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Abstract

Polyphasic taxonomic analysis was performed on a clinical isolate (NML 06-3099) from a cystic fibrosis patient, including whole-genome sequencing, proteomics, phenotypic testing, electron microscopy, chemotaxonomy and a clinical investigation. Comparative whole-genome sequence analysis and multilocus sequence analysis (MLSA) between ATCC 33301 and clinical isolate NML 06-3099 suggested that the clinical isolate was closely related to, but distinct from, the species . By 16S rRNA gene sequencing, the clinical isolate shared 98.7 % sequence identity with ATCC 33301. A concatenate of six MLSA loci (totalling 4500 bp) revealed < 93.9 % identity between ATCC 33301, other members of the genus and the clinical isolate. A whole-genome sequence comparison between NML 06-3099 and ATCC 33301 determined that the average nucleotide identity was 76.24 %. The overall DNA G+C content of NML 06-3099 was 51.27 %, consistent with members of the genus . By matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) MS analysis, NML 06-3099 had a genus-level match, but not a species-level match, to . By shotgun proteomics, ATCC 33301 and NML 06-3099 were found to have unique proteomes. The two strains had similar morphologies and multiple fimbriae, as observed by transmission electron microscopy, but were distinguishable by phenotypic testing. Cellular fatty acids found were typical for members of the . NML 06-3099 was susceptible to commonly used antibiotics. Based on these data, NML 06-3099 represents a novel species in the genus , for which the name sp. nov. is proposed (type strain NML 06-3099 = CCUG 55408 = DSM 19846).

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2015-06-01
2024-04-18
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References

  1. Abbott S. ( 2011;). Klebsiella Enterobacter Citrobacter Serratia Plesiomonas, and other Enterobacteriaceae . . In Manual of Clinical Microbiology, pp. 639657. Edited by Versalovic J., Carroll K. C., Funke G., Jorgensen J. H., Landry M. L., Warnock D. W. , 10th edn.., Washington, DC: American Society for Microbiology;.
    [Google Scholar]
  2. Berkta M., Uzun H., Bozkurt M., Kurto H., Guducuo H., Ayd S. ( 2001;). Pulmonary infection of Tatumella ptyseos developed on the background of pulmonary tuberculosis. East J Med 6 3334.
    [Google Scholar]
  3. Bernard K.A., Bellefeuille M., Ewan E.P. ( 1991;). Cellular fatty acid composition as an adjunct to the identification of asporogenous, aerobic gram-positive rods. J Clin Microbiol 29 8389 [PubMed].
    [Google Scholar]
  4. Brady C., Cleenwerck I., Venter S., Vancanneyt M., Swings J., Coutinho T. ( 2008;). Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst Appl Microbiol 31 447460 10.1016/j.syapm.2008.09.004 [PubMed]. [CrossRef]
    [Google Scholar]
  5. Brady C.L., Venter S.N., Cleenwerck I., Vandemeulebroecke K., De Vos P., Coutinho T.A. ( 2010;). Transfer of Pantoea citrea Pantoea punctata Pantoea terrea to the genus Tatumella emend. as Tatumella citrea comb. nov., Tatumella punctata comb. nov. and Tatumella terrea comb. nov. and description of Tatumella morbirosei sp. nov. Int J Syst Evol Microbiol 60 484494 10.1099/ijs.0.012070-0 [PubMed]. [CrossRef]
    [Google Scholar]
  6. Brousseau R., Hill J.E., Préfontaine G., Goh S.H., Harel J., Hemmingsen S.M. ( 2001;). Streptococcus suis serotypes characterized by analysis of chaperonin 60 gene sequences. Appl Environ Microbiol 67 48284833 10.1128/AEM.67.10.4828-4833.2001 [PubMed]. [CrossRef]
    [Google Scholar]
  7. Christensen J.J., Dargis R., Hammer M., Justesen U.S., Nielsen X.C., Kemp M., Danish MALDI-TOF MS Study Group. ( 2012;). Matrix-assisted laser desorption ionization-time of flight mass spectrometry analysis of Gram-positive, catalase-negative cocci not belonging to the Streptococcus or Enterococcus genus and benefits of database extension. J Clin Microbiol 50 17871791 10.1128/JCM.06339-11 [PubMed]. [CrossRef]
    [Google Scholar]
  8. CLSI ( 2012). Performance standards for antimicrobial susceptibility testing; 21st edn, 22nd informational supplement vol. 32., no. 1. M100-S22. Wayne, PA: Clinical Laboratory Standards Institute;.
    [Google Scholar]
  9. Costa P.S., Mendes J.M., Ribeiro G.M. ( 2008;). Tatumella ptyseos causing severe human infection: report of the first two Brazilian cases. Braz J Infect Dis 12 442443 10.1590/S1413-86702008000500017 [PubMed].
    [Google Scholar]
  10. Doern C.D. ( 2013;). Charting uncharted territory: a review of the verification and implementation process for matrix-assisted laser desorption ionization–time of flight mass spectrometry (MALDI-TOF MS) for organism identification. Clin Microbiol Newsl 35 6978 10.1016/j.clinmicnews.2013.04.001. [CrossRef]
    [Google Scholar]
  11. Drancourt M., Bollet C., Carta A., Rousselier P. ( 2001;). Phylogenetic analyses of Klebsiella species delineate Klebsiella Raoultella gen. nov., with description of Raoultella ornithinolytica comb. nov., Raoultella terrigena comb. nov. and Raoultella planticola comb. nov. Int J Syst Evol Microbiol 51 925932 10.1099/00207713-51-3-925 [PubMed]. [CrossRef]
    [Google Scholar]
  12. Dworzanski J.P., Snyder A.P. ( 2005;). Classification and identification of bacteria using mass spectrometry-based proteomics. Expert Rev Proteomics 2 863878 10.1586/14789450.2.6.863 [PubMed]. [CrossRef]
    [Google Scholar]
  13. Dworzanski J.P., Snyder A.P., Chen R., Zhang H., Wishart D., Li L. ( 2004;). Identification of bacteria using tandem mass spectrometry combined with a proteome database and statistical scoring. Anal Chem 76 23552366 10.1021/ac0349781 [PubMed]. [CrossRef]
    [Google Scholar]
  14. Dworzanski J.P., Deshpande S.V., Chen R., Jabbour R.E., Snyder A.P., Wick C.H., Li L. ( 2006;). Mass spectrometry-based proteomics combined with bioinformatic tools for bacterial classification. J Proteome Res 5 7687 10.1021/pr050294t [PubMed]. [CrossRef]
    [Google Scholar]
  15. Edwards U., Rogall T., Blöcker H., Emde M., Böttger E.C. ( 1989;). Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17 78437853 10.1093/nar/17.19.7843 [PubMed]. [CrossRef]
    [Google Scholar]
  16. Egelman E.H. ( 2000;). A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy 85 225234 10.1016/S0304-3991(00)00062-0 [PubMed]. [CrossRef]
    [Google Scholar]
  17. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., Leith A. ( 1996;). spider web: processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116 190199 10.1006/jsbi.1996.0030 [PubMed]. [CrossRef]
    [Google Scholar]
  18. Garcia-Armisen T., Papalexandratou Z., Hendryckx H., Camu N., Vrancken G., De Vuyst L., Cornelis P. ( 2010;). Diversity of the total bacterial community associated with Ghanaian and Brazilian cocoa bean fermentation samples as revealed by a 16S rRNA gene clone library. Appl Microbiol Biotechnol 87 22812292 10.1007/s00253-010-2698-9 [PubMed]. [CrossRef]
    [Google Scholar]
  19. Garver K.A., Dwilow A.G., Richard J., Booth T.F., Beniac D.R., Souter B.W. ( 2007;). First detection and confirmation of spring viraemia of carp virus in common carp, Cyprinus carpio L., from Hamilton Harbour, Lake Ontario, Canada. J Fish Dis 30 665671 10.1111/j.1365-2761.2007.00851.x [PubMed]. [CrossRef]
    [Google Scholar]
  20. Goris J., Konstantinidis K.T., Klappenbach J.A., Coenye T., Vandamme P., Tiedje J.M. ( 2007;). DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57 8191 10.1099/ijs.0.64483-0 [PubMed]. [CrossRef]
    [Google Scholar]
  21. Hill J.E., Penny S.L., Crowell K.G., Goh S.H., Hemmingsen S.M. ( 2004;). cpnDB: a chaperonin sequence database. Genome Res 14 16691675 10.1101/gr.2649204 [PubMed]. [CrossRef]
    [Google Scholar]
  22. Hollis D.G., Hickman F.W., Fanning G.R., Farmer J.J. III, Weaver R.E., Brenner D.J. ( 1981;). Tatumella ptyseos gen. nov., sp. nov., a member of the family Enterobacteriaceae found in clinical specimens. J Clin Microbiol 14 7988 [PubMed].
    [Google Scholar]
  23. Kämpfer P. ( 2012;). Systematics of prokaryotes: the state of the art. Antonie van Leeuwenhoek 101 311 10.1007/s10482-011-9660-4 [PubMed]. [CrossRef]
    [Google Scholar]
  24. Ken C.F., Lee C.C., Duan K.J., Lin C.T. ( 2005;). Unusual stability of manganese superoxide dismutase from a new species, Tatumella ptyseos ct: its gene structure, expression, and enzyme properties. Protein Expr Purif 40 4250 10.1016/j.pep.2004.10.003 [PubMed]. [CrossRef]
    [Google Scholar]
  25. Khamis A., Colson P., Raoult D., Scola B.L. ( 2003;). Usefulness of rpoB gene sequencing for identification of Afipia Bosea species, including a strategy for choosing discriminative partial sequences. Appl Environ Microbiol 69 67406749 10.1128/AEM.69.11.6740-6749.2003 [PubMed]. [CrossRef]
    [Google Scholar]
  26. Konstantinidis K.T., Tiedje J.M. ( 2007;). Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 10 504509 10.1016/j.mib.2007.08.006 [PubMed]. [CrossRef]
    [Google Scholar]
  27. Kuhnert P., Korczak B.M. ( 2006;). Prediction of whole-genome DNA–DNA similarity, determination of G+C content and phylogenetic analysis within the family Pasteurellaceae by multilocus sequence analysis (MLSA). Microbiology 152 25372548 10.1099/mic.0.28991-0 [PubMed]. [CrossRef]
    [Google Scholar]
  28. Ludtke S.J., Baldwin P.R., Chiu W. ( 1999;). eman: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128 8297 10.1006/jsbi.1999.4174 [PubMed]. [CrossRef]
    [Google Scholar]
  29. Marín-Cevada V., Caballero-Mellado J., Bustillos-Cristales R., Muñoz-Rojas J., Mascarúa-Esparza M.A., Castenéda-Lucio M., López-Reyes L., Martínez-Aguilar L., Fuentes-Ramírez L.E. ( 2010;). Tatumella ptyseos, an unrevealed causative agent of pink disease in pineapple. J Phytopathol 158 9399 10.1111/j.1439-0434.2009.01575.x. [CrossRef]
    [Google Scholar]
  30. Martens M., Delaere M., Coopman R., De Vos P., Gillis M., Willems A. ( 2007;). Multilocus sequence analysis of Ensifer and related taxa. Int J Syst Evol Microbiol 57 489503 10.1099/ijs.0.64344-0 [PubMed]. [CrossRef]
    [Google Scholar]
  31. McFadden J.F. ( 2000). Biochemical Tests for Identification of Medical Bacteria , 3rd edn.., Philadelphia: Lippincott Williams & Wilkins;.
    [Google Scholar]
  32. Papalexandratou Z., Falony G., Romanens E., Jimenez J.C., Amores F., Daniel H.M., De Vuyst L. ( 2011a;). Species diversity, community dynamics, and metabolite kinetics of the microbiota associated with traditional Ecuadorian spontaneous cocoa bean fermentations. Appl Environ Microbiol 77 76987714 10.1128/AEM.05523-11 [PubMed]. [CrossRef]
    [Google Scholar]
  33. Papalexandratou Z., Vrancken G., De Bruyne K., Vandamme P., De Vuyst L. ( 2011b;). Spontaneous organic cocoa bean box fermentations in Brazil are characterized by a restricted species diversity of lactic acid bacteria and acetic acid bacteria. Food Microbiol 28 13261338 10.1016/j.fm.2011.06.003 [PubMed]. [CrossRef]
    [Google Scholar]
  34. Papalexandratou Z., Lefeber T., Bahrim B., Lee O.S., Daniel H.M., De Vuyst L. ( 2013;). Hanseniaspora opuntiae Saccharomyces cerevisiae Lactobacillus fermentum, and Acetobacter pasteurianus predominate during well-performed Malaysian cocoa bean box fermentations, underlining the importance of these microbial species for a successful cocoa bean fermentation process. Food Microbiol 35 7385 10.1016/j.fm.2013.02.015 [PubMed]. [CrossRef]
    [Google Scholar]
  35. Paradis S., Boissinot M., Paquette N., Bélanger S.D., Martel E.A., Boudreau D.K., Picard F.J., Ouellette M., Roy P.H., Bergeron M.G. ( 2005;). Phylogeny of the Enterobacteriaceae based on genes encoding elongation factor Tu and F-ATPase β-subunit. Int J Syst Evol Microbiol 55 20132025 10.1099/ijs.0.63539-0 [PubMed]. [CrossRef]
    [Google Scholar]
  36. Pomfret A.J., Rice W.J., Stokes D.L. ( 2007;). Application of the iterative helical real-space reconstruction method to large membranous tubular crystals of P-type ATPases. J Struct Biol 157 106116 10.1016/j.jsb.2006.05.012 [PubMed]. [CrossRef]
    [Google Scholar]
  37. Richter M., Rosselló-Móra R. ( 2009;). Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106 1912619131 10.1073/pnas.0906412106 [PubMed]. [CrossRef]
    [Google Scholar]
  38. Sauer S., Kliem M. ( 2010;). Mass spectrometry tools for the classification and identification of bacteria. Nat Rev Microbiol 8 7482 10.1038/nrmicro2243 [PubMed]. [CrossRef]
    [Google Scholar]
  39. Sibley C.D., Rabin H., Surette M.G. ( 2006;). Cystic fibrosis: a polymicrobial infectious disease. Future Microbiol 1 5361 10.2217/17460913.1.1.53 [PubMed]. [CrossRef]
    [Google Scholar]
  40. Sogawa K., Watanabe M., Sato K., Segawa S., Miyabe A., Murata S., Saito T., Nomura F. ( 2012;). Rapid identification of microorganisms by mass spectrometry: improved performance by incorporation of in-house spectral data into a commercial database. Anal Bioanal Chem 403 18111822 10.1007/s00216-011-5656-1 [PubMed]. [CrossRef]
    [Google Scholar]
  41. Spröer C., Mendrock U., Swiderski J., Lang E., Stackebrandt E. ( 1999;). The phylogenetic position of Serratia Buttiauxella and some other genera of the family Enterobacteriaceae . Int J Syst Bacteriol 49 14331438 10.1099/00207713-49-4-1433 [PubMed]. [CrossRef]
    [Google Scholar]
  42. Stackebrandt E., Ebers J. ( 2006;). Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33 152155.
    [Google Scholar]
  43. Sutcliffe I.C., Trujillo M.E., Goodfellow M. ( 2012;). A call to arms for systematists: revitalising the purpose and practises underpinning the description of novel microbial taxa. Antonie van Leeuwenhoek 101 1320 10.1007/s10482-011-9664-0 [PubMed]. [CrossRef]
    [Google Scholar]
  44. Tan S.C., Wong Y.H., Jegathesan M., Chang S.M. ( 1989;). The first isolate of Tatumella ptyseos in Malaysia. Malays J Pathol 11 2527 [PubMed].
    [Google Scholar]
  45. Tindall B.J., Rosselló-Móra R., Busse H.J., Ludwig W., Kämpfer P. ( 2010;). Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60 249266 10.1099/ijs.0.016949-0 [PubMed]. [CrossRef]
    [Google Scholar]
  46. Tracz D.M., McCorrister S.J., Chong P.M., Lee D.M., Corbett C.R., Westmacott G.R. ( 2013a;). A simple shotgun proteomics method for rapid bacterial identification. J Microbiol Methods 94 5457 10.1016/j.mimet.2013.04.008 [PubMed]. [CrossRef]
    [Google Scholar]
  47. Tracz D.M., McCorrister S.J., Westmacott G.R., Corbett C.R. ( 2013b;). Effect of gamma radiation on the identification of bacterial pathogens by MALDI-TOF MS. J Microbiol Methods 92 132134 10.1016/j.mimet.2012.11.013 [PubMed]. [CrossRef]
    [Google Scholar]
  48. Vandamme P., Peeters C. ( 2014;). Time to revisit polyphasic taxonomy. Antonie van Leeuwenhoek 106 5765 10.1007/s10482-014-0148-x. [CrossRef]
    [Google Scholar]
  49. York M.K., Trayto M.M., Hardy J., Henry M. ( 2010;). Biochemical tests for the identification of aerobic bacteria. . In Clinical Microbiology Procedures Manual , 3rd edn. vol. 1, pp. 821–829. Edited by Garcia L., Isenberg I. Washington, DC: American Society for Microbiology;.
    [Google Scholar]
  50. Zerbino D.R. ( 2010;). Using the Velvet de novo assembler for short-read sequencing technologies. Curr Protoc Bioinformatics 11 (11.5)[PubMed].
    [Google Scholar]
  51. Zerbino D.R., Birney E. ( 2008;). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18 821829 10.1101/gr.074492.107 [PubMed]. [CrossRef]
    [Google Scholar]
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