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Abstract

A mycoplasma isolated from the liver of a dead Humboldt penguin (Spheniscus humboldti) and designated strain 56A97, was investigated to determine its taxonomic status. Complete 16S rRNA gene sequence analysis indicated that the organism was most closely related to Mycoplasma gallisepticum and Mycoplasma imitans (99.7 and 99.9 % similarity, respectively). The average DNA–DNA hybridization values between strain 56A97 and M. gallisepticum and M. imitans were 39.5 and 30 %, respectively and the Genome to Genome Distance Calculator gave results of 29.10 and 23.50 %, respectively. The 16S–23S rRNA intergenic spacer was 72–73 % similar to M. gallisepticum strains and 52.2 % to M. imitans . A partial sequence of rpoB was 91.1–92 % similar to M. gallisepticum strains and 84.7 % to M. imitans . Colonies possessed a typical fried-egg appearance and electron micrographs revealed the lack of a cell wall and a nearly spherical morphology, with an electron-dense tip-like structure on some flask-shaped cells. The isolate required sterol for growth, fermented glucose, adsorbed and haemolysed erythrocytes, but did not hydrolyse arginine or urea. The strain was compared serologically against 110 previously described Mycoplasma reference strains, showing that, except for M. gallisepticum , strain 56A97 is not related to any of the previously described species, although weak cross-reactions were evident. Genomic information, serological reactions and phenotypic properties demonstrate that this organism represents a novel species of the genus Mycoplasma , for which the name Mycoplasma tullyi sp. nov. is proposed; the type strain is 56A97 (ATCC BAA-1432, DSM 21909, NCTC 11747).

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2017-09-12
2019-10-23
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References

  1. Brown DR, May M, Bradbury JM, Balish MF, Calcutt MJ et al. Genus I. Mycoplasma. In Krieg NR, Staley JT, Brown DB, Hedlund BP, Paster BJ et al. (editors) Bergey's Manual of Systematic Bacteriology New York: Springer; 2010; pp. 575– 613
    [Google Scholar]
  2. Frasca S, Weber ES, Urquhart H, Liao X, Gladd M et al. Isolation and characterization of Mycoplasma sphenisci sp. nov. from the choana of an aquarium-reared jackass penguin (Spheniscus demersus). J Clin Microbiol 2005; 43: 2976– 2979 [CrossRef] [PubMed]
    [Google Scholar]
  3. Barreto M, Pires J, Lemos M, Silva M, Ogino L et al. Mycoplasma gallisepticum by PCR in glucose fermenting mycoplasma isolates from Magellanic penguins (Spheniscus magellanicus) in Brazil. In Proceedings of the Sixty-Second Western Poultry Disease Conference: Western Poultry Disease Conference 2013; pp. 73– 75
    [Google Scholar]
  4. Dewar ML, Arnould JP, Dann P, Trathan P, Groscolas R et al. Interspecific variations in the gastrointestinal microbiota in penguins. Microbiologyopen 2013; 2: 195– 204 [CrossRef] [PubMed]
    [Google Scholar]
  5. Brown DR, Whitcomb RF, Bradbury JM. Revised minimal standards for description of new species of the class Mollicutes (division Tenericutes). Int J Syst Evol Microbiol 2007; 57: 2703– 2719 [CrossRef] [PubMed]
    [Google Scholar]
  6. ICSB Subcommittee on the taxonomy of Mollicutes Revised minimum standards for description of new species of the class Mollicutes (division Tenericutes). Int J Syst Bacteriol 1995; 45: 605– 612 [Crossref]
    [Google Scholar]
  7. Bradbury JM, Abdul-Wahab OMS, Yavari CA, Dupiellet J-P, Bove JM. Mycoplasma imitans sp. nov. is related to Mycoplasma gallisepticum and found in birds. Int J Syst Bacteriol 1993; 43: 721– 728 [CrossRef]
    [Google Scholar]
  8. Dupeillet JP. Mycoplasmes De l’oie et du canard: contribution a l’etude serologique et moléculaire de souches apparentées à Mycoplasma gallisepticum. In PhD Thesis France: Universite De Bordeaux II: Villenave d’Ornon; 1988
    [Google Scholar]
  9. Dupiellet JP, Vuillaume A, Rousselot D, Bové JM, Bradbury JM. Serological and molecular studies on Mycoplasma gallisepticum strains. Zentralbl. Bakteriol Suppl 1990; 20: 859– 864
    [Google Scholar]
  10. Boyle JS. Phylogeny and diagnosis of several avian mycoplasma species. B. Sc. Thesis, Melbourne University, Australia 1993
  11. Nicholas RAJ, Ayling RD, Heldtander M, Johansson KE, Yavari CA et al. A mycoplasma resembling M. gallisepticum isolated from Humboldt penguins. In Abstracts of the 12th Congress of the International Organization for Mycoplasmology International Organization for Mycoplasmology; 1998; pp. 178
    [Google Scholar]
  12. Tully JG. Cloning and filtration techniques for mycoplasmas. In Razin S, Tully JG. (editors) Methods in Mycoplasmology New York: Academic Press; 1983; pp. 173– 177 [Crossref]
    [Google Scholar]
  13. Bradbury JM. Rapid biochemical tests for characterization of the Mycoplasmatales. J Clin Microbiol 1977; 5: 531– 534 [PubMed]
    [Google Scholar]
  14. Pitcher DG, Windsor D, Windsor H, Bradbury JM, Yavari C et al. Mycoplasma amphoriforme sp. nov., isolated from a patient with chronic bronchopneumonia. Int J Syst Evol Microbiol 2005; 55: 2589– 2594 [CrossRef] [PubMed]
    [Google Scholar]
  15. Harasawa R, Pitcher DG, Ramírez AS, Bradbury JM. A putative transposase gene in the 16S-23S rRNA intergenic spacer region of Mycoplasma imitans. Microbiology 2004; 150: 1023– 1029 [CrossRef] [PubMed]
    [Google Scholar]
  16. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215: 403– 410 [CrossRef] [PubMed]
    [Google Scholar]
  17. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22: 4673– 4680 [CrossRef] [PubMed]
    [Google Scholar]
  18. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999; 41: 95– 98
    [Google Scholar]
  19. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4: 406– 425 [PubMed]
    [Google Scholar]
  20. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007; 24: 1596– 1599 [CrossRef] [PubMed]
    [Google Scholar]
  21. Heldtander M, Pettersson B, Tully JG, Johansson KE. Sequences of the 16S rRNA genes and phylogeny of the goat mycoplasmas Mycoplasma adleri, Mycoplasma auris, Mycoplasma cottewii and Mycoplasma yeatsii. Int J Syst Bacteriol 1998; 48: 263– 268 [CrossRef] [PubMed]
    [Google Scholar]
  22. Fox GE, Wisotzkey JD, Jurtshuk P. How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Bacteriol 1992; 42: 166– 170 [CrossRef] [PubMed]
    [Google Scholar]
  23. Cole RM. Transmission electron microscopy: basic techniques. In Razin S, Tully JG. (editors) Methods in Mycoplasmology New York: Academic Press; 1983; pp. 43– 50 [Crossref]
    [Google Scholar]
  24. Razin S, Tully JG. Cholesterol requirement of mycoplasmas. J Bacteriol 1970; 102: 306– 310 [PubMed]
    [Google Scholar]
  25. Poveda JB. Biochemical characteristics in mycoplasma identification. In Miles R, Nicholas RAJ. (editors) Methods in Molecular Biology: Vol. 104. Mycoplasma Protocolsvol. 1998 Totowa, NJ: Humana Press; 1998; pp. 69– 78 [Crossref]
    [Google Scholar]
  26. Shepard MC, Howard DR. Identification of "T" mycoplasmas in primary agar cultures by means of a direct test for urease. Ann N Y Acad Sci 1970; 174: 809– 819 [CrossRef] [PubMed]
    [Google Scholar]
  27. Livingston CW. Isolation of T-strain of mycoplasma from Texas feedlot cattle. Am J Vet Res 1972; 33: 1925– 1929 [PubMed]
    [Google Scholar]
  28. Gardella RS, Haemagglutination D. haemadsorption and haemolysis. In Razin S, Tully JG. (editors) Methods in Mycoplasmology New York: Academic Press; 1983; pp. 379– 384 [Crossref]
    [Google Scholar]
  29. Bradbury JM, Forrest M, Williams A, Lipofaciens M. A new species of avian origin. Int J Syst Bacteriol 1983; 33: 329– 335 [Crossref]
    [Google Scholar]
  30. Bradbury JM, Jordan FT. The absorption of -globulins to Mycoplasma gallisepticum and the possible role in non-specific serological reactions. Vet Rec 1971; 89: 318 [CrossRef] [PubMed]
    [Google Scholar]
  31. Forrest M. Characterisation of three new species of avian Mycoplasma. PhD Thesis, University of Liverpool, UK 1982
  32. Rosendal S, Black FT. Direct and indirect immunofluorescence of unfixed and fixed Mycoplasma colonies. Acta Pathol Microbiol Scand Sect. B 1972; 80: 615– 622
    [Google Scholar]
  33. Clyde WA, Tests GI. Tests Ginhibition. In razin S, Tully JG. (editors) Methods in Mycoplasmology New York: Academic Press; 1983; pp. 405– 410 [Crossref]
    [Google Scholar]
  34. Stojiljkovic I, Evavold BD, Kumar V. Antimicrobial properties of porphyrins. Expert Opin Investig Drugs 2001; 10: 309– 320 [CrossRef] [PubMed]
    [Google Scholar]
  35. Taylor-Robinson D. Metabolism inhibition tests. In Razin S, Tully JG. (editors) Methods in Mycoplasmology. New York: Academic Pressvol. vol. 1983 1983; pp. 411– 417 [Crossref]
    [Google Scholar]
  36. Sachse K, Hotzel H. Classification of isolates by DNA–DNA hybridisation. In Miles R. (editor) Methods in Molecular Biology: Vol. 104. Mycoplasma Protocols Totowa, NJ: Humana Press; 1998; pp. 189– 195 [Crossref]
    [Google Scholar]
  37. Stackebrandt E, Goebel BM. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the Present Species Definition in Bacteriology. Int J Syst Evol Microbiol 1994; 44: 846– 849 [CrossRef]
    [Google Scholar]
  38. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 2006; 33: 152– 155
    [Google Scholar]
  39. Papazisi L, Gorton TS, Kutish G, Markham PF, Browning GF et al. The complete genome sequence of the avian pathogen Mycoplasma gallisepticum strain rlow. Microbiology 2003; 149: 2307– 2316 [CrossRef] [PubMed]
    [Google Scholar]
  40. Auch AF, von Jan M, Klenk HP, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2010; 2: 117– 134 [CrossRef] [PubMed]
    [Google Scholar]
  41. Johnson JL. Nucleic acids in bacterial classification. In Krieg NR, Holt JH. (editors) Bergey’s Manual of Systematic Bacteriologyvol. 1984 Baltimore: William & Wilkins Co; 1984; pp. 8– 11
    [Google Scholar]
  42. Stackebrandt E, Frederiksen W, Garrity GM, Grimont PA, Kämpfer P et al. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 2002; 52: 1043– 1047 [CrossRef] [PubMed]
    [Google Scholar]
  43. Kim KS, Ko KS, Chang MW, Hahn TW, Hong SK et al. Use of rpoB sequences for phylogenetic study of Mycoplasma species. FEMS Microbiol Lett 2003; 226: 299– 305 [CrossRef] [PubMed]
    [Google Scholar]
  44. Ko KS, Lee HK, Park MY, Lee KH, Yun YJ et al. Application of RNA polymerase beta-subunit gene (rpoB) sequences for the molecular differentiation of Legionella species. J Clin Microbiol 2002; 40: 2653– 2658 [PubMed] [Crossref]
    [Google Scholar]
  45. Schwarz R, Dayhoff MO. Matrices for detecting distant relationships. In Dayhoff MO. (editor) Atlas of Protein Sequences. Washington: National Biomedical Research Foundationvol. 1979 1979; pp. 353– 358
    [Google Scholar]
  46. Ramírez AS, Naylor CJ, Pitcher DG, Bradbury JM. High inter-species and low intra-species variation in 16S-23S rDNA spacer sequences of pathogenic avian mycoplasmas offers potential use as a diagnostic tool. Vet Microbiol 2008; 128: 279– 287 [CrossRef] [PubMed]
    [Google Scholar]
  47. Volokhov DV, George J, Liu SX, Ikonomi P, Anderson C et al. Sequencing of the intergenic 16S-23S rRNA spacer (ITS) region of Mollicutes species and their identification using microarray-based assay and DNA sequencing. Appl Microbiol Biotechnol 2006; 71: 680– 698 [CrossRef] [PubMed]
    [Google Scholar]
  48. Yavari CA.. Studies on a mycoplasma gallisepticum-like organism isolated from the humboldt penguin (Spheniscus humboldti). PhD Thesis, University of Liverpool, UK 2010
  49. Kempf I. DNA amplification methods for diagnosis and epidemiological investigations of avian mycoplasmosis. Avian Pathol 1998; 27: 7– 14 [CrossRef] [PubMed]
    [Google Scholar]
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