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ena M. Korczak1
1 Institute of Veterinary Bacteriology, University of Bern, CH-3012 Bern, Switzerland
2 SmartGene, Zug, Switzerland
Correspondence
Peter Kuhnert
peter.kuhnert{at}vbi.unibe.ch
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Published online ahead of print on 23 December 2005 as DOI 10.1099/ijs.0.64109-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA and rpoB gene sequences of the Campylobacter species determined in this study are shown in Table 1
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Distance matrices for the 16S rRNA and rpoB gene sequences for all the strains investigated in this study are available as Supplementary Tables S1 and S2 in IJSEM Online.
Present address: MCL Medical Laboratories, CH-3186 Düdingen, Switzerland. 
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). These taxa had formerly been classified as Vibrio species. In 1973, M. Véron and R. Chatelain included several misclassified Vibrio in the distinct Campylobacter genus based on serological, biochemical and DNA–DNA hybridization investigations (On, 2001). Since then, the taxonomy of the genus has changed dramatically. At present, it comprises 17 species with validly published names and six recognized subspecies (On, 2001; Foster et al., 2004). In addition, strains belonging to C. sputorum are divided into three biovars, sputorum, fecalis and paraureolyticus, on the basis of their ability to produce catalase or urease (On et al., 1998; Vandamme & On, 2001).
In general, members of the genus Campylobacter colonize the mucosal surfaces of the intestinal tract, oral cavity or urogenital tract of healthy, as well as diseased, humans and animals, especially birds. Several species may act as pathogens, causing disease in both human and animal hosts. Twelve of the 17 Campylobacter species are associated with human diseases. Campylobacter jejuni and Campylobacter coli are particularly frequent causative agents of human bacterial intestinal disorders worldwide (Skirrow, 1994). There have also been reported cases of diarrhoea in man caused by Campylobacter upsaliensis and Campylobacter lari, but the frequency of these infections is very low (Bourke et al., 1998; Van Doorn et al., 1998). Occasionally, Campylobacter species are implicated as causative agents of pericarditis, myocarditis and Guillain–Barré Syndrome (Kuwabara, 2004; Uzoigwe, 2005). The most important animal diseases are caused by Campylobacter fetus subsp. fetus, which is associated with abortion in cattle and sheep, and Campylobacter fetus subsp. venerealis, associated with infectious infertility in cattle (Skirrow, 1994).
Taxonomic classification and identification of Campylobacter species by phenotypic methods is often difficult and time-consuming because of their fastidious growth, low biochemical activity and the variability of results (Moore & Madden, 2003). Therefore, several genotypic methods have been used for identification and taxonomic investigations within the genus Campylobacter (On, 1996). A large DNA–rRNA hybridization study on the Campylobacter complex was carried out by Vandamme et al. (1991) and provided a basis for the revision of its taxonomy. Numerical analysis of amplified fragment length polymorphism (AFLP) profiles has been used for the investigation of the genetic relationships within the genus Campylobacter (On & Harrington, 2000). In other studies, 16S rRNA and 23S rRNA gene sequence-based phylogenies within the genus were analysed (Van Camp et al., 1993; Harrington & On, 1999; Gorkiewicz et al., 2003). Kärenlampi et al. (2004) performed phylogenetic analysis within the genus Campylobacter using partial sequences of the heat shock protein gene groEL. Most recently, the genetic relatedness between C. jejuni and C. coli was investigated by multilocus sequence typing (MLST) of certain housekeeping genes (Dingle et al., 2005; Miller et al., 2005).
Analysis of the sequences of rRNA genes has deeply modified the taxonomy and identification of many groups of bacteria. However, this tool has limitations due to the low polymorphism of 16S rRNA gene sequence data and high intraspecies diversity in some cases (Harrington & On, 1999; On, 2001). Therefore, additional genetic tools are needed to clarify the taxonomy of the genus Campylobacter and, at the same time, to enable the genetic identification of bacteria belonging to this genus. Analysis of the rpoB gene encoding the beta-subunit of RNA polymerase has greatly supported the identification and the elaboration of genetic relationships in several groups of bacteria (Mollet et al., 1997; Kim et al., 2003; Korczak et al., 2004; Christensen et al., 2004; Drancourt et al., 2004). Recently, the rpoB gene has also been used to support the description of novel taxa (Angen et al., 2003; Kuhnert et al., 2004).
In this study, we used a universal amplification and sequencing approach for the rpoB gene to investigate genetic relatedness within the genus Campylobacter.
Sequence comparison analysis was used to select the primers CamrpoB-L, 5'-CCAATTTATGGATCAAAC-3', and RpoB-R, 5'-GTTGCATGTTNGNACCCAT-3', which enabled the amplification of a 524 bp fragment from the rpoB gene of most Campylobacter species. The PCR product corresponded to region 1536–2059 bp of the Escherichia coli rpoB gene. For Campylobacter helveticus, Campylobacter curvus and Campylobacter lanienae, the primer CamrpoB-L1, 5'-GGKCARCTYTCKCAATTYATGG-3', was required. In this case, the gene fragment generated (535 bp) corresponded to the 1525–2059 bp position of the E. coli rpoB gene. The three primers could be combined in the same PCR at an annealing temperature of 54 °C without interfering with each other. Amplification was carried out in 50 µl volumes containing 20 pmol of each primer, 1 mM dNTP, 1x reaction buffer B (supplied with FIREPol DNA polymerase), 2.5 mM MgCl2 and 2.5 U FIREPol polymerase (Solis BioDyne). Approximately 100 ng template was added as genomic DNA or as lysate. Cycling conditions and purification steps were performed as previously described (Korczak et al., 2004). Finally, about 30 ng purified PCR product was used for sequencing with the BigDye Terminator cycle sequencing kit (Applied Biosystems) using either CamrpoB-L, CamrpoB-L1 or RpoB-R as sequencing primers. Sequences were analysed on an ABI Prism 3100 Genetic Analyzer (Applied Biosystems) and then edited using SEQUENCHER software (GeneCodes). The three primers used for amplifying and sequencing the partial rpoB gene of Campylobacter species were found to be universal within this genus, since all strains that have been analysed so far have yielded amplification products.
In order to confirm species identity and improve the available sequences (resolving unknown bases or generating longer sequence fragments), the 16S rRNA gene sequence of all the Campylobacter species was determined in parallel according to a previously described method (Kuhnert et al., 2002). PCR and sequencing resulted in a 1.3–1.5 kb fragment, depending on the presence of an intervening sequence. All sequences obtained were deposited in databases for 16S rRNA and rpoB gene sequences using the SmartGene IDNS platform (www.idns-smartgene.com), which allows parallel sequence comparisons of both target genes. At the same time, all rpoB sequences and improved 16S rRNA gene sequences were deposited in GenBank. Campylobacter type strains and reference strains from bacterial culture collections were used in this study. For some species where only a few strains were available, some field strains were also included. These had been identified previously by the Swiss National Centre for Enteropathogenic Bacteria using standard phenotyping methods, and the original species designation was used in this study. The strains used in this study, their origin and the GenBank accession numbers of the corresponding rpoB and 16S rRNA gene sequences are given in Table 1. Distance matrices using Jukes–Cantor correction and phylogenetic analysis using neighbour-joining tree building were performed with the BioNumerics program version 4.0 (Applied Maths).
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). Discrepancies in branching and clustering are most probably due to horizontal gene transfer, which is also known to occur with house-keeping genes such as 16S rRNA and rpoB (Ko et al., 2002; Acinas et al., 2004). The rpoB gene was found to provide a better resolution for Campylobacter species, with lower interspecies sequence similarities, ranging from 56.4 to 98.8 %, compared with those for the 16S rRNA gene (86.8–100 %). Thus, Campylobacter species can be better differentiated by using the rpoB gene than the 16S rRNA gene. This is also visible in Figs 1 and 2, which have the same scale bar, thereby showing clearly the higher resolution obtained with rpoB gene sequences. The distance matrices of the 16S rRNA and rpoB gene sequences for all the strains investigated in this study are available as Supplementary Tables S1 and S2 in IJSEM Online.
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; Nicholson & Patton, 1995). Many molecular tests that are useful for the differentiation of these two species have been developed, e.g. multiplex PCR or MLST (Cloak & Fratamico, 2002; Dedieu et al., 2004; Dingle et al., 2005; Nayak et al., 2005; Miller et al., 2005). In this study, it was impossible to separate C. jejuni and C. coli strains based on the 16S rRNA gene sequence (Fig. 1). Several C. jejuni and C. coli strains shared identical 16S rRNA gene sequences and nearly all the investigated strains of these taxa were mixed in a common cluster. Only the type strain of C. coli, LMG 6440T, formed a separate branch (Fig. 1) as previously observed by Gorkiewicz et al. (2003). In contrast, the rpoB gene is strongly conserved within most C. coli strains, which shared 100 % sequence identity with C. coli LMG 6440T. The location of the C. coli type strain in the rpoB tree on the same branch together with other C. coli strains is also seen with a tree based on groEL gene sequences (Kärenlampi et al., 2004). However, the still low rpoB sequence divergence between C. coli and C. jejuni strains, ranging from only 1.2 % to 3.8 %, makes it difficult to discriminate between the two species. A further discrepancy in the C. coli cluster in the 16S rRNA gene-based tree was found for strains NZ 2695-95 and NZ 1905-94, which formed a distinct cluster of their own in the rpoB-based tree (Fig. 2). Pairwise sequence comparison of these strains with C. coli LMG 6440T revealed rpoB gene sequence similarities of only 83.6 % and 82.8 %, respectively. This suggests that strains NZ 2695-95 and NZ 1905-94 may be genetically atypical C. coli-like strains or represent a novel species distinct from C. coli. Between these two strains, the rpoB sequence divergence was 6.2 %, indicating further heterogeneity within putative C. coli-like strains. Further investigation of the relatedness of these two strains, including genotypic and phenotypic analysis, is necessary.
The type strain of C. lari, NCTC 11352T, and the recently described novel species Campylobacter insulaenigrae displayed high 16S rRNA gene sequence similarity and both species are located within the C. jejuni/C. coli cluster. In contrast, in the rpoB tree, C. lari and C. insulaenigrae are clearly separated from other members of the genus Campylobacter and are also clearly separated from each other. This clustering based on rpoB sequences is supported by DNA–DNA hybridization results, which showed a close genetic relationship between C. insulaenigrae and C. lari and a significantly lower genetic relationship between C. insulaenigrae and C. jejuni (Foster et al., 2004).
It is known that C. lari is a phenotypically and genetically heterogeneous species. In a recent study by Duim et al. (2004), several groups were discerned within this species. A previous study based on numerical analysis of AFLP profiles demonstrated that classical urease-negative and urease-positive strains form closely related, but distinct, clusters (On & Harrington, 2000). Our results confirm that C. lari is a heterogeneous group as demonstrated in both the rpoB and 16S rRNA gene-derived trees. The C. lari cluster is split into two branches. The first branch is formed by the urease-negative and nalidixic acid-resistant type strain NCTC 11352T and the clinical isolate NZ 145-95. The second branch includes the two urease-positive and nalidixic acid-sensitive strains (NZ 3541-96 and NZ 3663-96) which share 100 % sequence similarity within the rpoB and 16S rRNA gene fragments. Their high rpoB sequence divergence from the type strain of C. lari (11.8 %) once more confirms the genetic diversity of this species. Sequencing of the rpoB gene therefore appears to be a promising tool for the differentiation of C. lari strains.
In both the rpoB and 16S rRNA gene-derived trees, C. upsaliensis and C. helveticus clustered in a similar way to that described for the phylogeny of the genus based on groEL gene sequences (Kärenlampi et al., 2004). A common cluster can be observed which consists of two clearly separated branches formed by C. upsaliensis and C. helveticus strains. It confirms their notable DNA similarity (Stanley et al., 1992). Moreover, C. helveticus appears to be a very genetically homogeneous group, reflected in a 100 % sequence match in rpoB genes between all investigated strains.
C. fetus and Campylobacter hyointestinalis subsp. hyointestinalis formed one cluster in both the rpoB tree and the 16S rRNA gene tree. The DNA–DNA hybridization study performed by Roop et al. (1984) also revealed some DNA similarity between these species. The two species are phenotypically and genotypically similar, but associated with different diseases (Skirrow, 1994; On, 2001). In the 16S rRNA gene sequence-based tree, C. hyointestinalis subsp. lawsonii clustered with C. lanienae and was clearly distinct from C. hyointestinalis subsp. hyointestinalis. Harrington et al. (1999) have already described wide 16S rRNA gene sequence diversity (1.0–4.3 %) between members of the two C. hyointestinalis subspecies. In contrast, in the rpoB gene based tree, both subspecies of C. hyointestinalis belong to the same subcluster, which is coupled to the branch formed by C. fetus strains. This location in the rpoB tree confirms the close phylogenetic relationship between these two subspecies and strongly supports the DNA–DNA hybridization results and phylogeny based on the groEL gene (On et al., 1995; Kärenlampi et al., 2004). In general, the rpoB and groEL genes possess similar characteristics concerning genetic relatedness within the genus Campylobacter. Both targets achieved nearly the same level of resolution of Campylobacter species. Moreover, a comparison of the tree topologies found with both gene targets shows similar clustering of species within the genus Campylobacter. However, the groEL gene tree is less extensive as it does not show all the recognized species and analyses fewer representative strains for the species that are included.
C. lanienae settles on a distinct branch, joined to the C. fetus/C. hyointestinalis cluster, in both the rpoB and 16S rRNA gene trees.
Distinguishing between C. fetus subsp. fetus and C. fetus subsp. venerealis poses a special problem for veterinary laboratories. Although several phenotypic and genotypic methods are useful for discriminating these two subspecies (Hum et al., 1997; On & Harrington, 2001), the final determination is based mainly on the different pathogenic associations of the subspecies. C. fetus subsp. fetus causes abortion in cattle and sheep, whereas C. fetus subsp. venerealis causes infectious infertility in cattle (Skirrow, 1994). Unfortunately, the resolution of the rpoB gene, as is the case for the 16S rRNA gene, does not allow the differentiation of C. fetus subsp. fetus from C. fetus subsp. venerealis.
The species C. sputorum and Campylobacter hominis clustered together in the 16S rRNA gene-based tree, but formed two clearly distant branches. This topology is similar to that found for the rpoB gene tree in this study, but is different from that shown in the 16S rRNA gene tree of the genus as described by Gorkiewicz et al. (2003).
In both the rpoB and 16S rRNA gene-derived trees, Campylobacter mucosalis and Campylobacter concisus showed some genetic relationship, in agreement with DNA hybridization results (Roop et al., 1985).
In the 16S rRNA gene tree, C. curvus clustered with C. concisus, whereas in the rpoB gene tree C. curvus is on a separate branch close to Campylobacter showae, Campylobacter gracilis and Campylobacter rectus. All four species have been isolated from the gingival crevices of healthy individuals and patients with periodontal diseases. In the 16S rRNA gene tree of Gorkiewicz et al. (2003), C. curvus showed the same phylogenetic position as observed in the rpoB tree. The similar position and clustering of C. rectus and C. showae in both trees demonstrates a close phylogenetic relationship that has been observed previously (Gorkiewicz et al., 2003). However, the heterogeneity of the rpoB sequences between the two C. showae strains is remarkable. The two strains showed a close relationship in their 16S rRNA gene sequences, sharing 99.8 % sequence identity, but their rpoB gene sequence similarity was only 92 %.
In certain Campylobacter species, intervening sequences (IVS) in the 16S rRNA gene have been described, particularly for C. sputorum, C. curvus, C. rectus, C. helveticus and C. hyointestinalis (Linton et al., 1994; Etoh et al., 1998). When compared with the 16S rRNA gene sequence of the type species C. fetus (GenBank accession no. DQ174127), all C. sputorum strains analysed in this study showed an IVS of 227–229 bp. In the C. curvus type strain, an IVS of 136 bp was present. Two of the four C. rectus strains investigated, CCUG 11640 and CCUG 27948, contained an IVS of 189 bp when compared with the other two C. rectus strains.
In conclusion, the rpoB gene has greater resolution than the 16S rRNA gene sequence for the genus Campylobacter. The rpoB resolution is sufficient for the differentiation of very closely related species as well as of most subspecies. However, it is probably not possible to separate C. coli and C. jejuni based on rpoB gene sequences. A separate study including a large number of C. coli and C. jejuni strains could help to clarify whether the high rpoB gene sequence conservation seen with C. coli strains might be useful for the differentiation of this species from C. jejuni. Generally, the rpoB gene sequence better reflects DNA–DNA hybridization results than the 16S rRNA gene sequence, as previously observed for the family Pasteurellaceae (Korczak et al., 2004). Therefore, the rpoB gene might be less prone to horizontal gene transfer and the partial rpoB gene sequence of 530 bp may better reflect the phylogeny of the genus Campylobacter (and eventually others) than does the 16S rRNA gene sequence. The rpoB gene sequence might be particularly useful for diagnostic purposes when sequencing a short fragment could give a clear-cut result.
The universally applicable amplification and sequencing approach for partial rpoB gene sequence determination that was devised in this study provides a powerful tool for DNA sequence-based identification of members of the genus Campylobacter.
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 D. J. Wilson, E. Gabriel, A. J.H. Leatherbarrow, J. Cheesbrough, S. Gee, E. Bolton, A. Fox, C. A. Hart, P. J. Diggle, and P. Fearnhead Rapid Evolution and the Importance of Recombination to the Gastroenteric Pathogen Campylobacter jejuni Mol. Biol. Evol., February 1, 2009; 26(2): 385 - 397. [Abstract] [Full Text] [PDF]
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T. Adekambi, T. M. Shinnick, D. Raoult, and M. Drancourt Complete rpoB gene sequencing as a suitable supplement to DNA-DNA hybridization for bacterial species and genus delineation Int J Syst Evol Microbiol, August 1, 2008; 58(8): 1807 - 1814. [Abstract] [Full Text] [PDF]
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 S. Kawasaki, P. M. Fratamico, I. V. Wesley, and S. Kawamoto Species-Specific Identification of Campylobacters by PCR-Restriction Fragment Length Polymorphism and PCR Targeting of the Gyrase B Gene Appl. Envir. Microbiol., April 15, 2008; 74(8): 2529 - 2533. [Abstract] [Full Text] [PDF]
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 S. Albini, B. M. Korczak, C. Abril, D. Hussy, S. Limat, V. Gerber, M. Hermann, B. Howald, and R. Miserez Mandibular lymphadenopathy caused by Actinomyces denticolens mimicking strangles in three horses Vet Rec., February 2, 2008; 162(5): 158 - 159. [Full Text] [PDF]
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G. D. Inglis, B. M. Hoar, D. P. Whiteside, and D. W. Morck Campylobacter canadensis sp. nov., from captive whooping cranes in Canada Int J Syst Evol Microbiol, November 1, 2007; 57(11): 2636 - 2644. [Abstract] [Full Text] [PDF]
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P. Kuhnert, B. M. Korczak, H. Christensen, and M. Bisgaard Emended description of Actinobacillus capsulatus Arseculeratne 1962, 38AL Int J Syst Evol Microbiol, March 1, 2007; 57(3): 625 - 632. [Abstract] [Full Text] [PDF]
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M. Kupfer, P. Kuhnert, B. M. Korczak, R. Peduzzi, and A. Demarta Genetic relationships of Aeromonas strains inferred from 16S rRNA, gyrB and rpoB gene sequences Int J Syst Evol Microbiol, December 1, 2006; 56(12): 2743 - 2751. [Abstract] [Full Text] [PDF]
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 U. Reischl Melting of the Ribosomal RNA Gene Reveals Bacterial Species Identity: A Step toward a New Rapid Test in Clinical Microbiology. Clin. Chem., November 1, 2006; 52(11): 1985 - 1987. [Full Text] [PDF]
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 P. Kuhnert and B. M. Korczak 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, September 1, 2006; 152(Pt 9): 2537 - 2548. [Abstract] [Full Text] [PDF]
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