1887

Abstract

As part of a larger study on carried by wild birds in the city of Valdivia (southern Chile), two curved rod-shaped Gram-stain-negative strains (A82 and WB-40) were recovered from faecal samples and subjected to a taxonomic study. Results of a genus-specific PCR showed that these isolates belonged to the genus . Further identification by 16S rRNA and (60 kDa heat-shock protein) gene sequence analysis revealed that they formed a separate phylogenetic clade, different from other known species with ‘’ CNRCH 2005/566H and WBE14 being the most closely related species. This was confirmed by core-genome phylogeny as well as digital DNA–DNA hybridization and average nucleotide identity analyses between the genomes of strains A82 and WB-40 and all other species. The draft genome sequences of A82 and WB-40, obtained by Illumina NextSeq 2000 sequencing, consisted of 1.6 Mb with a G+C content of 31.9–32.0 mol%. The results obtained from the phylogenetic and genomic characterization, together with their different morphological and biochemical features, revealed that these two strains represent a novel species, for which we propose the name sp. nov. with A82 (=LMG 32718=CCCT 22.04) as the type strain.

Keyword(s): Chile , faeces , Helicobacter and wild bird
Funding
This study was supported by the:
  • Comisión Nacional de Investigación Científica y Tecnológica (Award FONDECYT Project Nº 1200125)
    • Principle Award Recipient: LuisCollado
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005983
2023-11-28
2024-05-09
Loading full text...

Full text loading...

References

  1. Ochoa S, Collado L. Enterohepatic Helicobacter species - clinical importance, host range, and zoonotic potential. Crit Rev Microbiol 2021; 47:728–761 [View Article] [PubMed]
    [Google Scholar]
  2. Flahou B, Haesebrouck F, Smet A. Non-Helicobacter pylori Helicobacter infections in humans and animals. In Backert S, Yamaoka Y. eds Helicobacter Pylori Research Japan: Springer; 2016 pp 233–3369 [View Article]
    [Google Scholar]
  3. Dewhirst FE, Seymour C, Fraser GJ, Paster BJ, Fox JG. Phylogeny of Helicobacter isolates from bird and swine feces and description of Helicobacter pametensis sp. nov. Int J Syst Bacteriol 1994; 44:553–560 [View Article] [PubMed]
    [Google Scholar]
  4. Fox JG, Taylor NS, Howe S, Tidd M, Xu S et al. Helicobacter anseris sp. nov. and Helicobacter brantae sp. nov., isolated from feces of resident Canada geese in the greater Boston area. Appl Environ Microbiol 2006; 72:4633–4637 [View Article] [PubMed]
    [Google Scholar]
  5. Waldenström J, On SLW, Ottvall R, Hasselquist D, Harrington CS et al. Avian reservoirs and zoonotic potential of the emerging human pathogen Helicobacter canadensis. Appl Environ Microbiol 2003; 69:7523–7526 [View Article] [PubMed]
    [Google Scholar]
  6. Collado L, Jara R, González S. Description of Helicobacter valdiviensis sp. nov., an epsilonproteobacteria isolated from wild bird faecal samples. Int J Syst Evol Microbiol 2014; 64:1913–1919 [View Article] [PubMed]
    [Google Scholar]
  7. Aydin F, Saticioglu IB, Ay H, Kayman T, Karakaya E et al. Description of the two novel species of the genus Helicobacter: Helicobacter anatolicus sp. nov., and Helicobacter kayseriensis sp. nov., isolated from feces of urban wild birds. Syst Appl Microbiol 2022; 45:126357 [View Article] [PubMed]
    [Google Scholar]
  8. Fox JG, Chien CC, Dewhirst FE, Paster BJ, Shen Z et al. Helicobacter canadensis sp. nov. isolated from humans with diarrhea as an example of an emerging pathogen. J Clin Microbiol 2000; 38:2546–2549 [View Article] [PubMed]
    [Google Scholar]
  9. Fresia P, Jara R, Sierra R, Ferrés I, Greif G et al. Genomic and clinical evidence uncovers the enterohepatic species Helicobacter valdiviensis as a potential human intestinal pathogen. Helicobacter 2017; 22:e12425 [View Article] [PubMed]
    [Google Scholar]
  10. Ahmed NA, Gulhan T. Campylobacter in wild birds: is it an animal and public health concern?. Front Microbiol 2021; 12:812591 [View Article] [PubMed]
    [Google Scholar]
  11. Aydin F, Karakaya E, Kayman T, Abay S, Saticioglu IB. Helicobacter turcicus sp. nov., a catalase-negative new member of the Helicobacter genus, isolated from Anatolian ground squirrel (Spermophilus xanthoprymnus) in Turkey. Int J Syst Evol Microbiol 2022; 72:5338 [View Article] [PubMed]
    [Google Scholar]
  12. Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM. Identification of birds through DNA barcodes. PLoS Biol 2004; 2:e312 [View Article] [PubMed]
    [Google Scholar]
  13. Fox JG, Dewhirst FE, Shen Z, Feng Y, Taylor NS et al. Hepatic Helicobacter species identified in bile and gallbladder tissue from Chileans with chronic cholecystitis. Gastroenterology 1998; 114:755–763 [View Article] [PubMed]
    [Google Scholar]
  14. Vandamme P, Holmes B, Bercovier H, Coenye T. Classification of centers for disease control group Eugonic Fermenter (EF)-4a and EF-4b as Neisseria animaloris sp. nov. and Neisseria zoodegmatis sp. nov., respectively. Int J Syst Evol Microbiol 2006; 56:1801–1805 [View Article] [PubMed]
    [Google Scholar]
  15. Hill JE, Paccagnella A, Law K, Melito PL, Woodward DL et al. Identification of Campylobacter spp. and discrimination from Helicobacter and Arcobacter spp. by direct sequencing of PCR-amplified cpn60 sequences and comparison to cpnDB, a chaperonin reference sequence database. J Med Microbiol 2006; 55:393–399 [View Article] [PubMed]
    [Google Scholar]
  16. 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 [View Article] [PubMed]
    [Google Scholar]
  17. 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]
  18. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  19. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article] [PubMed]
    [Google Scholar]
  20. Andrews S. FastQC: a quality control tool for high throughput sequence data; 2010 http://www.bioinformatics.babraham.ac.uk/projects/fastqc
  21. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  22. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  23. Mikheenko A, Prjibelski A, Saveliev V, Antipov D, Gurevich A. Versatile genome assembly evaluation with QUAST-LG. Bioinformatics 2018; 34:i142–i150 [View Article] [PubMed]
    [Google Scholar]
  24. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  25. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  26. Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J. Helicobacter. In Bergey’s Manual of Systematics of Archaea and Bacteria New York (NY): Wiley; 2015
    [Google Scholar]
  27. de la Haba RR, López-Hermoso C, Sánchez-Porro C, Konstantinidis KT, Ventosa A. Comparative genomics and phylogenomic analysis of the genus Salinivibrio. Front Microbiol 2019; 10:2104 [View Article] [PubMed]
    [Google Scholar]
  28. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
    [Google Scholar]
  29. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article] [PubMed]
    [Google Scholar]
  30. Shimodaira H, Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 1999; 16:1114–1116 [View Article]
    [Google Scholar]
  31. Yoon SH, Ha SM, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
    [Google Scholar]
  32. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  33. On SLW, Miller WG, Houf K, Fox JG, Vandamme P. Minimal standards for describing new species belonging to the families Campylobacteraceae and Helicobacteraceae: Campylobacter, Arcobacter, Helicobacter and Wolinella spp. Int J Syst Evol Microbiol 2017; 67:5296–5311 [View Article] [PubMed]
    [Google Scholar]
  34. Mills CK, Gherna RL. Hydrolysis of indoxyl acetate by Campylobacter species. J Clin Microbiol 1987; 25:1560–1561 [View Article] [PubMed]
    [Google Scholar]
  35. Cook GT. A plate test for nitrate reduction. J Clin Pathol 1950; 3:359–362 [View Article] [PubMed]
    [Google Scholar]
  36. On SL, Holmes B. Effect of inoculum size on the phenotypic characterization of Campylobacter species. J Clin Microbiol 1991; 29:923–926 [View Article] [PubMed]
    [Google Scholar]
  37. Goodwin CS, Armstrong JA, Chilvers T, Peters M, Collins MD et al. Transfer of Campylobacter pylori and Campylobacter mustelae to Helicobacter gen. nov. as Helicobacter pylori comb. nov. and Helicobacter mustelae comb. nov., respectively. Int J Syst Bacteriol 1989; 39:397–405 [View Article]
    [Google Scholar]
  38. Vandamme P, Falsen E, Rossau R, Hoste B, Segers P et al. Revision of Campylobacter, Helicobacter, and Wolinella taxonomy: emendation of generic descriptions and proposal of Arcobacter gen. nov. Int J Syst Bacteriol 1991; 41:88–103 [View Article] [PubMed]
    [Google Scholar]
  39. Eaton KA, Dewhirst FE, Radin MJ, Fox JG, Paster BJ et al. Helicobacter acinonyx sp. nov., isolated from cheetahs with gastritis. Int J Syst Bacteriol 1993; 43:99–106 [View Article] [PubMed]
    [Google Scholar]
  40. Stanley J, Linton D, Burnens AP, Dewhirst FE, On SL et al. Helicobacter pullorum sp. nov. -genotype and phenotype of a new species isolated from poultry and from human patients with gastroenteritis. Microbiology 1994; 140:3441–3449 [View Article] [PubMed]
    [Google Scholar]
  41. Shen Z, Fox JG, Dewhirst FE, Paster BJ, Foltz CJ et al. Helicobacter rodentium sp. nov., a urease-negative Helicobacter species isolated from laboratory mice. Int J Syst Bacteriol 1997; 47:627–634 [View Article] [PubMed]
    [Google Scholar]
  42. Simmons JH, Riley LK, Besch-Williford CL, Franklin CL. Helicobacter mesocricetorum sp. nov., a novel Helicobacter isolated from the feces of Syrian hamsters. J Clin Microbiol 2000; 38:1811–1817 [View Article] [PubMed]
    [Google Scholar]
  43. Robertson BR, O’Rourke JL, Vandamme P, On SL, Lee A. Helicobacter ganmani sp. nov., a urease-negative anaerobe isolated from the intestines of laboratory mice. Int J Syst Evol Microbiol 2001; 51:1881–1889 [View Article] [PubMed]
    [Google Scholar]
  44. Shen Z, Mannion A, Lin M, Esmail M, Bakthavatchalu V et al. Helicobacter monodelphidis sp. nov. and Helicobacter didelphidarum sp. nov., isolated from grey short-tailed opossums (Monodelphis domestica) with endemic cloacal prolapses. Int J Syst Evol Microbiol 2020; 70:6032–6043 [View Article] [PubMed]
    [Google Scholar]
  45. Gruntar I, Kostanjšek R, Pirš T, Papić B. Helicobacter colisuis sp. nov., isolated from caecal contents of domestic pigs (Sus scrofa domesticus). Int J Syst Evol Microbiol 2022; 72:5600 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.005983
Loading
/content/journal/ijsem/10.1099/ijsem.0.005983
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error