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Volume 71, Issue 7

Reclassification of [] as gen. nov., comb. nov. including Bisgaard taxon 35 No Access

Abstract

[] and the unpublished Bisgaard taxon 35 are associated with respiratory and urogenital tract infections in dogs. A total of 21 strains including the type strain of [] were included in the investigation. Strains of [] and taxon 35 formed a monophyletic group demonstrating at least 97.8 and 96.5% similarities within the group based upon 16S rRNA and gene sequence comparisons, respectively. was the most closely related species to [] and taxon 35 with 96.1 % 16S rRNA gene sequence similarity which is slightly higher than the 95 % separating most genera of the family . However, the conserved protein sequence phylogeny documented a unique position of [] with only 81 % identity to the most closely related species, genomospecies 1 of the genus which is lower than the 85 % separating most genera of the family . The conserved protein sequence identity to , the type species of the genus, was 77%, demonstrating that [] is not properly classified as a member of the genus . On the basis of the phylogenetic comparisons, the taxa [] and taxon 35 are proposed to be included with a novel genus with one species, which is reclassified from [] . Phenotypic characters obtained with isolates genetically approved to represent were in accordance with those of the members of the family and the novel genus can be separated from most of the existing genera by a positive catalase reaction, lack of V-factor requirement for growth, lack of haemolysis of blood agar and negative Voges–Proskauer and urease tests. The novel genus cannot be separated by biochemical and physiological characteristics alone from the genera , , and . However, MALDI-TOF mass spectroscopy and also RpoB amino acid signatures allowed a clear separation from these taxa, supporting the existence of a novel genus. The DNA G+C content is 37.0–37.8 mol% for the genus, based on the whole genomic sequences. The type strain of is CCUG 3714 (=ATCC 19416=NCTC 1659) isolated in 1901 from the prepuce of a dog in Germany.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): EF 32 , haemin , haemorrhagic pneumonia , porphyrin , prostate inflammation and U24 of Biberstein
© 2021 The Authors
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2021-07-15
2024-04-26
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References

  1. Christensen H, Kuhnert P, Busse H-J, Blackall P, Bisgaard M. Pasteurella. In Trujillo M, Dedysh S, DeVos P, Hedlund B, Kämpfer P. eds Bergey’s Manual of Systematics of Archaea and Bacteria Wiley & Sons; 2020
     [Google Scholar]
  2. Bisgaard M. Ecology and significance of Pasteurellaceae in animals. Zentralbl Bakteriol 1993; 279:7–26 [View Article] [PubMed]
     [Google Scholar]
  3. Dousse F, Thomann A, Brodard I, Korczak BM, Schlatter Y et al. Routine phenotypic identification of bacterial species of the family Pasteurellaceae isolated from animals. J Vet Diagn Invest 2008; 20:716–724 [View Article] [PubMed]
     [Google Scholar]
  4. Korczak BM, Bisgaard M, Christensen H, Kuhnert P. Frederiksenia canicola gen. nov., sp. nov. isolated from dogs and human dog-bite wounds. Antonie van Leeuwenhoek 2014; 105:731–741 [View Article]
     [Google Scholar]
  5. Biberstein EL, Jang SS, Kass PH, Hirsh DC. Distribution of indole-producing urease-negative pasteurellas in animals. J Vet Diagn Invest 1991; 3:319–323 [View Article] [PubMed]
     [Google Scholar]
  6. Kilian M. A taxonomic study of the genus Haemophilus, with the proposal of a new species. J Gen Microbiol 1976; 93:9–62 [View Article] [PubMed]
     [Google Scholar]
  7. Mutters R, Mannheim W, Bisgaard M. Taxonomy of the group. In Adlam C, Rutter JM. eds Pasteurella and Pasteurellosis London: Acad. Press; 1989 pp 3–34
     [Google Scholar]
  8. Christensen H, Kuhnert P, Busse H-J, Frederiksen WC, Bisgaard M. Proposed minimal standards for the description of genera, species and subspecies of the Pasteurellaceae. Int J Syst Evol Microbiol 2007; 57:166–178 [View Article] [PubMed]
     [Google Scholar]
  9. Christensen H, Bisgaard M. Proper identification of Pasteurellaceae from dogs and dog bite wounds can only be obtained by genotypic characterization. Abstract for Pasteurellaceae 2014
     [Google Scholar]
  10. Friedberger E. Ueber ein neues zur Gruppe des Influenzabacillus gehöriges hämoglobinophiles Bakterium (”Bacillus haemoglobinophilus canis”. Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene 1 Abteilung Reihe A Originale, Medizinische Mikrobiologie und Parasitologie 1903; 33:401–406
     [Google Scholar]
  11. Rivers TM. Bacillus hemoglobinophilus canis (Friedberger) (Hemophilus canis emend. J Bacteriol 1922; 7:579–581 [View Article] [PubMed]
     [Google Scholar]
  12. Christensen H, Angen Ø, Olsen JE, Bisgaard M. Genotypical characterization of atypical isolates of Pasteurella multocida and revised description of P. multocida to include phenotypic variants previously classified as biovar 2 of P. canis and P. avium. Microbiology 2004; 150:1757–1767
     [Google Scholar]
  13. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article] [PubMed]
     [Google Scholar]
  14. Rice P, Longden I, Bleasby A. EMBOSS: The European Molecular Biology Open Software Suite. Trends Genetics 2000; 16:276–277 [View Article]
     [Google Scholar]
  15. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 1997; 23:2947–2948
     [Google Scholar]
  16. Kumar S, Stecher G, Tamura K. MEGA7: Molecular evolutionary genetics analysis Version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
     [Google Scholar]
  17. Angen Ø, Ahrens P, Kuhnert P, Christensen H, Mutters R. Proposal of Histophilus somni gen. nov., sp. nov. for the three species incertae sedis “Haemophilus somnus”, “Haemophilus agni” and “Histophilus ovis”. Int J Syst Evol Microbiol 2003; 53:1449–1456 [View Article] [PubMed]
     [Google Scholar]
  18. Adhikary S, Nicklas W, Bisgaard M, Boot R, Kuhnert P et al. Rodentibacter gen. nov. including Rodentibacter pneumotropicus comb. nov., Rodentibacter heylii sp. nov., Rodentibacter myodis sp. nov., Rodentibacter ratti sp. nov., Rodentibacter heidelbergensis sp. nov., Rodentibacter trehalosifermentans sp. nov., Rodentibacter rarus sp. nov., Rodentibacter mrazii and two genomospecies. Int J Syst Evol Microbiol 2017; 67:1793–1806 [View Article] [PubMed]
     [Google Scholar]
  19. Tindall BJ, Rosselló-Móra R, Busse HJ, Ludwig W, Kämpfer P. Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 2010; 60:249–266 [View Article] [PubMed]
     [Google Scholar]
  20. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617
     [Google Scholar]
  21. De Ley J, Mannheim W, Mutters R, Piechulla K, Tytgat R et al. Inter- and intrafamilial similarities of rRNA cistrons of Pasteurellaceae. Int J System Bacteriol 1990; 40:126–137
     [Google Scholar]
  22. Dewhirst FE, Paster BJ, Olsen I, Fraser GJ. Phylogeny of the Pasteurellaceae as determined by comparison of 16S ribosomal ribonucleic acid sequences. Zentralbl Bakteriol 1993; 279:35–44 [View Article] [PubMed]
     [Google Scholar]
  23. Korczak B, Christensen H, Emler S, Frey J, Kuhnert P. Phylogeny of the family Pasteurellaceae based on rpoB sequences. Int J Syst Evol Microbiol 2004; 54:1393–1399 [View Article] [PubMed]
     [Google Scholar]
  24. Mollet C, Drancourt M, Raoult D. rpoB sequence analysis as a novel basis for bacterial identification. Mol Microbiol 1997; 26:1005–1011 [View Article]
     [Google Scholar]
  25. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article] [PubMed]
     [Google Scholar]
  26. Sayers EW, Beck J, Bolton EE, Bourexis D, Brister JR et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 2021; 49:D10–D17 [View Article] [PubMed]
     [Google Scholar]
  27. Lee I, Ouk Kim Y, Park SC, Chun J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article] [PubMed]
     [Google Scholar]
  28. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351
     [Google Scholar]
  29. Auch AF, von Jan M, Klenk H-P, 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 [View Article] [PubMed]
     [Google Scholar]
  30. Auch AF, Klenk HP, Göker M. Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci 2010; 2:142–148 [View Article] [PubMed]
     [Google Scholar]
  31. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O et al. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 1987; 37:463–464
     [Google Scholar]
  32. Walk ST. The “Cryptic” Escherichia. EcoSalPlus. Domain 6. ESP-0002-2015. ASMScience.org/EcoSalPlus; 2015
  33. Christensen H, Kuhnert P, Busse HJ, Blackall P, Bisgaard M. Pasteurellaceae. In Trujillo M, Dedysh S, DeVos P, Hedlund B, Kämpfer P. eds Bergey’s Manual of Systematics of Archaea and Bacteria New York: Wiley & Sons; 2020
     [Google Scholar]
  34. Bisgaard M, Christensen H. Classification of Bisgaard’s taxa 14 and 32 and a taxon from kestrels demonstrating satellitic growth and proposal of Spirabiliibacterium gen. nov., including the description of three species: Spirabiliibacterium mucosae sp. nov., Spirabiliibacterium pneumoniae sp. nov., and Spirabiliibacteriumfalconis sp. nov. printed IJSEM 2021
     [Google Scholar]
  35. Kuhnert P, Korczak BM. 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 (Reading) 2006; 152:2537–2548 [View Article] [PubMed]
     [Google Scholar]
  36. Zeigler DR. Gene sequences useful for predicting relatedness of whole genomes in bacteria. Int J Syst Evol Microbiol 2003; 53:1893–1900 [View Article] [PubMed]
     [Google Scholar]
  37. Christensen H, Bisgaard M. Cytolethal distending proteins predicted in (Haemophilus) haemoglobinophilus and Bisgaard taxon 35 by genomics. 2014, poster. International Pasteurellaceae Conference 2014, Prado; 2014
  38. Chen Y-C, Tan D-H, Shien J-H, Hsieh M-K, Yen T-Y et al. Identification and functional analysis of the cytolethal distending toxin gene from Avibacterium paragallinarum. Avian Pathol 2014; 43:43–50 [View Article] [PubMed]
     [Google Scholar]
  39. Lara-Tejero M, Galán JE. Cytolethal distending toxin: limited damage as a strategy to modulate cellular functions. Trends Microbiol 2002; 10:147–152 [View Article] [PubMed]
     [Google Scholar]
  40. Lara-Tejero M, Galán JE. A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science 2000; 290:354–357 [View Article] [PubMed]
     [Google Scholar]
  41. Bisgaard M, Houghton SB, Mutters R, Stenzel A. Reclassification of German, British and Dutch isolates of so-called Pasteurella multocida obtained from pneumonic calf lungs. Vet Microbiol 1991; 26:115–124 [View Article] [PubMed]
     [Google Scholar]
  42. Bisgaard M, Mutters R. Characterization of some previously unclassified “Pasteurella” spp. obtained from the oral cavity of dogs and cats and description of a new species tentatively classified with the family Pasteurellaceae Pohl 1981 and provisionally called taxon 16. Acta Pathol Microbiol Immunol Scand B 1986; 94:177–184 [View Article] [PubMed]
     [Google Scholar]
  43. Harris TM, Price EP, Sarovich DS, Nørskov-Lauritsen N, Beissbarth J et al. Comparative genomic analysis identifies X-factor (haemin)-independent Haemophilus haemolyticus: a formal re-classification of “Haemophilus intermedius”. Microb Genom 2020; 6:e000303 [View Article] [PubMed]
     [Google Scholar]
  44. Frey J, Kuhnert P. Identification of animal Pasteurellaceae by MALDI-TOF mass spectrometry. Methods Mol Biol 2015; 1247:235–243 [View Article] [PubMed]
     [Google Scholar]
  45. Kuhnert P, Bisgaard M, Korczak BM, Schwendener S, Christensen H et al. Identification of animal Pasteurellaceae by MALDI-TOF mass spectrometry. J Microbiol Methods 2012; 89:1–7 [View Article] [PubMed]
     [Google Scholar]
  46. Jukes TH, Cantor CR. Evolution of protein molecules. In Munro H. eds Mammalian Protein Metabolism New York: Academic Press; 1969 pp 21–132
     [Google Scholar]
  47. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
     [Google Scholar]
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Reclassification of [Haemophilus] haemoglobinophilus as Canicola haemoglobinophilus gen. nov., comb. nov. including Bisgaard taxon 35
Int J Syst Evol Microbiol 71, 004881 (2021); https://doi.org/10.1099/ijsem.0.004881
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/content/journal/ijsem/10.1099/ijsem.0.004881
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