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Isolation and complete genome sequence of a bacteriophage lysing Tetrasphaera jenkinsii, a filamentous bacteria responsible for bulking in activated sludge

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Abstract

The Nosticoida limicola filamentous morphotype is held responsible for incidents of bulking and foaming in activated sludge. Members of the actinobacterial N. limicola II have been isolated and grown in pure culture and shown to belong to the genus Tetrasphaera, and play an important role in phosphorus removal. This article describes the isolation and genomic characterization of a phage able to lyse Tetrasphaera jenkinsii, TJE1. This lytic phage is a member of the Caudovirales specific for T. jenkinsii. The complete DNA sequence of TJE1 phage revealed it to have a circularly permuted genome (49,219 bp) with 66 putative open reading frames, a single transcriptional terminator, and 6 pairs of inverted repeats within the genome sequence. The TJE1 phage genome is organised into a modular gene structure, but shares only limited sequence identity with other phages so far described.

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References

  1. P.H. Nielsen, H. Daims, H. Lemmer, FISH Handbook for Biological Wastewater Treatment (IWA Publishing, London, 2009)

    Google Scholar 

  2. F. Rohwer, Global phage diversity. Cell 18, 113–141 (2003)

    Google Scholar 

  3. L.L. Blackall, E.M. Seviour, D. Bradford, S. Rossetti, V. Tandoi, R.J. Seviour, ‘Candidatus Nostocoida limicola’, a filamentous bacterium from activated sludge. Int. J. Syst. Evol. Microbiol. 50, 703–709 (2000)

    Article  PubMed  CAS  Google Scholar 

  4. C.M. McKenzie, E.M. Seviour, P. Schumann, A.M. Maszenan, J.R. Liu, R.I. Webb, P. Monis, C.P. Saint, U. Steiner, R.J. Seviour, Isolation of ‘Candidatus Nostocoida limicola’ Blackall et al. 2000 should be described as three novel species of the genus Tetrasphaera, as Tetrasphaera jenkinsii sp. nov. and Tetrasphaera veronensis sp. nov. Int. J. System. Evol. Microbiol. 56, 2279–2290 (2006)

    Article  CAS  Google Scholar 

  5. Y. Kong, J.L. Nielsen, P.H. Nielsen, Identity and ecophysiology of uncultured actinobacterial polyphosphate-accumulating organisms in full-scale enhanced biological phosphorus removal plants. Appl. Environ. Microbiol. 71, 4076–4085 (2005)

    Article  PubMed  CAS  Google Scholar 

  6. K.D. McMahon, S. He, A. Oehmen, The microbiology of phosphorous removal, in Microbial Ecology of Activated Sludge, ed. by R.J. Seviour, P.H. Nielsen (IWA publishing, London, 2010), pp. 281–320

    Google Scholar 

  7. H.T.T. Nguyen, V.Q. Le, A.A. Hansen, J.L. Nielsen, P.H. Nielsen, High Diversity and abundance of putative polyphosphate- accumulating Tetrasphaera-related bacteria in activated sludge systems. FEMS Microbiol. Ecol. 76, 256–267 (2011)

    Article  PubMed  CAS  Google Scholar 

  8. S. Chibani-Chennoufi, A. Bruttin, M.L. Dillmann, H. Brussow, Phage–host interaction: an ecological perspective. J. Bacteriol. 186, 3677–3678 (2004)

    Article  PubMed  CAS  Google Scholar 

  9. N.H. Mann, The third age of phage. PLoS Biol. 3, e182 (2005)

    Article  PubMed  Google Scholar 

  10. E. Jensen, H. Schrader, B. Rieland, T. Thompson, K. Lee, K. Nickerson, T. Kokjohn, Prevalence of broad-host range lytic bacteriophages of Spherotilus natans, Escherichia coli, and Pseudomonas aeruginosa. Appl. Environ. Microbiol. 64, 575–580 (1998)

    PubMed  CAS  Google Scholar 

  11. S.M. Kotay, T. Datta, J. Choi, R. Goel, Biocontrol of biomass bulking caused by Haliscomenobacter hydrossis using a newly isolated lytic bacteriophage. Water Res. 45, 694–704 (2011)

    Article  PubMed  CAS  Google Scholar 

  12. S. Petrovski, R.J. Seviour, D. Tillett, Genome sequence and characterization of the Tsukamurella bacteriophage TPA2. Appl. Environ. Microbiol. 77, 1389–1398 (2011)

    Article  PubMed  CAS  Google Scholar 

  13. A.J. Drummond, B. Ashton, M. Cheung, J. Heled, M. Kearse, R. Moir, S. Stones-Havas, T. Thierer, A. Wilson, Geneious v5.1. http://www.geneious.com (2010)

  14. S.F. Altschul, W. Gish, W. Miller, E.W. Myers, D.J. Lipman, Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990)

    PubMed  CAS  Google Scholar 

  15. D. Laslett, B. Canback, ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucl. Acids Res. 32, 11–16 (2004)

    Article  PubMed  CAS  Google Scholar 

  16. E.A. Lesnik, R. Sampath, H.B. Levene, T.J. Henderson, J.A. McNiel, D.J. Ecker, Prediction of rho-independent transcriptional terminators in Escherichia coli. Nucl. Acids Res. 29, 3583–3594 (2007)

    Article  Google Scholar 

  17. S. Petrovski, D. Tillett, R.J. Seviour, Genome sequence and characterization of the related Gordonia phages GTE5 and GRU1 and their use as biocontrol agents. Appl. Environ. Microbiol. 78, 42–47 (2012)

    Article  PubMed  CAS  Google Scholar 

  18. S. Petrovski, R.J. Seviour, D. Tillett, 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. App. Environ. Microbiol. 77, 3923–3929 (2011)

    Article  CAS  Google Scholar 

  19. H. Brüssow, F. Desiere, Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. Mol. Microbiol. 39, 213–223 (2001)

    Article  PubMed  Google Scholar 

  20. M. Borriss, T. Lombardot, F.O. Glöckner, D. Becher, D. Albretcht, T. Schweder, Genome and proteome characterization of psychrophilic Flavobacterium bacteriophage 11b. Extremophiles 11, 95–104 (2007)

    Article  PubMed  CAS  Google Scholar 

  21. F.N. Enikeeva, K.V. Severinov, M.S. Gelfand, Restriction-modification systems and bacteriophage invasion: who wins? J. Theor. Biol. 266, 550–559 (2010)

    Article  PubMed  CAS  Google Scholar 

  22. C. Yang, U. Curth, C. Urbanke, C. Kang, Crystal structure of human mitochondrial single-stranded DNA binding protein at 2.4 Å resolution. Nat. Struct. Biol. 4, 153–157 (1997)

    Article  PubMed  CAS  Google Scholar 

  23. M.S. Lee, K.J. Marians, Escherichia coli replication factor Y, a component of the primosome, can act as a DNA helicase. Proc. Natl. Acad. Sci. USA 84, 8345–8349 (1987)

    Article  PubMed  CAS  Google Scholar 

  24. E.V. Koonin, K.E. Rudd, A conserved domain in putative bacterial and bacteriophage transglycosylases. Trends Biochem. Sci. 19, 106–107 (1994)

    Article  PubMed  CAS  Google Scholar 

  25. D. Kapitaniov, R.K. Yu, Conserved domains of glycosyltransferases. Glycobiology 9, 961–978 (1999)

    Article  Google Scholar 

  26. J. Fricke, J. Neuhard, R.A. Kelln, S. Pedersen, The cmk gene encoding cytidine monophosphate kinase is located in the rpsa operon and is required for normal replication rate in Escherichia coli. J. Bacteriol. 177, 517–523 (1995)

    PubMed  CAS  Google Scholar 

  27. J.B. Thoden, A.D. Hedeman, G. Wesenberg, M.C. Chapeau, P.A. Frey, H.M. Holden, Structural analysis of UDP-sugar binding to UDP-galactose 4-epimerase from Escherichia coli. Biochemistry 36, 6294–6304 (1997)

    Article  PubMed  CAS  Google Scholar 

  28. N. Kikuchi, H. Narimatsu, Bioinformatics for comprehensive finding and analysis of glycosyltransferases. Biochem. Biophys. Acta. 1760, 578–583 (2006)

    Article  PubMed  CAS  Google Scholar 

  29. R. Ghai, A.B. Martin-Cuadrado, A.G. Molto, I.G. Heredia, R. Cabrera, J. Martin, M. Verdú, P. Deschamps, D. Moreira, P. López-García, A. Mira, F. Rodriguez-Valera, Metagenome of the Mediterranean deep chlorophyll maximum studied by direct and fosmid library 454 pyrosequencing. ISME J. 4, 1154–1166 (2010)

    Article  PubMed  CAS  Google Scholar 

  30. G.L. Newton, P. Ta, K.P. Bzymek, R.C. Fahey, Biochemistry of the initial steps of mycothiol biosynthesis. J. Biol. Chem. 281, 33910–33920 (2006)

    Article  PubMed  CAS  Google Scholar 

  31. C.E. Catalano, The terminase enzyme from bacteriophage lambda: a DNA-packaging machine. Cell. Mol. Life Sci. 57, 128–148 (2000)

    Article  PubMed  CAS  Google Scholar 

  32. G.F. Hatfull, D. Jacobs-Sera, J.G. Lawrence, W.H. Pope, D.A. Russell, C.C. Ko, R.J. Weber, M.C. Patel, K.L. Germane, R.H. Edgar, N.N. Hoyle, C.A. Bowman, A.T. Tantoco, E.C. Paladin, M.S. Myers, A.L. Smith, M.S. Grace, T.T. Pham, M.B. O’Brien, A.M. Vogelsberger, A.J. Hryckowian, J.L. Wynalek, H. Donis-Keller, M.W. Bogel, C.L. Peebles, S.G. Cresawn, R.W. Hendrix, Comparative genomic analysis of 60 mycobacteriophage geneomes: genome clustering, gene acquisition and gene size. J. Mol. Biol. 397, 119–143 (2010)

    Article  PubMed  CAS  Google Scholar 

  33. P.B. Perler, Protein splicing of inteins and hedgehog autoproteolysis: structure, function and evolution. Cell 92, 1–4 (1998)

    Article  PubMed  CAS  Google Scholar 

  34. S. Elleuche, S. Pöggeler, Inteins, valuable genetic elements in molecular biology and biotechnology. Appl. Microbiol. Biotechnol. 87, 479–489 (2010)

    Article  PubMed  CAS  Google Scholar 

  35. C.L. Chen, T.Y. Pan, S.C. Kan, Y.C. Kuan, L.Y. Hong, K.R. Chiu, K.S. Sheu, J.S. Yang, W.H. Hsu, H.Y. Hu, Genome sequence of the lytic bacteriophage P1201 from Corynebacterium glutamicum NCHU 87078: evolutionary relationships to phages from Corynebacterineae. Virology 378, 226–232 (2008)

    Article  PubMed  CAS  Google Scholar 

  36. G.J. Morgan, G.F. Hatfull, S. Casjens, R.W. Hendrix, Bacteriophage Mu genome sequence: analysis and comparison with Mu-like pathogens in Haemophilus, Neisseria and Deinococcus. J. Mol. Biol. 317, 337–359 (2002)

    Article  PubMed  CAS  Google Scholar 

  37. N.M. Luscombe, S.E. Austin, H.M. Berman, J.M. Thornton, An overview of the structures of protein–DNA complexes. Genome Biol. 1:REVIEWS001 (2000)

  38. A. Daniel, P.E. Bonnen, V.A. Fischetti, First complete genome sequence of two Staphylococcus epidermidis bacteriophages. J. Bacteriol. 189, 2086–2100 (2007)

    Article  PubMed  CAS  Google Scholar 

  39. M. Sharma, R.L. Ellis, D.M. Hinton, Identification of a family of bacteriophage T4 genes encoding proteins similar to those present in group I introns of fungi and phage. Proc. Natl. Acad. Sci. USA 89, 6658–6662 (1992)

    Article  PubMed  CAS  Google Scholar 

  40. L.M. Iyer, E.V. Koonin, L. Aravind, Classification and evolutionary history of the single-strand annealing proteins, RecT, Redbeta, ERF and RAD52. BMC Genomics 3, 8 (2002)

    Article  PubMed  Google Scholar 

  41. T.S. Vellani, R.S. Myers, Bacteriophage SPP1 Chu is an alkaline exonuclease in the SynExo family of viral two-component recombinases. J. Bacteriol. 185, 2465–2474 (2003)

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The research was supported by the Australian Research Council Linkage Grant (LP0774913) together with Melbourne Water and South East Water who are thanked for their financial support. S. Petrovski was funded by the ARC Linkage and La Trobe University grants.

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Author notes

  1. Robert J. Seviour

    Present address: Department of Microbiology, La Trobe University, Bundoora, VIC, 3086, Australia

  2. Steve Petrovski

    Present address: Department of Pathology, Peter MacCallum Cancer Centre, Melbourne, VIC, Australia

Authors and Affiliations

  1. La Trobe Institute for Molecular Sciences, La Trobe University, Bendigo, VIC, Australia

    Steve Petrovski, Daniel Tillett & Robert J. Seviour

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  1. Steve Petrovski
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Correspondence to Steve Petrovski.

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Petrovski, S., Tillett, D. & Seviour, R.J. Isolation and complete genome sequence of a bacteriophage lysing Tetrasphaera jenkinsii, a filamentous bacteria responsible for bulking in activated sludge. Virus Genes 45, 380–388 (2012). https://doi.org/10.1007/s11262-012-0771-4

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