Campylobacter cuniculorum sp. nov., from rabbits

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Campylobacter cuniculorum sp. nov., from rabbits
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  Downloaded from www.microbiologyresearch.org byIP: 174.129.184.250On: Wed, 17 Aug 2016 11:37:10 Campylobacter cuniculorum  sp. nov., from rabbits Renato Giulio Zanoni, 1 Lies Debruyne, 2 Mirko Rossi, 1 3  Joana Revez 1 and Peter Vandamme 2 Correspondence Mirko Rossimirko.rossi@helsinki.fi 1 Department of Veterinary Public Health and Animal Pathology, Alma Mater Studiorum, Universityof Bologna, Via Tolara di Sopra 50, 40064 Ozzano Emilia, Bologna, Italy 2 Department of Biochemistry, Physiology and Microbiology, Faculty of Sciences, Ghent University,K. L. Ledeganckstraat 35, B-9000 Gent, Belgium Eight strains of an unknown thermotolerant  Campylobacter   species were isolated from the caecalcontents of rabbits (  Oryctolagus cuniculus ). All strains were initially identified as belonging to thegenus  Campylobacter   by means of genus-specific PCR, but none were identified using species-specific PCR for known thermophilic species. Cells were spiral shaped with bipolar unsheathedflagella, with no periplasmic fibres, and appeared coccoid after 10–12 days of incubation.Phylogenetic analyses based on 16S rRNA gene,  rpoB  and  groEL  sequences revealed that allstrains formed a robust clade that was very distinct from recognized  Campylobacter   species. 16SrRNA gene sequence pairwise comparisons of strain 150B T with the type strains of other Campylobacter   species revealed that the nearest phylogenetic neighbour was  Campylobacter helveticus  NCTC 12470 T , with 96.6% similarity. The uniqueness of these rabbit isolates wasconfirmed by whole-cell protein electrophoresis. Taken together, these data indicate that thestrains belong to a novel  Campylobacter   species for which the name  Campylobacter cuniculorum sp. nov. is proposed, with 150B T (  5 LMG 24588 T 5 CCUG 56289 T ) as the type strain. The genus  Campylobacter   was proposed by Sebald & Ve´ron(1963) .  In the following decades, this genus has expandedwith the description of species srcinating from mammalsand birds and now, after various reclassifications, includes18 established species and six subspecies (Foster  et al. ,2004; Vandamme  et al. , 2005; Inglis  et al. , 2007). So far, thefew reports on the isolation of campylobacters from rabbitsinclude strains of   Campylobacter jejuni   (Prescott & Bruin-Mosch, 1981; Weber  et al. , 1982) and a  Campylobacter  -likeorganism (Reynaud  et al. , 1993) from healthy anddiarrhoeic animals. In the present paper, we describe theresults of a polyphasic taxonomic investigation of eightstrains of a  Campylobacter  -like organism recovered fromrabbits ( Oryctolagus cuniculus  ) in Italy.Eight  Campylobacter  -like unidentified isolates were recov-ered from the caecal contents of eight rabbits during routinebacteriological analysis. The isolates were obtained between2005 and 2007 from animals reared in intensive andextensive farms in different regions, thereby representing atemporally, geographically and epidemiologically independ-ent set of isolates. Isolations were made after6–8 days of incubation at 37  u C in a microaerobicatmosphere with hydrogen, on nutrient sheep-blood agar [  nutrient broth No. 2 (Oxoid) with 1.5% Bacto agar (Difco)and 5% sheep blood ]  plus cefoperazone, amphotericin B,teicoplanin selective supplement (CAT; Oxoid), on modi-fied-charcoal cefoperazone deoxycholate agar (CM0739;Oxoid) and on nutrient sheep-blood agar using a filtermethod (Zanoni  et al. , 2007). The microaerobic atmospherewith hydrogen was obtained by the gas replacement methodusing an anaerobic gas mixture (10% H 2 , 10% CO 2 , 80%N 2 ) as described by Bolton  et al.  (1992).After 6 days of incubation on nutrient sheep-blood agar,colonies were 1–2 mm in diameter, grey–green, flat withrough margins and slightly mucoid-looking; sometimes thecolonies were  a -haemolytic and exhibited a tailing effectalong the streak line. Cells were Gram-negative, ple-omorphic, typically sigmoid to allantoid in shape,2.6 ± 0.7  m m (mean ± SD ) in length and 0.3 ± 0.1  m m inwidth when observed after Gram-staining. Cells appearedcoccoid after 10–12 days of incubation.Bacterial DNA was extracted by using a ChargeSwitchgDNA Mini bacteria kit (Invitrogen). The strains were 3 Present address:  Department of Food and Environmental Hygiene,University of Helsinki, PO Box 66, Agnes Sjo¨bergin katu 2, FI-00014Helsinki, Finland.The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA, rpoB   and  groEL  gene sequences of strains 150B T , 117/07 and 120/07are DQ400345, EU636818 and EU636820 (16S rRNA gene),EU636830, EU636833 and EU636836 ( rpoB  ) and EU636828,EU636824 and EU636827 ( groEL ), respectively.Neighbour-joining dendrograms based on  rpoB   and  groEL  partial genesequences are available as supplementary material with the onlineversion of this paper. International Journal of Systematic and Evolutionary Microbiology   (2009),  59,  1666–1671  DOI  10.1099/ijs.0.007286-01666 007286 G 2009 IUMS  Printed in Great Britain  Downloaded from www.microbiologyresearch.org byIP: 174.129.184.250On: Wed, 17 Aug 2016 11:37:10 identified as  Campylobacter   using the genus-specific PCR described by Linton  et al.  (1996), but were not identified atthe species level using species-specific PCR tests for Campylobacter coli   and  C. jejuni   (Denis  et al. , 1999), for C. upsaliensis   and  C. helveticus   (Lawson  et al. , 1997) orfor  C. lari   (Linton  et al. , 1996).In order to establish the taxonomic position of the rabbitisolates, a phylogenetic analysis based on the sequences of the 16S rRNA gene was carried out. The nearly complete16S rRNA gene was amplified using universal primers p27f (5 9 -AGAGTTTGATCCTGGCTCAG-3 9 ) and p1492r (5 9 -TACGGCTACCTTGTTACGACT-3 9 ) and the PCR-amp-lified template was sequenced by primer walking (PrimmSRL). Sequences were assembled with  VECTOR NTI  software(Invitrogen) and then aligned in BioEdit (http://www.mbio.ncsu.edu/BioEdit/bioedit.html) with  CLUSTALW  using publicly available  Campylobacter   referencesequences. The alignment was adjusted visually, removingintervening sequence regions and unknown bases, and datawere corrected for multiple base changes by the method of Jukes & Cantor (1969). A phylogenetic tree was con-structed in  MEGA 3 (http://www.megasoftware.net/) usingthe neighbour-joining method. Bootstrap analysis wasperformed with 1000 reassembled datasets.A fragment of 1283 bp of the 16S rRNA gene wassequenced from each strain and a search of the NCBIdatabase using  MEGABLAST  (http://www.ncbi.nlm.nih.gov/blast/) determined that the strains were most closely relatedto taxa within the genus  Campylobacter  , confirming theresults from the genus-specific PCR. Pairwise comparisonsof 16S rRNA gene sequences showed that the rabbit isolateswere genetically highly related to each other, exhibiting99.1–100% sequence similarity. Furthermore, the neigh-bour-joining dendrogram (Fig. 1) indicated that all eightstrains formed a robust clade (100% bootstrap support)that was clearly distinct from all other  Campylobacter  species. Pairwise sequence comparisons of strain 150B T with the type strains of the most closely related speciesrevealed similarities of 96.6, 96.5 and 96.1% with  C.helveticus   NCTC 12470 T ,  C. jejuni   NCTC 11351 T and  C.upsaliensis   CCUG 14913 T , respectively.In view of the low 16S rRNA gene sequence divergencebetween the unidentified strains and other  Campylobacter  species, the phylogenetic relationships were further exam-ined by   rpoB   (Korczak   et al.  2006) and  groEL   (Ka¨renlampi et al. , 2004) sequence analysis. Sequences were processed asdescribed above. Phylogenetic trees based on partialnucleotide sequences of   rpoB   and  groEL   from eight strainsand reference  Campylobacter   strains are shown inSupplementary Fig. S1 (available in IJSEM Online). In bothtrees, all of the unidentified strains clustered together in atight clade clearly separated from all other  Campylobacter  species (100% bootstrap support). The  rpoB   sequencesimilarity values within the clade of the rabbit strains were97.9–100%, while the similarity values towards the other Campylobacter   species were 60.5–80.5%. Likewise,  groEL  sequence similarity values among the rabbit strains were97.7–100% and values between strain 150B T and other Campylobacter   species were below 86%. Similarly toKorczak   et al.  (2006) and Ka¨renlampi  et al.  (2004), weobserved good congruence between  rpoB  ,  groEL   and 16SrRNA gene sequence results, since each of the phylogenetictrees showed a similar topology. However, compared to the16S rRNA gene sequence analysis, the  rpoB   and  groEL  sequence analysis showed lower interspecies similarity. Fig. 1.  Unrooted tree based on 16S rRNAgene sequences showing the relationships ofthe eight strains of  Campylobacter cunicu-lorum  sp. nov. with related species. Numbersat nodes (  ¢ 85%) indicate support for internalbranches within the tree obtained by bootstrapanalysis (percentages of 1000 bootstraps).Bar, 0.02 nucleotide substitutions per base. Campylobacter cuniculorum  sp. nov., from rabbitshttp://ijs.sgmjournals.org 1667  Downloaded from www.microbiologyresearch.org byIP: 174.129.184.250On: Wed, 17 Aug 2016 11:37:10 Although all sequence data demonstrated that the eightisolates represent a coherent taxon, whole-cell proteinelectrophoresis was used to examine further the relation-ships between the isolates. Whole-cell protein electrophor-esis was performed after culturing strains on Mueller–Hinton agar supplemented with 5% horse blood at 37  u Cfor 48 h under microaerobic conditions with hydrogen.Protein extraction and SDS-PAGE were performed asdescribed by Pot  et al.  (1994). Similarity between thenormalized whole-cell protein patterns was determined by the Pearson product–moment correlation coefficient, afterwhich clustering was performed by the unweighted pairgroup method with arithmetic averages (UPGMA), using GELCOMPAR   version 4.2 (Applied Maths). As with many other  Campylobacter   species, a prominent protein bandwith variable position (36.1–43.2 kDa) was present in theprofiles of the rabbit isolates (Fig. 2) and, for numericalanalysis, the region was excluded to increase speciesdiscrimination (Vandamme  et al. , 1991). Excluding thisvariable dense band region from the numerical analysis toenhance species-level discrimination resulted in a cleargrouping of the rabbit isolates.DNA–DNA hybridizations were subsequently performedbetween strains 150B T and 116/07. For this purpose, DNAwas extracted from 0.25–0.5 g (wet weight) cells asdescribed by Pitcher  et al.  (1989). DNA–DNA hybridiza-tions were performed at 30  u C with photobiotin-labelledprobes in microplate wells (Ezaki  et al. , 1989) using anHTS7000 Bio Assay Reader (PerkinElmer) for the fluor-escence measurements. A DNA–DNA hybridization valueof 92% was calculated.The physiological characters of the novel species, deter-mined using standard methods (On & Holmes, 1991a, b,1992; Ursing  et al. , 1994; On  et al. , 1996), along with thoseof all  Campylobacter   reference strains are represented inTable 1 and in the species description. These characteristicsallowed differentiation of the rabbit isolates from recog-nized  Campylobacter   species (Table 1).Morphological characteristics were determined usingtransmission electron microscopy (TEM). For TEM, 48-h-old cells were negatively stained with 1% (w/v)phosphotungstic acid (Sigma) and examined using aZeiss E900 TEM microscope. Cells were spiral shaped,with bipolar unsheathed flagella; periplasmic fibres on thesurface were not observed (data not shown).For the determination of G + C content, DNA wasenzymically degraded into nucleosides as described by Mesbah & Whitman (1989). The nucleoside mixture wasseparated by HPLC using a Waters SymmetryShield C8 Fig. 2.  Dendrogram of the eight strains of  Campylobacter cuniculorum  sp. nov. and representatives of other  Campylobacter  species based on UPGMA cluster analysis of one-dimensional SDS-PAGE cell protein profiles. R. G. Zanoni and others1668  International Journal of Systematic and Evolutionary Microbiology   59  Downloaded from www.microbiologyresearch.org byIP: 174.129.184.250On: Wed, 17 Aug 2016 11:37:10 Table 1.  Phenotypic characteristics of  Campylobacter   species Species/subspecies: 1,  Campylobacter cuniculorum  sp. nov.; 2,  C. canadensis  ; 3,  C. coli  ; 4,  C. concisus  ; 5,  C. curvus  ; 6,  C. fetus   subsp.  fetus  ; 7,  C. fetus   subsp.  venerealis  ; 8,  C. gracilis  ; 9,  C. helveticus  ; 10, C. hominis  ; 11,  C. hyointestinalis   subsp.  hyointestinalis  ; 12,  C. hyointestinalis   subsp.  lawsonii  ; 13,  C. insulaenigrae  ; 14,  C. jejuni   subsp.  doylei  ; 15,  C. jejuni   subsp.  jejuni  ; 16,  C. lanienae  ; 17,  C. lari  ; 18, C. mucosalis  ; 19,  C. rectus  ; 20,  C. showae  ; 21,  C. sputorum ; 22,  C. upsaliensis  . Data for reference species were taken from On  et al.  (1996), Foster  et al.  (2004), Vandamme  et al.  (2005) and Inglis  et al. (2007). No taxa grow aerobically at 37  u C.  + , 90–100% Strains positive; ( + ), 75–89% positive;  V , 26–74% positive; ( 2 ), 11–25% positive; 2 , 0–10% positive;  ND , no data available. mCCDA,modified-charcoal cefoperazone deoxycholate agar; TSI agar, triple sugar-iron agar; TTC, triphenyl tetrazolium chloride. Characteristic 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 a -Haemolysis  +  2  ( 2 ) ( 2 ) ( 2 )  2  V  2  +  ND V V ND  + + +  V  2  + + + + Oxidase  + + +  V  + + +  2  + + + + + + + + + + +  V  + + Catalase  +  V  +  2 2  +  ( + )  V  2 2  + + +  V  + + +  2  ( 2 )  +  V  2 Alkaline phosphatase  2 2 2  V V  2 2 2 2 2 2  ( 2 )  ND  2 2  +  2  ( + )  2 2 2 2 c -Glutamyltranspeptidase  2  ( + )  2 2  ND  2  ND ND  2  ND  2 2  ND  2 2  ND  2  ND ND ND  2 2 Urease  2  V  2 2 2 2 2 2 2 2 2 2 2 2 2 2  V  2 2 2  V *  2 Hydrolysis of:Hippurate  2 2 2 2  ( 2 )  2 2 2 2 2 2 2 2  + +  2 2 2 2 2 2 2 Indoxyl acetate  +  2  +  2  V  2 2  V  +  2 2 2 2  + +  2 2 2  +  2 2  + Reduction of:Nitrate  +  V  +  ( 2 )  + + +  ( + )  +  2  + + +  2  + + +  2  + + + + Selenite  2  ND V  ( 2 )  2  ( + )  2 2 2 2  + +  ND  2  + + +  2  + + + + TTC  V ND  +  2  V  2 2 2 2  ND  2 2  ND V  +  ND  +  2 2 2 2  V Trace H 2 S production on TSI agar  2  V  2 2  ( 2 )  2 2 2 2 2  + +  2 2 2 2 2  +  2  V  +  2 Growth at/in/on:25  u C (microaerobic)  2 2 2 2 2  + +  2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 37  u C (microaerobic)  + + + +  V  + +  2  + + + + + + + + + +  2  V  + + 42  u C (microaerobic) ( + )  + +  ( + )  V  ( + )  2  V  +  ( 2 )  + +  2 2  + + + +  ( 2 )  V  + + 37  u C (anaerobic)  2  +  2  + +  ( 2 )  V  +  2  +  2  +  2 2 2  +  2  + + + +  2 Nutrient agar  +  2  +  ( 2 )  + + + +  ( + )  ND  + +  ND  + +  ND  + +  ( 2 )  V  + + mCCDA ( + )  + +  ( 2 ) ( + )  + +  V  +  ND  + +  ND  + +  ND  + +  2  +  ( + )  + MacConkey agar  2  +  V  2  ( + ) ( + )  V  ( + )  2 2  V V ND  2 2  +  2  ( + )  2  +  V  2 1% Glycine  2  V  +  ( 2 )  + +  2  +  V  + +  V  +  ( 2 )  +  2  +  V  +  V  + + 2% NaCl  2  ND  2  ( 2 )  V  2 2  V  2  +  2 2 2 2 2 2  ( + )  +  V  + +  2 1% Bile  V ND  ( + )  2 2  + +  2  +  ND  +  ( + )  ND  + +  ND  + +  2 2  V  + Requirement for H 2  2 2 2  + +  2 2  +  2  +  V V ND  2 2 2 2  + + +  2 2 Resistance to:Cephalotin ( + )  2  +  2 2 2 2 2 2 2  ( 2 )  2  +  2  + + +  2 2 2 2  ( 2 )Nalidixic acid  V V  2  ( + )  + +  V V  2  V  + + +  2 2  +  V  ( + ) ( + )  2  ( + )  2 *Strains of biovar paraureolyticus are urease-positive; other strains are urease-negative (On  et al. , 1998).  C am  p  y l     o b   a c t    er   c uni     c ul     or   um  s   p.n ov .  ,f   r   omr   a b   b  i     t    s h   t    t     p:  /  /  i      j     s . s   gm  j     o ur  n al     s . or    g1  6  6  9   Downloaded from www.microbiologyresearch.org byIP: 174.129.184.250On: Wed, 17 Aug 2016 11:37:10 column maintained at 37  u C. The solvent was 0.02 M(NH 4 )H 2 PO 4  (pH 4.0) with 1.5% acetonitrile. Non-methylated  l -phage DNA (Sigma) was used as thecalibration reference. The DNA G + C content of strain150B T was 32.4 mol%. This value is within the rangereported for the genus  Campylobacter   (29–47 mol%)(Vandamme  et al. , 2005).In conclusion, the results of this polyphasic taxonomicstudy indicate that the isolates recovered from the caecalcontents of rabbits represent a homogeneous novel specieswithin the genus  Campylobacter  , for which we propose thename  Campylobacter cuniculorum  sp. nov. Description of  Campylobacter cuniculorum  sp. nov. Campylobacter cuniculorum  (cu.ni.cu.lo 9 rum. L. gen. pl. n. cuniculorum  of rabbits).Cells are spiral, Gram-negative rods, motile, 0.2–0.4  m mwide and 1.9–3.3  m m long, possessing a single flagellum atboth poles. After subculturing on nutrient sheep-bloodagar, colonies are grey–green, flat with rough margins andslightly mucoid-looking; after 72–96 h at 37  u C undermicroaerobic conditions, colonies are smooth,  a -hae-molytic, 1–2 mm in diameter. Colony appearance onmodified-charcoal cefoperazone deoxycholate agar(mCCDA) and cefoperazone, amphotericin B, teicoplaninselective supplement (CAT) is similar to that on nutrientagar but growth on the first medium is slightly restricted.Strictly microaerobic. Able to grow at 37  u C and moststrains grow at 42  u C; no growth at 25  u C or underanaerobic or aerobic conditions. Hydrogen is not requiredfor growth. Oxidase and catalase are produced, but noturease,  c -glutamyltranspeptidase or alkaline phosphatase.Hydrolyses indoxyl acetate but not hippurate, and reducesnitrate but not selenite. Some strains reduce triphenyltetrazolium chloride (TTC) and grow on nutrient agarwithout blood but not on MacConkey agar. No growthoccurs in the presence of 1% (w/v) glycine and 2% (w/v)NaCl and only few strains grow in the presence of 1% (w/v) bile. Most strains are resistant to ( m g per disc) nalidixicacid (30) and cephalothin (30) by disc diffusion test.Strains have been recovered from rabbit caecal contents butpathogenicity is unknown. The G + C content of the typestrain is 32.4 mol%.The type strain is 150B T ( 5 LMG 24588 T 5 CCUG 56289 T ),which was isolated from a rabbit in 2005. Acknowledgements We thank Dr Maria Renzi (Istituto Zooprofilattico Sperimentale dellaLombardia e dell’Emilia Romagna, Bologna) for access to samples of rabbit caecal contents. We would also like to thank Dr Jean Euze´by (E´cole Nationale Ve´te´rinaire, Toulouse, France) for help with namingthe novel species, Professor Roberto Chiocchetti (Department of Veterinary Morphophysiology and Animal Productions, University of Bologna, Italy) for help with the TEM analysis and Professor ValeriaSanguinetti for all the support given. References Bolton, F. J., Wareing, D. R. A., Skirrow, M. B. & Hutchinson, D. N.(1992).  Identification and biotyping of campylobacters. In Identification Methods in Applied and Environmental Microbiology  ,pp. 151–161. Edited by R. G. Board, D. Jones & F. A Skinner. Oxford:Blackwell Scientific. Denis, M., Soumet, C., Rivoal, K., Ermel, G., Blivet, D., Salvat, G. &Colin, P. (1999).  Development of a m-PCR assay for simultaneousidentification of   Campylobacter jejuni   and  C. coli. Lett Appl Microbiol  29 , 406–410. Ezaki, T., Hashimoto, Y. & Yabuuchi, E. (1989).  Fluorometricdeoxyribonucleic acid-deoxyribonucleic acid hybridization in micro-dilution wells as an alternative to membrane filter hybridization inwhich radioisotopes are used to determine genetic relatedness amongbacterial strains.  Int J Syst Bacteriol   39 , 224–229. Foster, G., Holmes, B., Steigerwalt, A. G., Lawson, P. A., Thorne, P.,Byrer, D. E., Ross, H. M., Xerry, J., Thompson, P. M. & Collins, M. D.(2004).  Campylobacter insulaenigrae   sp. nov., isolated from marinemammals.  Int J Syst Evol Microbiol   54 , 2369–2373. Inglis, G. D., Hoar, B. M., Whiteside, D. P. & Morck, D. W. (2007). Campylobacter canadensis   sp. nov., from captive whooping cranes inCanada.  Int J Syst Evol Microbiol   57 , 2636–2644. Jukes, T. H. & Cantor, C. R. (1969).  Evolution of protein molecules. In Mammalian Protein Metabolism , vol. 3, pp. 21–132. Edited by H. N.Munro. New York: Academic Press. Ka ¨ renlampi, R. I., Tolvanen, T. P. & Ha ¨ nninen, M. L. (2004). Phylogenetic analysis and PCR-restriction fragment length poly-morphism identification of   Campylobacter   species based on partial groEL   gene sequences.  J Clin Microbiol   42 , 5731–5738. Korczak, B. M., Stieber, R., Emler, S., Burnens, A. P., Frey, J. &Kuhnert, P. (2006).  Genetic relatedness within the genus  Campylob-acter   inferred from  rpoB   sequences.  Int J Syst Evol Microbiol   56 , 937–945. Lawson, A. J., Linton, D., Stanley, J. & Owen, R. J. (1997).  Polymerasechain reaction detection and speciation of   Campylobacter upsaliensis  and  C. helveticus   in human faeces and comparison with culturetechniques.  J Appl Microbiol   83 , 375–380. Linton, D., Owen, R. J. & Stanley, J. (1996).  Rapid identification by PCR of the genus Campylobacter and of five  Campylobacter   speciesenteropathogenic for man and animals.  Res Microbiol   147 , 707–718. Mesbah, M. & Whitman, W. B. (1989).  Measurement of deoxyguano-sine/thymidine ratios in complex mixtures by high-performanceliquid chromatography for determination of the mole percentageguanine  +  cytosine of DNA.  J Chromatogr   479 , 297–306. On, S. L. & Holmes, B. (1991a).  Effect of inoculum size on thephenotypic characterization of   Campylobacter   species.  J Clin Microbiol  29 , 923–926. On, S. L. & Holmes, B. (1991b).  Reproducibility of tolerance tests thatare useful in the identification of campylobacteria.  J Clin Microbiol   29 ,1785–1788. On, S. L. & Holmes, B. (1992).  Assessment of enzyme detection testsuseful in identification of campylobacteria.  J Clin Microbiol   30 , 746–749. On, S. L., Holmes, B. & Sackin, M. J. (1996).  A probability matrix forthe identification of campylobacters, helicobacters and allied taxa.  J Appl Bacteriol   81 , 425–432. On, S. L. W., Atabay, H. I., Correy, J. E. L., Harrington, C. S. &Vandamme, P. (1998).  Emended description of   Campylobacter sputorum  and revision of its infrasubspecific (biovar) divisions,including  C. sputorum  biovar paraureolyticus, a urease-producingvariant from cattle and humans  Int J Syst Bacteriol   48 , 195–206. R. G. Zanoni and others1670  International Journal of Systematic and Evolutionary Microbiology   59
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