertebr Pathol 2010; 103:S10–S19 [View Article]
     [Google Scholar]
  2. Genersch E, Ashiralieva A, Fries I. Strain- and genotype-specific differences in virulence of Paenibacillus larvae subsp. larvae, a bacterial pathogen causing American foulbrood disease in honeybees. Appl Environ Microbiol 2005; 71:7551–7555 [View Article]
     [Google Scholar]
  3. Yue D, Nordhoff M, Wieler LH, Genersch E. Fluorescence in situ hybridization (FISH) analysis of the interactions between honeybee larvae and Paenibacillus larvae, the causative agent of American foulbrood of honeybees (Apis mellifera). Environ Microbiol 2008; 10:1612–1620 [View Article]
     [Google Scholar]
  4. Lindström A, Korpela S, Fries I. The distribution of Paenibacillus larvae spores in adult bees and honey and larval mortality, following the addition of American foulbrood diseased brood or spore-contaminated honey in honey bee (Apis mellifera) colonies. J Invertebr Pathol 2008; 99:82–86 [View Article]
     [Google Scholar]
  5. Hasemann L. How long can spores of American foulbrood live?. Am Bee J 1961; 101:298–299
     [Google Scholar]
  6. Evans JD. Diverse origins of tetracycline resistance in the honey bee bacterial pathogen Paenibacillus larvae . J Invertebr Pathol 2003; 83:46–50 [View Article]
     [Google Scholar]
  7. Murray KD, Aronstein KA. Oxytetracycline-resistance in the honey bee pathogen Paenibacillus larvae is encoded on novel plasmid pMA67 . J Apic Res 2006; 45:207–214 [View Article]
     [Google Scholar]
  8. Miyagi T, Peng CYS, Chuang RY, Mussen EC, Spivak MS et al. Verification of oxytetracycline-resistant American foulbrood pathogen Paenibacillus larvae in the United States. J Invertebr Pathol 2000; 75:95–96 [View Article]
     [Google Scholar]
  9. Tian B, Fadhil NH, Powell JE, Kwong WK, Moran NA. Long-Term exposure to antibiotics has caused accumulation of resistance determinants in the gut microbiota of honeybees. mBio 2012; 3:e00377-12 [View Article]
     [Google Scholar]
  10. White GF. The Bacteria of the Apiary with Special Reference to Bee Disease, Technical Series no. 14 Washington, DC: Bureau of Entomology, USDA; 1906
     [Google Scholar]
  11. Katznelson H. Bacillus pulvifaciens (n. sp.), an organism associated with powdery scale of honeybee larvae. J Bacteriol 1950; 59:153–155 [View Article]
     [Google Scholar]
  12. Ash C, Priest FG, Collins MD. Molecular identification of rRNA group 3 bacilli (Ash, Farrow, Wallbanks and Collins) using a PCR probe test. Antonie van Leeuwenhoek 1994; 64:253–260 [View Article]
     [Google Scholar]
  13. Heyndrickx M, Vandemeulebroecke K, Hoste B, Janssen P, Kersters K et al. Reclassification of Paenibacillus (formerly Bacillus) pulvifaciens (Nakamura 1984) Ash et al. 1994, a later subjective synonym of Paenibacillus (formerly Bacillus) larvae (White 1906) Ash et al. 1994, as a subspecies of P. larvae, with emended descriptions of P. larvae as P. larvae subsp. larvae and P. larvae subsp. pulvifaciens . Int J Syst Bacteriol 1996; 46:270–279
     [Google Scholar]
  14. Genersch E, Forsgren E, Pentikäinen J, Ashiralieva A, Rauch S et al. Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. Int J Syst Evol Microbiol 2006; 56:501–511 [View Article]
     [Google Scholar]
  15. Smirnova NI. Isolation and the use of a bacteriophage of Bacillus larvae in the diagnosis of American foulbrood. Sbornik nauchnykh trudov Leningradskogo instituta usovershenstvovaniya veterinarykh vrachel 1953; 9:85–88 (in Russian)
     [Google Scholar]
  16. Gochnauer TA. The isolation of a bacteriophage (bacterial virus) from Bacillus larvae . Bee World 1955; 36:101–103 [View Article]
     [Google Scholar]
  17. Gochnauer TA, L’Arrivee JCM. Experimental infections with Bacillus larvae. II. Bacteriophage production in the host. J Invertebr Pathol 1969; 14:417–418
     [Google Scholar]
  18. Gochnauer TA. Some properties of a bacteriophage from Bacillus larvae . J Invertebr Pathol 1970; 15:149–156 [View Article]
     [Google Scholar]
  19. Valerianov T, Popova A, Toshkov AS. Isolation from the soil of a bacteriophage lysing Bacillus larvae . Acta Microbiol Virol Immunol 1976; 4:81–85
     [Google Scholar]
  20. Drobníková V, Ludvík J. Bacteriophage of Bacillus larvae . J Apic Res 1982; 21:53–56 [View Article]
     [Google Scholar]
  21. Benada O, Ludvík J, Drobníková V. Morphology of a new bacteriophage isolated from Bacillus larvae . Folia Microbiol 1984; 29:520–521 [View Article]
     [Google Scholar]
  22. Dingman DW, Bakhiet N, Field CC, Stahly DP. Isolation of two bacteriophages from Bacillus larvae, PBL1 and PBL0.5, and partial characterization of PBL1. J Gen Virol 1984; 65:1101–1105 [View Article]
     [Google Scholar]
  23. Bakhiet N, Stahly DP. Properties of clear plaque mutants of the Bacillus larvae bacteriophages PBL0.5 and PBL2. J Invertebr Pathol 1988; 52:78–83 [View Article]
     [Google Scholar]
  24. Campana CF, Bakhiet N, Stahly DP. Morphology of Bacillus larvae bacteriophage PBL3 and physical map of its DNA. J Invertebr Pathol 1991; 57:141–143 [View Article]
     [Google Scholar]
  25. Stahly DP, Alippi AM, Bakhiet N, Campana CF, Novak CC et al. PPL1c, a virulent mutant bacteriophage useful for identification of Paenibacillus larvae subspecies larvae. J Invertebr Pathol 1999; 74:295–296 [View Article]
     [Google Scholar]
  26. Oliveira A, Melo LDR, Kropinski AM, Azeredo J. Complete genome sequence of the broad-host-range Paenibacillus larvae phage phiIBB_Pl23. Genome Announc 2013; 1:e00438-13 [View Article]
     [Google Scholar]
  27. Beims H, Wittmann J, Bunk B, Spröer C, Rohde C et al. Paenibacillus larvae-directed bacteriophage HB10c2 and its application in American foulbrood-affected honey bee larvae. Appl Environ Microbiol 2015; 81:5411–5419 [View Article]
     [Google Scholar]
  28. Carson S, Bruff E, DeFoor W, Dums J, Groth A et al. Genome sequences of six Paenibacillus larvae Siphoviridae phages. Genome Announc 2015; 3:e00101-15 [View Article]
     [Google Scholar]
  29. Abraham J, Bousquet A-C, Bruff E, Carson N, Clark A et al. Paenibacillus larvae phage Tripp genome has 378-base-pair terminal repeats. Genome Announc 2016; 4:e01498-15 [View Article]
     [Google Scholar]
  30. Tsourkas PK, Yost DG, Krohn A, LeBlanc L, Zhang A et al. Complete genome sequences of nine phages capable of infecting Paenibacillus larvae, the causative agent of American foulbrood disease in honeybees. Genome Announc 2015; 3:e01120-15 [View Article]
     [Google Scholar]
  31. Walker JK, Merrill BD, Berg JA, Dhalai A, Dingman DW et al. Complete genome sequences of Paenibacillus larvae phages BN12, Dragolir, Kiel007, Leyra, Likha, Pagassa, PBL1c, and Tadhana. Genome Announc 2018; 6:e01602-17 [View Article]
     [Google Scholar]
  32. Merrill BD, Fajardo CP, Hilton JA, Payne AM, Ward AT et al. Complete genome sequences of 18 Paenibacillus larvae phages from the western United States. Microbiol Resource Announc 2018; 7:e00966-18
     [Google Scholar]
  33. Yost DG, Chang C, LeBlanc L, Cassin E, Peterman C et al. Complete Genome Sequences of Paenibacillus larvae Phages Halcyone, Heath, Scottie, and Unity from Las Vegas, Nevada. Microbiol Resour Announc 2018; 7:e00977-18 [View Article]
     [Google Scholar]
  34. Stamereilers C, LeBlanc L, Yost D, Amy PS, Tsourkas PK. Comparative genomics of 9 novel Paenibacillus larvae bacteriophages. Bacteriophage 2016; 6:e1220349 [View Article]
     [Google Scholar]
  35. Stamereilers C, Fajardo CP, Walker JK, Mendez KN, Castro-Nallar E et al. Genomic analysis of 48 Paenibacillus larvae bacteriophages. Viruses 2018; 10:377 [View Article]
     [Google Scholar]
  36. Yost DG, Tsourkas P, Amy PS. Experimental bacteriophage treatment of honeybees (Apis mellifera) infected with Paenibacillus larvae, the causative agent of American foulbrood disease. Bacteriophage 2016; 6:e1122698 [View Article]
     [Google Scholar]
  37. ICTV taxonomic proposal 2016.017a-dB.A.v1. Harrisonvirus: create genus Harrisonvirus in the family Siphoviridae, order Caudovirales; 2016. http://www.ictv.global/proposals-16/2016.017a-dB.A.v1.Harrisonvirus.pdf
     [Google Scholar]
  38. ICTV taxonomic proposal 2016.052a-dB.A.v1. Vegasvirus: create genus Vegasvirus in the family Siphoviridae, order Caudovirales; 2016. http://www.ictv.global/proposals-16/2016.052a-dB.A.v1.Vegasvirus.pdf
     [Google Scholar]
  39. Salisbury A, Tsourkas PK. A method for improving the accuracy and efficiency of bacteriophage genome annotation. Int J Mol Sci 2019; 20:e3391 [View Article]
     [Google Scholar]
  40. Merrill BD, Ward AT, Grose JH, Hope S. Software-based analysis of bacteriophage genomes, physical ends, and packaging strategies. BMC Genomics 2016; 17:679 [View Article]
     [Google Scholar]
  41. Casjens SR, Gilcrease EB. Determining DNA packaging strategy by analysis of the termini of the chromosomes in tailed-bacteriophage virions. In Clokie MRJ, Kropinski AM. (editors) Bacteriophages: Methods and Protocols, Volume 2: Molecular and Applied Aspects (Methods in Molecular Biology series vol. 502) New York: Humana Press; 2009 pp 91–111
     [Google Scholar]
  42. Young RY. Bacteriophage lysis: mechanism and regulation. Microbiol Rev 1992; 56:430–481
     [Google Scholar]
  43. Wang I-N, Smith DL, Young R. Holins: the protein clocks of bacteriophage infections. Annu Rev Microbiol 2000; 54:799–825 [View Article]
     [Google Scholar]
  44. Young I, Wang I, Roof WD. Phages will out: strategies of host cell lysis. Trends Microbiol 2000; 8:120–128 [View Article]
     [Google Scholar]
  45. Oliveira A, Leite M, Kluskens LD, Santos SB, Melo LD et al. The first Paenibacillus larvae bacteriophage endolysin (PlyPl23) with high potential to control American foulbrood. PLoS One 2015; 10:e0132095
     [Google Scholar]
  46. Santos SB, Oliveira A, Melo LDR, Azeredo J. Identification of the first endolysin cell binding domain (CBD) targeting Paenibacillus larvae . Sci Rep 2019; 9:2568 [View Article]
     [Google Scholar]
  47. LeBlanc L, Nezami S, Yost D, Tsourkas P, Amy PS. Isolation and characterization of a novel phage lysin active against Paenibacillus larvae, a honeybee pathogen. Bacteriophage 2015; 5:e1080787 [View Article]
     [Google Scholar]
  48. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 2015; 10:845–858 [View Article]
     [Google Scholar]
  49. Ghorbani-Nezami S, LeBlanc L, Yost DG, Amy PS. Phage therapy is effective in protecting honeybee larvae from American foulbrood disease. J Insect Sci 2015; 15:84–89 [View Article]
     [Google Scholar]
  50. Brady TS, Merrill BD, Hilton JA, Payne AM, Stephenson MB et al. Bacteriophages as an alternative to conventional antibiotic use for the prevention or treatment of Paenibacillus larvae in honeybee hives. J Invertebr Pathol 2017; 150:94–100 [View Article]
     [Google Scholar]
  51. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006; 23:254–267 [View Article]
     [Google Scholar]
  52. Cresawn SG, Bogel M, Day N, Jacobs-Sera D, Hendrix RW et al. Phamerator: a bioinformatic tool for comparative bacteriophage genomics. BMC Bioinformatics 2011; 12:395 [View Article]
     [Google Scholar]
  53. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001; 305:567–580 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000329
Loading
Paenibacillus larvae bacteriophages: obscure past, promising future
M Gen 6, e000329 (2020); https://doi.org/10.1099/mgen.0.000329
/content/journal/mgen/10.1099/mgen.0.000329
/content/journal/mgen/10.1099/mgen.0.000329
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error