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1 Department of Veterinary Microbiology, Stigbøjlen 4, Royal Danish Veterinary and Agricultural University, 1870 Frederiksberg C, Denmark
2 Institute of Veterinary Bacteriology, University of Bern, Laenggass-Strasse 122, CH-3012 Bern, Switzerland
Correspondence
Henrik Christensen
hech{at}kvl.dk
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession number for the sequences obtained in this study are AY296207–AY296246 and AY314025–AY314043.
Details of strains analysed and sequence accession numbers are available as supplementary material in IJSEM Online.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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was originally proposed to accommodate existing genera and species on the basis of phenotypic and genotypic characteristics (Pohl, 1981) and has subsequently been shown to be monophyletic on the basis of rRNA–DNA hybridization and 16S rRNA gene sequence comparisons (De Ley et al., 1990; Dewhirst et al., 1992). Members of the family have been isolated from mucosal membranes of the respiratory, reproductive and alimentary tracts of healthy as well as diseased vertebrates (Bisgaard, 1993). Eight genera have now been named, accommodating 57 named species. In spite of the naming of five genera during the last decade, the three ‘old’ genera, Haemophilus, Actinobacillus and Pasteurella, still seem to be polyphyletic. The existence of around 40 unnamed taxa is predominantly due to insufficient designation of type strains and lack of characters to separate them from existing named species. Other limitations include the limited number of strains available for some taxa and the lack of DNA–DNA hybridization results, which would permit distinct genotypes to be validated as new candidates for species.
16S rRNA gene sequence comparison has been the most beneficial tool so far to improve the classification of members of the Pasteurellaceae. Ninety-five of the species or species-like taxa have been characterized by 16S rRNA gene sequence analysis. In addition, phylogenetic inference based on 16S rRNA gene sequence comparison has been used for classification at the family level as well as for investigation of particular groups (Dewhirst et al., 1993; Møller et al., 1996; Angen et al., 1999, 2003; Guettler et al., 1999; Foster et al., 2000; Christensen et al., 2004; Olsen et al., 2004).
Phylogenetic trees of the Pasteurellaceae based on maximum-likelihood analysis of 16S rRNA gene sequences have recently been published (Angen et al., 2003; Christensen & Bisgaard, 2003, 2004; Christensen et al., 2003b). To aid in comparison in the present study, such analysis has been included (Fig. 1). The tree was constructed according to Christensen et al. (2003b) and the ‘multiple outgroup’ approach was used to determine the phylogeny of the family. Thirteen monophyletic groups and 13 monotypic taxa were identified by maximum-likelihood analysis of 16S rRNA gene sequences, with reasonably good correspondence to the neighbour-joining tree published by Olsen et al. (2004). The groups are summarized briefly below to allow further comparison to the phylogenetic analysis of housekeeping genes. Whenever possible, the names of the groups of Olsen et al. (2004) have been adopted. The core group of Pasteurella sensu stricto, the Mannheimia, Actinobacillus sensu stricto, Rodent and Parasuis groups were identified as monophyletic. Recently, Histophilus somni was proposed as a new monotypic genus (Angen et al., 2003), and formed a group with the Succinogenes group related to the Seminis group. The Haemophilus and Aphrophilus groups were identified and included within a monophyletic group. The Avian group included taxon 33 of Bisgaard (proposed as Volucribacter; Christensen et al., 2004) in addition to the genus Gallibacterium (Christensen et al., 2003a), avian members of Pasteurella sensu stricto and three unnamed taxa of Bisgaard. The Testudinis group formed the outgroup to which Phocoenobacter uteri and [Haemophilus] parainfluenzae were closely related. The Rossii group was recognized, but left Bisgaard taxon 7 monotypic. The two species [Actinobacillus] scotia and [Actinobacillus] delphinicola formed the group Delphinicola and Pasteurella langaaensis formed the group Langaa with [Pasteurella] caballi. The six remaining taxa, [Haemophilus] ducreyi, [Haemophilus] felis, Lonepinella koalarum, [Pasteurella] bettyae, [Pasteurella] trehalosi and taxon 5 of Bisgaard, could not be allocated to any of the monophyletic groups, whereas Taxon 16 of Bisgaard was found to be closely related to Mannheimia. The major drawback with phylogenetic inference based on 16S rRNA gene sequence comparison is insufficient separation with certain species (Fox et al., 1992; Stackebrandt & Goebel, 1994) despite this being the most valuable unit for classification. Analysis of the so-called housekeeping genes has been suggested to avoid this problem, which will also base phylogenetic inference on a number of genes. These genes have been selected with regard to properties suitable for phylogenetic inference, such as evolutionary conservation and low selection pressure.
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; Petersen et al., 2001; Angen et al., 2003; Korczak et al., 2004; Nørskov-Lauritsen et al., 2004). At the domain level, informational genes branched more deeply than operational ones (Rivera et al., 1998; Garcia-Vallvé et al., 2000). For this reason, both informational and operational genes, both referred to as housekeeping genes, were selected for evaluation of the consistency of 16S rRNA gene-based phylogeny in the present investigation. The gene atpD encodes the 
-subunit of the ATP synthase and has been used for phylogenetic investigation of the domain Bacteria and the genus Salmonella (Ludwig et al., 1993; Christensen & Olsen, 1998). The infB gene encodes the translation initiation factor 2, which is essential for the initiation of protein synthesis in prokaryotes (Laalami et al., 1991). The region compared encodes some of the most conserved and essential parts of the gene, including the G-domain and the ribosome-binding sites (March & Inouye, 1985). DNA sequence comparison of infB has been used for phylogenetic investigation of the Enterobacteriaceae (Hedegaard et al., 1999), the genus Haemophilus (Hedegaard et al., 2001) and members of Actinobacillus (Nørskov-Lauritsen et al., 2004). DNA sequence comparison of rpoB, encoding the -subunit of RNA polymerase, was used for classification by Mollet et al. (1997), used for the classification of Histophilus somni (Angen et al., 2003) and recently for phylogenetic analysis of the Pasteurellaceae (Korczak et al., 2004). The gene codons 509–680 (according to the Escherichia coli numbering) were chosen to represent a variable part of the gene (Klenk & Zillig, 1994; Mollet et al., 1997). The genes atpD, infB and rpoB chosen for the present study are genetically unlinked, as indicated by the fact that they are dispersed over at least 14 kbp on the genomic sequences of Haemophilus influenzae and Pasteurella multocida available from public databases (http://www.ncbi.nlm.nih.gov). The aim of the study was to compare phylogenies of housekeeping gene sequences with the 16S rRNA gene sequence-based phylogeny in order to improve the classification of the bacterial family Pasteurellaceae and to obtain information about the evolutionary relationships of its members.
DNA sequencing and phylogenetic analysis
Sequencing of atpD was performed according to Petersen et al. (2001) with modification of the oligonucleotide primers in order to sequence the different taxa investigated (Table 1). The sequencing of a fragment of the infB gene was performed as reported by Nørskov-Lauritsen et al. (2004) with modified oligonucleotide primers (Table 1). The partial rpoB sequence was determined according to Korczak et al. (2004) using oligonucleotide primers listed in Table 1. Bacteria were cultured overnight in brain heart infusion broth (Difco) or blood agar base supplemented with 5 % bovine blood and DNA was extracted or colonies lysed by boiling and used directly for PCR. PCR amplification of atpD and infB was performed according to the standard conditions of 35 cycles of 30 s denaturation at 94 °C, 120 s annealing at 55 °C and 60 s extension at 72 °C. PCR amplification of rpoB was performed as described by Korczak et al. (2004) with 35 cycles of 30 s denaturation at 94 °C, 30 s annealing at 54 °C and 30 s extension at 72 °C. PCR-amplified fragments were purified on Microspin columns (Amersham Pharmacia Biotech) and cycle-sequenced (Thermo Sequenase fluorescent labelled primer cycle sequencing kit; Amersham Pharmacia Biotech) on an ALF Sequencer (Pharmacia Biotech) using fluorescein-labelled primers for atpD and infB or cycle-sequenced on an ABI3100 with the dRhodamine kit according to protocols described in the Applied Biosystems Chemistry Guide for rpoB.
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Sequences were aligned with PILEUP (Wisconsin sequence analysis package, GCG). Positions with gaps in the alignments were excluded in the phylogenetic analysis. In the protein alignment of atpD, one amino acid insertion was found in [Actinobacillus] rossii, [Actinobacillus] succinogenes, [Pasteurella] caballi and taxon 14 of Bisgaard compared with the other taxa investigated. With the infB protein alignment, a single amino acid was found to be deleted in sequences of Pasteurella multocida, [A.] succinogenes, L. koalarum and taxon 7 of Bisgaard compared with the other taxa investigated. With the rpoB protein alignment, a single amino acid was deleted in Mannheimia compared with the other taxa investigated. Phylogenetic analysis was performed by PROTML as included in MOLPHY version 2.3b3 (http://ftp.ism.ac.jp:8000/ISMLIB/MOLPHY) using the PAM substitution matrix. Parsimony analysis was performed by PROTPARS with standard settings and bootstrap analysis as included with PHYLIP (Felsenstein, 1995). Neighbour-joining analysis was performed with NEIGHBOR after construction of the distance matrix with PROTDIST using the pam substitution matrix (PHYLIP). To allow consensus comparison between phylogenetic trees derived from housekeeping gene and 16S rRNA gene sequences, new 16S rRNA gene alignments were constructed that included exactly the taxa analysed in the respective housekeeping gene sequence alignments. Majority rule consensus comparisons between housekeeping gene-derived and 16S rRNA gene sequence-based trees were performed by CONSENSE (PHYLIP).
The phylogeny obtained by alignment of the region 12–428 (E. coli numbering) of the deduced atpD protein sequences corresponded to the 16S rRNA gene phylogeny in that the Mannheimia, core Pasteurella sensu stricto, Rodent and Gallibacterium groups could be recognized. In addition, the two members of the Haemophilus and Aphrophilus groups formed a monophyletic unit (Fig. 2a, Table 2). The inclusion of [Haemophilus] ducreyi with the taxa of Actinobacillus sensu stricto and the close relationship of this group to [Haemophilus] parasuis, [Pasteurella] trehalosi and Mannheimia within a large monophyletic group supported by high bootstrap values was unrecognized by 16S rRNA gene phylogenetic analysis (Fig. 2a, Table 2).
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) and between Gallibacterium and the two strains of taxon 14 of Bisgaard were not recognized in the 16S rRNA gene-derived phylogeny (Fig. 2b
, Table 2). As with the atpD-derived phylogeny, a monophyletic group of members of Mannheimia, [Haemophilus] ducreyi, Actinobacillus sensu stricto, [Haemophilus] parasuis and [Pasteurella] trehalosi was also recognized (Fig. 2b).
Phylogenetic analysis of the alignment of the region 509–680 (E. coli numbering) of the deduced rpoB protein sequence allowed recognition of the core Pasteurella sensu stricto, Gallibacterium, Actinobacillus sensu stricto and Mannheimia 16S rRNA gene groups, whereas members of Haemophilus–Aphrophilus, Rodent and Avian groups did not form monophyletic units (Fig. 2c, Table 2). Identical protein sequences were observed for the two taxa of Mannheimia, the two taxa of Gallibacterium and for [Pasteurella] pneumotropica and taxon 17 of Bisgaard. The 16S rRNA gene monophyletic groups recognized by housekeeping gene sequence analysis were recognized by all three phylogenetic methods (Figs 2a–c, Table 2); however, the recognition of these groups should be taken with caution since some of the groups were represented by only a few taxa (Fig. 2). Further investigation is necessary in order to document fully the monophyly of these groups.
Comparison of the deduced protein sequences of all three housekeeping genes atpD, infB and rpoB (end-to-end) was possible for 23 taxa with 707 positions. The 16S rRNA gene groups Gallibacterium, Actinobacillus sensu stricto and Rodent were recognized (Fig. 3). Strong support was found for the group with Mannheimia, Actinobacillus sensu stricto, [Haemophilus] ducreyi and [Pasteurella] trehalosi. The two members of the Rodent group and Haemophilus influenzae were closely related to this group. In addition, Gallibacterium and taxon 14 of Bisgaard formed a group. Pairwise consensus comparisons between the three housekeeping gene-derived trees showed only 19 % (atpD–infB, atpD–rpoB) to 29 % (infB–rpoB) of all nodes to be conserved. In comparison, nodes supported by all three phylogenetic methods with bootstrap values higher than 50 % accounted for around 40 % of all nodes in the trees shown in Figs 2 and 3. In all three pairs (atpD–infB, atpD–rpoB, infB–rpoB), the two taxa of Gallibacterium, [Pasteurella] pneumotropica and taxon 17 of Bisgaard and [Haemophilus] ducreyi and A. pleuropneumoniae formed common nodes. When conserved nodes were counted between the housekeeping gene and 16S rRNA gene trees in Fig. 2(a–c), similarly low percentages of conserved nodes were observed (19–26 %). Based on these approximate consensus comparisons, the congruence between individual housekeeping gene trees was no better than between these and the 16S rRNA gene tree.
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). The Haemophilus and Aphrophilus groups were confirmed by partial infB sequence comparison, except for the inclusion of [Haemophilus] parainfluenzae (see also Hedegaard et al., 2001) (Table 2).
The 16S rRNA gene groups Rodent and Avian were only occasionally recognized by housekeeping gene-derived phylogenetic analysis (Table 2). The Histophilus–Succinogenes and Histophilus–Succinogenes–Seminis groups were never determined by housekeeping gene sequence-derived phylogenies. The 16S rRNA gene groups Seminis, Rossii, Langaa, Capsulatus, Parasuis, Delphinicola and Testudinis were only represented by one taxon in the housekeeping gene analysis and, therefore, their monophyly could not be tested. In addition, housekeeping gene sequences were not available for the monotypic taxa Phocoenobacter uteri, [Actinobacillus] minor, taxon 16 of Bisgaard, [Haemophilus] haemoglobinophilus and [Haemophilus] felis. Further investigation is needed to justify the phylogenetic relationship of these taxa based on housekeeping gene sequence comparison.
The likelihood ratio test was used to test whether alternative topologies were supported by significantly high logarithms (ln) of likelihood values (Huelsenbeck & Chandall, 1997). The null distribution of the likelihood ratio was approximated with an 
2 distribution. The 2 test supplied with the fastDNAmL program (Olsen et al., 1994) was used. Given that the same taxa are compared, it is therefore possible to test statistically the difference between phylogenetic trees by the likelihood ratio test. To test the 16S rRNA gene-derived phylogenies against housekeeping gene phylogenies, new 16S rRNA gene alignments were constructed, which included only the taxa analysed by housekeeping gene sequence analysis. The 16S rRNA gene-derived phylogeny, based on maximum-likelihood analysis, was chosen as H0 and tested against the topologies obtained by phylogenetic analysis of the deduced protein sequences of housekeeping genes. For all three housekeeping genes, including the tree of all three genes, significant differences were obtained between 16S rRNA gene- and housekeeping gene-derived phylogenies (data not shown). Classification based on 16S rRNA gene sequences has provided the background for modern prokaryotic systematics (Woese, 1987; Garrity & Holt, 2001; Ludwig & Klenk, 2001) and congruence is expected when other well-conserved genes are used for phylogenetic analysis. In the present comparison, members of Pasteurellaceae that were recognized based on housekeeping genes showed congruence with the 16S rRNA gene-derived groups. However, new groups could also be recognized to be conserved between the different housekeeping genes, indicating different evolutions of the 16S rRNA gene and housekeeping genes. Such a lack of congruence has been explained by higher variation and relatively fewer informative positions of the housekeeping gene sequences compared with 16S rRNA gene sequences, resulting in lower phylogenetic resolution by housekeeping gene analysis (Ludwig & Klenk, 2001). The phylogenetic resolution in this sense is defined in relation to informational content, since resolution in relation to the population level in general seems to be higher with the housekeeping genes compared with the 16S rRNA gene. The small number of taxa analysed for housekeeping genes in the present study and the short partial sequences available for rpoB and infB are also expected to result in a lower degree of phylogenetic resolution compared with the 16S rRNA gene. Lateral gene transfer and/or duplication of housekeeping gene sequences has also been suggested as a possible reason for lack of congruence (Doolittle, 1999; Ludwig & Klenk, 2001). The possibility of different rates of evolution due to different selection forces on the various genes also needs to be considered. Some or all of these factors (short partial sequences compared, low informational content, lateral gene transfer, different rates of evolution) probably also account for the different phylogenies determined with each of the housekeeping genes.
It was surprising to observe the conservation of members of Mannheimia, Actinobacillus sensu stricto, [Haemophilus] ducreyi, [Pasteurella] trehalosi and [Haemophilus] parasuis within a monophyletic group by housekeeping gene analysis. With the exception of [Haemophilus] ducreyi and a few species of Actinobacillus sensu stricto and Mannheimia, these taxa are mainly associated with artiodactyls (animals with paired hooves), and RTX-type toxins have been found in three of them (Mannheimia, Actinobacillus sensu stricto and [Pasteurella] trehalosi; Frey & Kuhnert, 2002). The housekeeping gene-derived phylogeny justifies the classification of Mannheimia and Gallibacterium. Further support for groups like Actinobacillus sensu stricto, the core group of Pasteurella sensu stricto (Olsen et al., 2004) and the split of the Avian group into different genera such as Gallibacterium and the new genus proposed as Volucribacter (Christensen et al., 2004) was also obtained. The split of the Somnus group was previously justified with formation of the new monotypic genus Histophilus (Angen et al., 2003).
The limitations in order to achieve congruence of housekeeping gene- and 16S rRNA gene-derived phylogenies question the appropriateness of further investigations with the deeper branchings. The 16S rRNA gene-derived phylogeny showed good congruence with whole genome-based phylogeny (Henz et al., 2003) and might still be best suited for the deeper branching levels. Using gyrB sequence-based phylogenetic analysis with the Enterobacteriaceae, congruence was obtained at the species level but not at deeper levels (Dauga, 2002). Comparisons of housekeeping genes are probably best suited for separation and analysis at the species and genus level and could serve as an alternative to DNA–DNA hybridizations (Zeigler, 2003). The analysis of housekeeping genes is a promising approach capable of contributing to the ongoing revision and improvement of the taxonomy of the Pasteurellaceae. Further investigations should focus on analysis of the whole gene sequences of infB and rpoB in order to confirm the regions most suitable for phylogenetic analysis. Analysis of more housekeeping genes from both the informational and the operational groups should also be performed.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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M. Martens, M. Delaere, R. Coopman, P. De Vos, M. Gillis, and A. Willems Multilocus sequence analysis of Ensifer and related taxa Int J Syst Evol Microbiol, March 1, 2007; 57(3): 489 - 503. [Abstract] [Full Text] [PDF]
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H. Christensen, P. Kuhnert, H.-J. Busse, W. C. Frederiksen, and M. Bisgaard Proposed minimal standards for the description of genera, species and subspecies of the Pasteurellaceae Int J Syst Evol Microbiol, January 1, 2007; 57(1): 166 - 178. [Abstract] [Full Text] [PDF]
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 A. Olvera, M. Cerda-Cuellar, and V. Aragon Study of the population structure of Haemophilus parasuis by multilocus sequence typing Microbiology, December 1, 2006; 152(12): 3683 - 3690. [Abstract] [Full Text] [PDF]
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 J. Gioia, X. Qin, H. Jiang, K. Clinkenbeard, R. Lo, Y. Liu, G. E. Fox, S. Yerrapragada, M. P. McLeod, T. Z. McNeill, et al. The Genome Sequence of Mannheimia haemolytica A1: Insights into Virulence, Natural Competence, and Pasteurellaceae Phylogeny. J. Bacteriol., October 1, 2006; 188(20): 7257 - 7266. [Abstract] [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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B. M. Korczak, R. Stieber, S. Emler, A. P. Burnens, J. Frey, and P. Kuhnert Genetic relatedness within the genus Campylobacter inferred from rpoB sequences. Int J Syst Evol Microbiol, May 1, 2006; 56(Pt 5): 937 - 945. [Abstract] [Full Text] [PDF]
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S. M. Naser, F. L. Thompson, B. Hoste, D. Gevers, P. Dawyndt, M. Vancanneyt, and J. Swings Application of multilocus sequence analysis (MLSA) for rapid identification of Enterococcus species based on rpoA and pheS genes Microbiology, July 1, 2005; 151(7): 2141 - 2150. [Abstract] [Full Text] [PDF]
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 A.-L. Gautier, D. Dubois, F. Escande, J.-L. Avril, P. Trieu-Cuot, and O. Gaillot Rapid and Accurate Identification of Human Isolates of Pasteurella and Related Species by Sequencing the sodA Gene J. Clin. Microbiol., May 1, 2005; 43(5): 2307 - 2314. [Abstract] [Full Text] [PDF]
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H. Christensen, M. Bisgaard, O. Angen, W. Frederiksen, and J. E. Olsen Characterization of Sucrose-Negative Pasteurella multocida Variants, Including Isolates from Large-Cat Bite Wounds J. Clin. Microbiol., January 1, 2005; 43(1): 259 - 270. [Abstract] [Full Text] [PDF]
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