Archives of Virology

, Volume 161, Issue 1, pp 149–158 | Cite as

Isolation and characterization of bacteriophage SPI1, which infects the activated-sludge-foaming bacterium Skermania piniformis

  • Z. A. Dyson
  • J. Tucci
  • R. J. Seviour
  • S. Petrovski
Brief Report


Foaming in activated sludge plants is a worldwide problem commonly caused by proliferation of bacteria of the order Corynebacteriales. These include Skermania piniformis, a filamentous bacterium that has been documented to be a major cause of foaming globally, and particularly in Australian treatment plants. Phage SPI1 is the first phage that was isolated and shown to infect this organism. It targets seven of the nine strains of S. piniformis held in our culture collection, but none of the other 73 mycolata strains of different genera, mostly isolated from wastewater, against which it was tested. Phage SPI1 is a member of the family Siphoviridae and has a circularly permuted dsDNA genome of 55,748 bp with a G+C content of 67.8 mol %. It appears to be obligatorily lytic, with no evidence of genes related to a lysogenic mode of existence.


Phage Bacteriophage Skermania piniformis PTLO Activated sludge foaming Bio-control Wgs Phage therapy 



The authors thank Dr. Alexander Fink (La Trobe University) for assistance with transmission electron microscopy, and Dr. Daniel Tillett for useful discussions. Z.A. Dyson was the recipient of an Australian Postgraduate Award PhD Scholarship. The authors declare no conflict of interest.

Supplementary material

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Supplementary material 1 (DOCX 52 kb)
705_2015_2631_MOESM2_ESM.docx (41 kb)
Supplementary material 2 (DOCX 41 kb)


  1. 1.
    Ammelburg M, Frickey T, Lupas AN (2006) Classification of AAA+ proteins. J Struct Biol 156:2–11PubMedCrossRefGoogle Scholar
  2. 2.
    Blackall LL, Harbers AE, Greenfield PF, Hayward AC (1991) Foaming in activated sludge plants: a survey in Queensland, Australia and an evaluation of some control strategies. Water Res 25:313–317CrossRefGoogle Scholar
  3. 3.
    Catalano CE (2000) The terminase enzyme from bacteriophage lambda: a DNA-packaging machine. Cell Mol Life Sci 57:128–148PubMedCrossRefGoogle Scholar
  4. 4.
    Chun J, Blackall LL, Kang S-O, Hah YC, Goodfellow M (1997) A proposal to reclassify Nocardia pinensis Blackall et al. as Skermania pinifomis gen. nov., comb. nov. IJSEM 47:127–131Google Scholar
  5. 5.
    Cserzo M, Wallin E, Simon I, Gv Heijne, Elofsson A (1997) Prediction of transmembrane alpha-helices in procariotic membrane proteins: the Dense Alignment Surface method. Protein Eng 10:673–676PubMedCrossRefGoogle Scholar
  6. 6.
    Daniel A, Bonnen PE, Fischetti VA (2007) First complete genome sequence of two Staphylococcus epidermidis bacteriophages. J Bacteriol 189:2086–2100PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    de los Reyes FL III (2010) Foaming. In: Seviour RJ, Nielsen PH (eds) Microbial ecology of activated sludge. IWA Publishing, London, pp 215–258Google Scholar
  8. 8.
    Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Deng Z, Kieser T, Hopwood DA (1987) Activity of a Streptomyces transcriptional terminator in Escherichia coli. Nucleic Acids Res 15:2665–2675PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Fujisawa H, Morita M (1997) Phage DNA packaging. Genes Cells 2:537–545PubMedCrossRefGoogle Scholar
  11. 11.
    Goddard AJ, Forster CF (1987) Stable foams in activated sludge plants. Enzyme Microb Technol 9:164–168CrossRefGoogle Scholar
  12. 12.
    Hatfull GF, Jacobs-Sera D, Lawrence JG, Pope WH, Russell DA, Ko CC, Weber RJ, Patel MC, Germane KL, Edgar RH, Hoyte NN, Bowman CA, Tantoco AT, Paladin EC, Myers MS, Smith AL, Grace MS, Pham TT, O’Brien MB, Vogelsberger AM, Hryckowian AJ, Wynalek JL, Donis-Keller H, Bogel MW, Peebles CL, Cresawn SG, Hendrix RW (2010) Comparative genomic analysis of 60 mycobacteriophage genomes: genome clustering, gene acquisition, and gene size. J Mol Biol 397:119–143PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Jenkins D, Daigger GT, Richard MG (1993) Manual on the causes and control of activated sludge bulking and foaming. Lewis, United StatesGoogle Scholar
  14. 14.
    Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327PubMedCrossRefGoogle Scholar
  15. 15.
    Laslett D, Canback B (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32:11–16PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Lesnik EA, Sampath R, Levene HB, Henderson TJ, McNeil JA, Ecker DJ (2001) Prediction of rho-independent transcriptional terminators in Escherichia coli. Nucleic Acids Res 29:3583–3594PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Lipps G, Weinzierl AO, von Scheven G, Buchen C, Cramer P (2004) Structure of a bifunctional DNA primase-polymerase. Nat Struct Mol Biol 11:157–162PubMedCrossRefGoogle Scholar
  18. 18.
    Lu Z, Altermann E, Breidt F, Kozyavkin S (2010) Sequence analysis of Leuconostoc mesenteroides bacteriophage Φ1-A4 isolated from an industrial vegetable fermentation. Appl Environ Microbiol 76:1955–1966PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    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, Hendrix RW, Hatfull GF (2003) Origins of highly mosaic mycobacteriophage genomes. Cell 113:171–182PubMedCrossRefGoogle Scholar
  20. 20.
    Petrovski S, Dyson ZA, Quill ES, McIlroy SJ, Tillett D, Seviour RJ (2011) An examination of the mechanisms for stable foam formation in activated sludge systems. Water Res 45:2146–2154PubMedCrossRefGoogle Scholar
  21. 21.
    Petrovski S, Seviour RJ, Tillett D (2011) Genome sequence and characterization of the Tsukamurella bacteriophage TPA2. Appl Environ Microbiol 77:1389–1398PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Petrovski S, Seviour RJ, Tillett D (2011) Characterization of the genome of the polyvalent lytic bacteriophage GTE2, which has potential for biocontrol of Gordonia, Rhodococcus, and Nocardia stabilized foams in activated sludge plants. Appl Environ Microbiol 77:3923–3929PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Petrovski S, Seviour RJ, Tillett D (2011) Prevention of Gordonia and Nocardia stabilized foam formation by using bacteriophage GTE7. Appl Environ Microbiol 77:7864–7867PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Petrovski S, Dyson ZA, Seviour RJ, Tillett D (2012) Small but sufficient: the Rhodococcus phage RRH1 has the smallest known Siphoviridae genome at 14.2 kilobases. J Virol 86:358–363PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Petrovski S, Tillett D, Seviour RJ (2012) Genome sequences and characterization of the related Gordonia phages GTE5 and GRU1 and their use as potential biocontrol agents. Appl Environ Microbiol 78:42–47PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Petrovski S, Seviour RJ, Tillett D (2013) Characterization and whole genome sequences of the Rhodococcus bacteriophages RGL3 and RER2. Arch Virol 158:601–609PubMedCrossRefGoogle Scholar
  27. 27.
    Petrovski S, Seviour RJ, Tillett D (2013) Genome sequence and characterization of a Rhodococcus equi phage REQ1. Virus Genes 46:588–590PubMedCrossRefGoogle Scholar
  28. 28.
    Petrovski S, Seviour RJ, Tillett D (2014) Genome sequence of the Nocardia bacteriophage NBR1. Arch Virol 159:167–173PubMedCrossRefGoogle Scholar
  29. 29.
    Rao VB, Feiss M (2008) The bacteriophage DNA packaging motor. Ann Rev Gene 42:647–681CrossRefGoogle Scholar
  30. 30.
    Ratcliff SW, Luh J, Ganesan AT, Behrens B, Thompson R, Montenegro MA, Morelli G, Trautner TA (1979) The genome of Bacillus subtilis phage SPP1. Mol Gen Genet 168:165–172PubMedCrossRefGoogle Scholar
  31. 31.
    Salifu SP, Valero-Rello A, Campbell SA, Inglis NF, Scortti M, Foley S, Vázquez-Boland JA (2013) Genome and proteome analysis of phage E3 infecting the soil-borne actinomycete Rhodococcus equi. Environ MicrobiolRep 5:170–178Google Scholar
  32. 32.
    Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–W689PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Seviour EM, Williams C, DeGrey B, Soddell JA, Seviour RJ, Lindrea KC (1994) Studies on filamentous bacteria from Australian activated sludge plants. Water Res 28:2335–2342CrossRefGoogle Scholar
  34. 34.
    Seviour EM, Williams CJ, Seviour RJ, Soddell JA, Lindrea KC (1990) A survey of filamentous bacterial populations from foaming activated sludge plants in eastern states of Australia. Water Res 24:493–498CrossRefGoogle Scholar
  35. 35.
    Sharples GJ, Corbett LM, McGlynn P (1999) DNA structure specificity of Rap endonuclease. Nucleic Acids Res 27:4121–4127PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Soddell JA, Seviour RJ (1998) Numerical taxonomy of Skermania piniformis and related isolates from activated sludge. J Appl Microbiol 84:272–284CrossRefGoogle Scholar
  37. 37.
    Thomas JA, Soddell JA, Kurtböke DÍ (2002) Fighting foam with phages. Water Sci Technol 46:511–553PubMedGoogle Scholar
  38. 38.
    Wang IN, Smith DL, Young R (2000) Holins: the protein clocks of bacteriophage infections. Annu Rev Microbiol 54:799–825PubMedCrossRefGoogle Scholar
  39. 39.
    Xu J, Hendrix RW, Duda RL (2004) Conserved translational frameshift in dsDNA bacteriophage tail assembly genes. Mol Cell 16:11–21PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2015

Authors and Affiliations

  • Z. A. Dyson
    • 1
  • J. Tucci
    • 1
  • R. J. Seviour
    • 2
  • S. Petrovski
    • 2
  1. 1.La Trobe Institute of Molecular SciencesBendigoAustralia
  2. 2.Department of Physiology, Anatomy and MicrobiologyLa Trobe UniversityBundooraAustralia

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