Divergence between the Highly Virulent Zoonotic Pathogen Helicobacter heilmannii and Its Closest Relative, the Low-Virulence "Helicobacter ailurogastricus" sp. nov

Infect Immun. 2015 Nov 2;84(1):293-306. doi: 10.1128/IAI.01300-15. Print 2016 Jan.

Abstract

Helicobacter heilmannii naturally colonizes the stomachs of dogs and cats and has been associated with gastric disorders in humans. Nine feline Helicobacter strains, classified as H. heilmannii based on ureAB and 16S rRNA gene sequences, were divided into a highly virulent and a low-virulence group. The genomes of these strains were sequenced to investigate their phylogenetic relationships, to define their gene content and diversity, and to determine if the differences in pathogenicity were associated with the presence or absence of potential virulence genes. The capacities of these helicobacters to bind to the gastric mucosa were investigated as well. Our analyses revealed that the low-virulence strains do not belong to the species H. heilmannii but to a novel, closely related species for which we propose the name Helicobacter ailurogastricus. Several homologs of H. pylori virulence factors, such as IceA1, HrgA, and jhp0562-like glycosyltransferase, are present in H. heilmannii but absent in H. ailurogastricus. Both species contain a VacA-like autotransporter, for which the passenger domain is remarkably larger in H. ailurogastricus than in H. heilmannii. In addition, H. ailurogastricus shows clear differences in binding to the gastric mucosa compared to H. heilmannii. These findings highlight the low-virulence character of this novel Helicobacter species.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Adhesion / genetics
  • Bacterial Proteins / genetics
  • Cats
  • Cell Line
  • Deoxyribonucleases, Type II Site-Specific / genetics
  • Dogs
  • Epithelial Cells / microbiology
  • Gastric Mucosa / cytology
  • Gastric Mucosa / microbiology*
  • Gastritis / microbiology*
  • Gerbillinae
  • Glycosyltransferases / genetics
  • Helicobacter Infections / microbiology
  • Helicobacter heilmannii / classification
  • Helicobacter heilmannii / genetics*
  • Helicobacter heilmannii / pathogenicity*
  • Humans
  • Intestinal Mucosa / cytology
  • Intestinal Mucosa / microbiology*
  • Molecular Sequence Data
  • Phylogeny
  • Protein Structure, Tertiary
  • RNA, Ribosomal, 16S / genetics
  • Virulence / genetics
  • Zoonoses / microbiology

Substances

  • Bacterial Proteins
  • RNA, Ribosomal, 16S
  • iceA1 protein, Helicobacter pylori
  • Glycosyltransferases
  • Deoxyribonucleases, Type II Site-Specific
  • HrgA protein, Helicobacter pylori

Grants and funding

Agentschap voor Innovatie door Wetenschap en Technologie (IWT) provided funding to Myrthe Joosten under grant number SB-121092. Fonds Wetenschappelijk Onderzoek (FWO) provided funding to Annemieke Smet. Research Fund Ghent University provided funding to Richard Ducatelle and Freddy Haesebrouck under grant number GOA 01G00408. Svenska Forskningsrådet Formas (Swedish Research Council Formas) (grant numbers 221-2011-1036 and 221-2013-590), Vetenskapsrådet (Swedish Research Council; grant number 521-2011-2370), the Swedish Cancer Foundation, and the Söderbergs Foundation provided funding to Sara K. Lindén, Emma Skoog, and Médea Padra. National Health and Medical Research Council (NHMRC) (grant number 572723) and the University of Western Australia (UWA) provided funding to Alfred Chin Yen Tay, Fanny Peters, Tim Perkins, and Barry J. Marshall.