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1 Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
2 Department of Biochemistry, Physiology and Microbiology, Faculty of Sciences, Ghent University, Ledeganckstraat 35, B-9000 Ghent, Belgium
3 Institute of Microbiology and Parasitology, Veterinary Faculty, University of Ljubljana, Gerbiceva 60, 1000 Ljubljana, Slovenia
4 CODA – CERVA – VAR, Groeselenberg 99, B-1180 Brussels, Belgium
Correspondence
M. Baele
Margo.Baele{at}UGent.be
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA, partial ureAB and hsp60 gene sequences of H. baculiformis M50T are EF070342, EF070343 and EF070344, respectively.
Supplementary tables showing the distance matrix values for the Helicobacter strains examined in this study based on 16S rRNA, ureAB and hsp60 gene sequences are available with the online version of this paper.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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). Two other species have been described after their isolation from dog stomachs, namely Helicobacter bizzozeronii and Helicobacter salomonis (Hänninen et al., 1996; Jalava et al., 1997). The prevalence of H. bizzozeronii, H. felis and H. salomonis in the stomachs of 110 dogs and 43 cats was investigated by a multiplex PCR and it was found that in cats, H. felis (63 %) and H. bizzozeronii (35 %) were the most predominant species, while only 2.3 % of the animals were colonized by H. salomonis (Van den Bulck et al., 2005). Based on 16S rRNA gene sequence analysis, all three species are phylogenetically very highly related to each other and to ‘Helicobacter heilmannii’ type 2 organisms, detected in the human gastric mucosa (Solnick et al., 1993). The similarity of the ureAB urease genes of the three species is, however, lower than 85 %, allowing discrimination between these species. A fourth uncultured species has been detected in wild feline and in human gastric biopsies by PCR. Sequencing analysis of urease genes showed sufficient differences to those of H. felis, H. bizzozeronii and H. salomonis and this fourth uncultured species was provisionally named ‘Candidatus Helicobacter heilmannii’ (O'Rourke et al., 2004). Recently, another isolate from the stomach of a dog was described as Helicobacter cynogastricus after a polyphasic taxonomic study (Van den Bulck et al., 2006).
Bacteria with a corkscrew-like motion similar to that of species of the genus Helicobacter but with a different morphology have been isolated from animals and humans and are designated as ‘Flexispira rappini’ (Eaton et al., 1996). This is a provisional name given to Gram-negative, microaerophilic, motile, fusiform-shaped organisms with spiral periplasmic fibres and bipolar tufts of sheathed flagella, which explain the corkscrew movement. Phylogenetic analysis of several ‘Flexispira rappini’ isolates from sheep, pigs, rodents, dogs and primates has shown that these all belong to the genus Helicobacter. Strains belonging to flexispira taxa 1, 4, 5 and 6 have been described as Helicobacter trogontum (Dewhirst et al., 2000a; Hänninen et al., 2003; Mendes et al., 1996), while Helicobacter bilis comprises taxa 2, 3, 8 and 9 (Dewhirst et al., 2000a; Hänninen et al., 2005). H. bilis was also isolated from feline faeces (Hänninen et al., 2005), but until now, no organisms with a flexispira morphology have been described that colonize the feline stomach. Helicobacter sp. flexispira taxon 7 comprised one isolate from a dog's stomach (Dewhirst et al., 2000a; Eaton et al., 1996).
In this study, we describe the isolation and characterization of a Helicobacter strain with flexispira-like morphology, isolated from the stomach mucosa of a cat.
The novel strain, designated M50T, was isolated from the mucosa of the stomach of a cat euthanized at the Veterinary Faculty, University of Ljubljana, Slovenia. Tissue samples were handled as described by Gruntar et al. (2003). Bacteria were grown on fresh Columbia agar plates (Oxoid) containing 7 % defibrinated and lysed horse blood, 7 % defibrinated and lysed sheep blood, vancomycin (5 mg l–1; Sigma), trimethoprim (3 mg l–1; Sigma), polymyxin B (2500 U l–1; Sigma) and amphotericin B (Fungizone; 5 mg l–1; Bristol–Myers Squibb). Plates were incubated with lids uppermost at 37 °C under humidified microaerophilic conditions in a closed circuit that was created by evacuating 75 % of the normal atmosphere and introducing a gas mixture of 6.7 % CO2, 1.3 % H2 and 92 % N2. Plates were checked every two days and BHI broth supplemented with 20 % horse serum (Sigma) and 20 % yeast extract (Biolife) was added to the agar surface to ensure that the plates did not dry out. Primary growth was detected after 3 days of incubation by examination of the broth by dark-field microscopy, revealing the presence of large, rod-shaped and motile bacterial cells. Growth of subcultures occurred as a spreading layer on moist agar plates. Rapid oxidase, catalase and urease tests were positive and the isolate was unable to grow aerobically. Gram staining revealed that the isolate was Gram-negative and had a bacillary shape. Pinpoint colonies were observed when an abundant amount of bacteria was inoculated onto a dry agar surface; however, bacteria grown on such a medium mainly lost their bacillary morphology and transformed to coccoid forms. The isolate was stored in sterile skimmed milk with 15 % glycerol at –70 °C for later studies.
Genomic DNA of strain M50T was extracted using the DNeasy Tissue kit (Qiagen) according to the manufacturer's instructions.
The 16S rRNA gene was amplified using the commercially available Qiagen Taq Mastermix, to which primers 
β-NOT (5'-AGTTTGATCCTGGCTCAG-3') and 
MB (5'-TACCTTGTTACGACTTCGTCCCA-3') were added at a concentration of 0.2 mM. The PCR products were sequenced using the BigDye Terminator sequencing kit (Applied Biosystems) and primers pD, 
*, 3 and O* (Coenye et al., 1999), as described previously (Baele et al., 2001), and determined on a DNA sequencer (ABI Prism 3100 Genetic Analyzer, Applied Biosystems). The electropherograms were exported and converted to KODON (Applied Maths). The sequences were compared with the NCBI GenBank by using the BLAST search tool. Phylogenetic analysis was performed using the KODON software after including the consensus sequence in an alignment of small ribosomal subunit sequences collected from GenBank. The 16S rRNA gene of strain M50T (GenBank accession no. EF070342) showed 98–99 % sequence similarity with ‘H. heilmannii’ type 2, H. felis, H. salomonis and H. bizzozeronii.
Multiple alignment was calculated using an open gap penalty of 100 % and a unit gap penalty of 0 %. A tree was constructed using the neighbour-joining method. The dendrogram is shown in Fig. 1 and strain M50T was situated near the H. felis, H. bizzozeronii, H. salomonis, H. cynogastricus, and ‘Ca. H. heilmannii’ cluster. These species have all been isolated from the stomachs of dogs (Hänninen et al., 1996; Jalava et al., 1997; Van den Bulck et al., 2006), cats (Lee et al., 1988; O'Rourke et al., 2004) and/or humans (Andersen et al., 1999; Jalava et al., 2001; O'Rourke et al., 2004). Only 90.7 % 16S rRNA gene sequence similarity was found to ‘Flexispira rappini’ taxon 7, comprising a Helicobacter isolate from a dog stomach (accession no. U51874). Multiple aligned distances, as calculated using KODON, are shown in Supplementary Table S1 (available at IJSEM Online).
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). DNA extracted from pure cultures of H. felis, H. salomonis and H. bizzozeronii served as positive controls, while highly purified water was included as a negative control. Fluorescently labelled PCR products were separated by means of capillary electrophoresis using an ABI Prism 3100 Genetic Analyzer (Applied Biosystems). Product lengths were determined by interpolation with an internal size standard mixture of GENESCAN 500 ROX (Applied Biosystems) and GENESCAN 400-HD ROX (Applied Biosystems) using GeneMapper (Applied Biosystems).
Strain M50T yielded an amplicon of 137 bp with the tRNA intergenic spacer-specific primers, which is the same as the amplicon obtained for H. felis strains. However, no H. felis-specific urease gene fragment was obtained with the NED-labelled primers.
The sequences of the urease genes ureA and ureB have been shown to be more discriminative than the 16S rRNA gene sequence and are thus very useful for phylogenetic analysis of gastric Helicobacter species (O'Rourke et al., 2004). A 1224 bp fragment of the ureAB genes was amplified and sequenced using primers U430F and U1735R and with conditions as described above. A sequence of 1072 bp (GenBank accession no. EF070343) was obtained and showed about 80 % similarity with the urease sequence of H. felis strain INTO (AY368267).
Multiple alignment was calculated using an open gap penalty of 100 % and a unit gap penalty of 0 %. A tree was constructed using the neighbour-joining method and is shown in Fig. 2. Highest similarity (77–81 %) was obtained with sequences from H. felis strains. Gene sequence similarities of 78–80 %, 75–76 %, 73–75 %, 72–74 % and 71 % were obtained to H. salomonis, H. bizzozeronii, ‘Ca. H. suis’, ‘Ca. H. heilmannii’ and H. cynogastricus, respectively. The results of comparisons of the urease sequences of strain M50T with other gastric Helicobacter species are shown in a distance matrix (see Supplementary Table S2 available in IJSEM Online).
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). A 515 bp sequence (GenBank accession no. EF070344) obtained from isolate M50T using the methodology described by Mikkonen et al. (2004) placed this taxon into the cluster of H. felis, H. bizzozeronii, H. salomonis and H. cynogastricus, confirming the results based on 16S rRNA gene and ureAB sequence analysis. Only 70–75 % similarity was obtained with these species, yielding sufficient difference to consign isolate M50T into a new taxon. Multiple aligned distances are shown in Supplementary Table S3 (see IJSEM Online). A phylogenetic tree obtained from this matrix using the neighbour-joining method is shown in Fig. 3.
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recently suggested that 16S rRNA gene sequence data do not always faithfully reflect phylogenetic relationships and that 23S rRNA gene sequence data are significantly more reliable for identification and classification of helicobacters due to the threefold-higher number of informative bases. Therefore, we also attempted to amplify the 23S rRNA gene of strain M50T using PCR primers O68 and M89 (Dewhirst et al., 2005). However, no amplicons were obtained in this PCR. DNA of H. cynogastricus strain JKM4T was used as a positive control and did yield a band of the expected length (approx. 2730 bp).
Polyacrylamide gel electrophoresis (PAGE) of whole-cell proteins of strain M50T was performed in order to confirm its distinct taxonomic status. For this purpose, strain M50T was grown on BHI agar supplemented with 5 % (v/v) horse blood and was incubated at 37 °C in a micro-aerobic atmosphere as described above. A whole-cell protein extract was prepared and sodium dodecyl sulphate PAGE was performed as described previously (Pot et al., 1994). Whole-cell protein profiles of H. bizzozeronii, H. salomonis, H. felis and H. cynogastricus reference strains and of type and reference strains of other Helicobacter species were available from previous studies (Jalava et al., 1998, 2001; Van den Bulck et al., 2006). Densitometric analysis, normalization and interpolation of the protein profiles, and numerical analysis were performed using the GelCompar software package version 4.2 (Applied Maths). The similarity between all pairs of traces was expressed by the Pearson product moment correlation coefficient presented as percentages of similarity. This analysis demonstrated that strain M50T can be clearly distinguished from all of its cultured closest relatives (Fig. 4). Given the correlation between level of whole-cell protein electrophoretic similarity and DNA–DNA hybridization (Dewhirst et al., 2000b; Vandamme et al., 1996), these results confirm that strain M50T represents a species distinct from its nearest phylogenetic neighbours.
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) and after ultrathin sectioning as described by Mast et al. (2005) (Fig. 5).
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Biochemical and tolerance tests were carried out according to the recommendations of Dewhirst et al. (2000b). Growth of strain M50T was examined on Brucella agar supplemented with 20 % fetal calf serum at 25, 37 and 42 °C under microaerobic conditions, and at 37 °C under aerobic, microaerobic and anaerobic conditions. Tolerance to 1 % bile, 1 % glycine and 1.5 % NaCl was determined on Brucella agar with 20 % fetal calf serum. Growth was tested on BHI agar, Brucella agar and Mueller–Hinton agar, supplemented with 20 % fetal calf serum or 10 % defibrinated horse blood. All media were incubated for 7 days in a microaerobic atmosphere at 37 °C. The isolates were Gram stained and examined for catalase activity by standard microbiological methods. Oxidase activity was determined with Bactident Oxidase strips (Merck). With the API Campy identification system (bioMérieux), the following biochemical analyses were performed: urease activity, reduction of nitrates, esterase activity, hydrolysis of hippurate, -glutamyltransferase activity, reduction of triphenyl-tetrazoliumchloride (TTC), alkaline phosphatase activity and pyrrolidonyl, L-arginine and L-aspartate arylamidase activities. Tests were read after 24 h of incubation at 37 °C in an aerobic atmosphere. Indoxyl acetate hydrolysis was determined as previously described by Mills & Gherna (1987). Susceptibility to cephalothin and nalidixic acid (both at 30 µg per disc; Becton Dickinson) was examined on BHI agar plates supplemented with 10 % defibrinated horse blood, as recommended by Dewhirst et al. (2000b). Growth in the presence of metronidazole was determined with BHI agar (Oxoid) containing 10 % horse blood and 5 µg ml–1 of the test compound. A detailed list of results is given in the description section below and a comparison of the most important phenotypic characteristics of strain M50T with those of other Helicobacter species is shown in Table 1.
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Description of Helicobacter baculiformis sp. nov.
Helicobacter baculiformis (ba.cu.li.for'mis. L. n. baculus rod; L. suff. -formis of the shape of; N.L. masc. adj. baculiformis rod-shaped).
Cells are large, slender to slightly spiral rods that are approximately 10 µm long and approximately 1 µm wide. They possess four periplasmic fibrils running along the external side of the helix. Coccoid cells predominate in older cultures. Cells are Gram-negative and non-sporulating. They are motile by means of tufts of up to 11 sheathed flagella at both ends of the cells. The flagella are blunt-ended and the terminal diameter is wider than the average diameter of the flagellar body. Growth is observed on BHI agar, Brucella agar and on Mueller–Hinton agar supplemented with 20 % fetal calf serum or with 10 % defibrinated horse blood. Grows in micro-aerophilic conditions as well as in a 5 % CO2-supplemented atmosphere. Weak growth is seen after anaerobic incubation. Grows at 37 °C, but not at 25 °C or 42 °C. No growth on media supplemented with 1.5 % NaCl, 1 % glycine or 1 % ox bile. Oxidase-, catalase- and urease-positive. Reduces nitrate and TTC and tests positive for esterase, -glutamyl transpeptidase, L-arginine arylamidase and alkaline phosphatase. Hippurate and indoxyl acetate are not hydrolysed and activity of pyrrolidonyl arylamidase and L-aspartate arylamidase is not detected. The type strain, strain M50T, is resistant to cephalothin (30 µg) and intermediately susceptible to nalidixic acid (30 µg). The clinical significance of H. baculiformis is unknown.
The type strain, strain M50T (=LMG 23839T=CCUG 53816T), was isolated from the gastric mucosa of a cat.
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ACKNOWLEDGEMENTS |
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