International Journal of Systematic and Evolutionary Microbiology (2012), 62, 1396–1401
DOI 10.1099/ijs.0.035246-0
Classification of Pasteurella species B as
Pasteurella oralis sp. nov.
Henrik Christensen,1 Mads F. Bertelsen,1,2 Anders Miki Bojesen1
and Magne Bisgaard1
Correspondence
Henrik Christensen
[email protected]
1
Department of Veterinary Disease Biology, Faculty of Life Sciences, University of Copenhagen,
DK-1870 Frederiksberg C, Denmark
2
Center for Zoo and Wild Animal Health, Copenhagen Zoo, DK-2000 Frederiksberg, Denmark
Pasteurella species B has so far only been reported from the oral cavity of dogs, cats and a ferret.
In the present study, information from 15 recent isolates from different sources, including African
hedgehogs (Atelerix albiventris), banded mongoose (Mungos mungo), Moholi bushbabies
(Galago moholi) and pneumonia of a cat, were compared to five strains investigated previously
from bite wounds in humans inflicted by a cat and dog and from gingiva of a cat. rpoB gene
sequence comparison showed that 17 isolates, including the reference strain (CCUG 19794T),
had identical sequences, whereas two were closely related and demonstrated 97.9 and 99.6 %
similarity to strain CCUG 19794T, respectively; the type strain of Pasteurella stomatis was the
most closely related strain, with 92.3 % similarity. This is within the mean range (76–100 %) of
rpoB gene sequence similarity between species of the same genus within the family
Pasteurellaceae. 16S rRNA gene sequencing of four strains selected based on rpoB sequence
comparison showed at least 99.7 % similarity between strains of Pasteurella species B, with
96.2 % similarity to the type strain of the closest related species (Pasteurella canis), indicating
that Pasteurella species B should have separate species status. Separate species status was also
documented when recN sequence comparisons were converted to a genome similarity of 93.7 %
within Pasteurella species B and 59.0 % to the type strain of the closest related species (P.
canis). Based on analysis of the phylogenetic and phenotypic data, and since most isolates
originate from the oral cavities of a diverse group of animals, it is suggested that these bacteria be
classified as Pasteurella oralis sp. nov.; the type strain is P683T (5CCUG 19794T5CCM
7950T5strain 23193T5MCCM 00102T), obtained from a cat. Previous reports of the type strain
have shown ubiquinone-8, demethylmenaquinone-8 and menaquinone-8 as the major quinones.
Polyamines in the type strain were reported as diaminopropane, putrescine, cadaverine, symnorspermidine, spermidine and spermine in a previous investigation, and the major fatty acids of
the type strain were reported to be C16 : 0, C16 : 1v7c and C14 : 0, with minor amounts of C18 : 0 and
C18 : 1v9c. The DNA G+C content of the type strain has been reported to be 40.0 mol%.
The name of the genus Pasteurella was first published by
Trevisan (1887). The heterogeneity of the genus was
initially recognized based upon DNA–DNA hybridizations
(Pohl, 1981). Further investigations showed that Pasteurella
sensu stricto should be restricted to include the nine named
species Pasteurella multocida, Pasteurella canis, Pasteurella
The GenBank/DDBJ/EMBL accession numbers for the partial 16S
rRNA sequence of strain F12_tonsilmale is JN050250, for the partial
rpoB sequences of strains P683T, Pind2A and Gal2B are JN050251,
JN050253 and JN050252, respectively, and for the partial recN gene
sequences for strains P683T and F12_tonsilmale are JN050255 and
JN050254, respectively.
Four supplementary tables and two supplementary figures are available
with the online version of this paper.
1396
stomatis, Pasteurella dagmatis, [Pasteurella] gallinarum,
[Pasteurella] avium, [Pasteurella] volantium, [Pasteurella]
langaaensis [the original spelling of the specific epithet,
langaa, was corrected by Trüper & De’Clari (1997)] and
[Pasteurella] anatis, in addition to two unnamed taxa,
[Pasteurella] species A and Pasteurella species B (Mutters
et al., 1985a, b, 1989) (species found to be unrelated to
members of the genera Pasteurella and Haemophilus were
informally excluded by writing the genus name of these
species in square brackets; Mutters et al., 1989). According
to 16S rRNA gene sequence-based phylogenetic analysis, P.
multocida, P. canis, P. stomatis, P. dagmatis and Pasteurella
species B form a monophyletic group referred to as cluster
3B (Dewhirst et al., 1993), whereas the avian taxa [P.]
gallinarum, [P.] avium, [P.] volantium and [Pasteurella]
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Pasteurella oralis sp. nov.
species A form another monophyletic group, cluster 3A
(Dewhirst et al., 1993). Reclassification of cluster 3A led to
the formation of a new genus, Avibacterium (Blackall et al.,
2005), which also included, in addition to the type species
Avibacterium gallinarum, [P.] avium, [P.] volantium and
[Pasteurella] sp. A, originally described by Mutters et al.
(1985a), [Haemophilus] paragallinarum (Biberstein & White,
1969) and, subsequently, the novel species Avibacterium
endocarditidis (Bisgaard et al., 2007). [P.] anatis was
reclassified as Gallibacterium anatis by Christensen et al.
(2003). After the reclassification, P. multocida, P. canis, P.
stomatis, P. dagmatis and Pasteurella species B were left in
Pasteurella sensu stricto (Christensen & Bisgaard, 2006).
Considerable diversity of P. multocida has been reported
and, based upon phylogenetic analysis, two lineages, A
(P. multocida subsp. multocida and P. multocida subsp.
gallicida) and B (P. multocida subsp. septica), have been
described, the biological significance of which remains to
be elucidated (Davies, 2004; Bisgaard et al., 2008). In
addition, two new taxa (taxon 45 and 46 of Bisgaard)
associated with large cats were outlined by Christensen et al.
(2005), both of which were classified within Pasteurella
sensu stricto.
Isolates reported as Pasteurella species B have so far only
been reported from the oral cavity of dogs and cats, a
European vespertilionid bat and a ferret (Bisgaard, 1993;
Mühldorfer et al., 2011), and the clinical impact of these
organisms remains to be investigated. Although it clustered
with P. multocida, P. canis, P. stomatis and P. dagmatis, the
strain investigated by 16S rRNA sequence comparison
(CCUG 19974T) branched deeply with these species
(Dewhirst et al., 1993). DNA–DNA hybridizations between
two strains of Pasteurella species B showed 87 % reassociation, whereas low values were demonstrated to other taxa
of Pasteurella sensu stricto with 63, 37, 19 and 4 % DNA
reassociation to type strains of P. stomatis, P. dagmatis, P.
canis and P. multocida, respectively (Mutters et al., 1985b).
rRNA cistron similarities of members of the Pasteurellaceae
showed that Pasteurella species B strain P683T clustered
with the common root of the rRNA branches for Aggregatibacter actinomycetemcomitans, Aggregatibacter aphrophilus, [Haemophilus] influenzae, Actinobacillus lignieresii
and P. multocida (De Ley et al., 1990). Compared to the
type strain of P. multocida, diaminopropane was only
present in Pasteurella species B strain MCCM 00102T,
whereas the other polyamines putrescine, cadaverine, symnorspermidine, spermidine and spermine were present in
both strains (Busse et al., 1997). To improve our knowledge of Pasteurella species B, the aims of the current
investigation were to characterize, classify and name
organisms referred to as Pasteurella species B to provide
unambiguous methods for separation of these organisms in
the clinical laboratory.
To extend the existing strain collection, samples were
collected from the oral/gingival mucosa of selected animals
from Copenhagen Zoo including large cats, hedgehogs, a
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banded mongoose, a member of the Varanidae and a
Moholi bushbaby using sterile cotton swabs. All samples
were immediately plated on blood agar (blood agar base,
CM55; Oxoid) containing 5 % sterile bovine blood and
incubated at 37 uC for 24 h. Subcultures of greyish, small
to medium-sized colonies typical of members of the
Pasteurellaceae were made after 24 h and subjected to
phenotypic testing; cultures were stored frozen as described
by Christensen et al. (2007).
A total of nine isolates of Pasteurella species B obtained
from African hedgehogs (Atelerix albiventris), three from
the banded mongoose (Mungos mungo), and single isolates
from a Moholi bushbaby (Galago moholi) and a Varanus
albigularis, respectively, were compared phenotypically
(Bisgaard et al., 1991); data from strains CCUG 19794T,
CCUG 28019, CCUG 19994, HPA 175, C22189 and 46667/
75 have been partly investigated previously (Table S1,
available in IJSEM Online). The strain from a ferret was
characterized by phenotype, but died out before genotypic
characterization could be initiated. Type strains of species
of Pasteurella sensu stricto were included for comparison.
The CAMP test was performed by inoculating a blood
agar plate with the test organism at a right angle to the
inoculated line of a b-toxinogenic strain of Staphylococcus
aureus followed by overnight incubation (Christie et al.,
1944). CAMP is an abbreviation of the first initials of family
names of the authors who described the test (Christie et al.,
1944). Phenotypic results obtained were similar to those
previously published for Pasteurella species B (Mutters et al.,
2005; Christensen & Bisgaard, 2006). Differences in urease
and ornithine decarboxylase activities, and production of
acid from (+)-D-xylose, dulcitol, (2)-D-mannitol, maltose
and dextrin separate Pasteurella species B from members of
other taxa of Pasteurella (Table 1).
Analysis of fatty acids (strains P683T and P809; see Table
S1) has been published previously by Engelhard et al.
(1991). In the proposed type strain, major fatty acids were
reported as C16 : 0, C16 : 1cis9 and C14 : 0, with minor amounts
of C18 : 0, C18 : 1cis9 and traces of C20 : 4cis5, C14 : 0 3-OH,
C20 : 1trans11, C20 : 0, C18 : 1cis9, C16 : 1C, C15 : 0, C14 : 5 and
C12 : 0. This profile is in accordance with other members of
Pasteurella sensu stricto including P. multocida (Table S2).
Analysis of ubiquinones (Q) for the reference strain of
Pasteurella species B has been published previously (Table
S3). Ubiquinone Q-8, demethylmenaquinone DMK-8 and
menaquinone MK-8 were the major quinones. All three
types of molecules (Q-8, DMK-8, MK-8) have also been
found in the other members of Pasteurella sensu stricto
investigated including the type strain of P. multocida, although in different proportions depending on the investigation (Table S3). The reason for different proportions of
ubiquinones, menaquinones and demethylmenaquinones
seems to be the higher degree of aeration used during
cultivation by Kainz et al. (2000) than in the investigations
of Kroppenstedt & Mannheim (1989) and Engelhard et al.
(1991).
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H. Christensen and others
Table 1. Phenotypic separation of P. oralis from related members of Pasteurella sensu stricto
Taxa: 1, P. oralis; 2, P. multocida; 3, P. canis; 4, P. stomatis; 5, P. dagmatis. Data were obtained using the same methodology and under the same
culture conditions. +, Positive within 1–2 days; (+), positive within 3–14 days; 2, negative after 14 days; d, different.
Characteristic
1
2
3
4
5
Urease
Ornithine decarboxylase
Acid from:
(+)-D-Xylose
Dulcitol
(2)-D-Mannitol
Maltose
Dextrin
2
+
2
+
2
+
2
2
+
2
+
+
2
+
+
d
d
+
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
+
+/(+)
rpoB gene sequence-based classification has previously been
used with members of the Pasteurellaceae (Angen et al.,
2003; Korczak et al., 2004). The partial rpoB sequences of
19 isolates (Table S1) were determined according to Mollet
et al. (1997) and Korczak et al. (2004) covering the region
509–680 (Escherichia coli position) of the deduced protein
sequence. In addition to published primers, the forward
PCR primer rpobfAp (59-GCAGTGAAAGAGTTCTTYGGTTC) was used for PCR amplification and DNA sequencing. Sequencing was performed by Macrogen (Seoul,
Korea).
Sequencing of the 16S rRNA gene of four strains selected
based on rpoB sequence comparison was performed
according to previous reports (Christensen et al., 2002;
Angen et al., 2003). recN gene sequences were used as a
representative target for determining whole-genome sequence
similarity as described by Kuhnert & Korczak (2006), with
1311 bp of the gene being sequenced in two strains according
to Kuhnert & Korczak (2006). Whole genome similarity
values were calculated according to Zeigler (2003).
A BLAST search (Altschul et al., 1997) was performed in
GenBank (Benson et al., 2006). Pairwise comparisons
for similarity were performed by the program WATER
included in EMBOSS (Rice et al., 2000). Multiple alignment
was performed by CLUSTAL_X (Thompson et al., 1997).
Maximum-likelihood analysis, including bootstrap analysis, was performed by fastDNAml (Felsenstein, 1995;
Olsen et al., 1994) on a Linux 7.2-compatible server. The
analysis was run with transition/transversion ratios of 1.0,
1.5 and 1.6 for 16S rRNA, rpoB and recN gene sequences,
respectively.
Analysis of the rpoB gene sequences showed that the 17
isolates of Pasteurella species B characterized (including
strain CCUG 19794T) were identical in sequence to the
published sequence of strain E135/09/1 (GenBank/EMBL/
DDBJ accession no. HM747014; Mühldorfer et al., 2011).
Only Gal2B and Pind2A diverged by 99.6 and 97.9 %,
respectively. The highest similarity with other members of
the genus Pasteurella was obtained with the type strain of P.
stomatis (92.3 %); 88.1 % similarity was observed with the
type strain of P. multocida. Both values are within the lower
1398
range of the mean rpoB gene sequence similarity between
species of the same genus within the Pasteurellaceae
(range 76–100 %) for 62 type strains of the Pasteurellaceae
belonging to species with validly published names (Table
S4). Using these limits as criteria to define new genera of
Pasteurellaceae, the isolates should be classified as representatives of the genus Pasteurella; however, the species status
should not be defined by rpoB comparison alone. The rpoB
phylogeny is shown in Fig. S1.
The 16S rRNA gene sequence analysis showed that three of
the isolates characterized were identical to the published
sequence of strain E135/09/1 (GenBank/EMBL/DDBJ
accession no. HM746983) included in the publication of
Mühldorfer et al. (2011). The lowest similarity within the
group was between CCUG 19794T and the sequence of
strain F12_tonsilmale (99.3 %). The highest 16S rRNA gene
sequence similarity outside the group was 96.2 %, which
was obtained with the type strain of P. canis, thus
indicating the separate species status of Pasteurella species
B and that DNA–DNA reassociation experiments are not
mandatory for establishing the taxon as a novel species
(Tindall et al., 2010). Separate species status within the
genus Pasteurella was also shown by the phylogeny in
which monophyly was demonstrated for members of the
Pasteurella, including the type species P. multocida (Fig. 1).
In the figure, taxon 45 is related to the two subspecies of P.
multocida and the three taxa form a paraphyletic group. In
previous investigations, we have shown that taxon 45 is a
new genomospecies of Pasteurella that cannot be phenotypically separated from P. multocida. Taxon 45 was found
to be genotypically distinct from P. multocida but still
closely related to it (Christensen et al., 2005). The distinct
phylogenetic positions of P. multocida subsp. multocida
and P. multocida subsp. septica also reflect their genotypic
diversity. DNA reassociation was 80 % between the type
strains of the two subspecies and it was concluded that they
could have been classified as different species; however,
from a clinical viewpoint, they were left as subspecies of P.
multocida (Mutters et al., 1985b).
A separate species status was also documented by recN
sequence comparisons, giving a genome similarity of
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Pasteurella oralis sp. nov.
Fig. 1. Phylogenetic relationships between isolates of P. oralis and other members of Pasteurella sensu stricto based on
maximum-likelihood analysis of partial 16S rRNA sequences. Support for monophyletic groups by bootstrap analysis is
indicated as numbers out of 100. Strains sequenced in this study are given in bold. The asterisk indicates that three additional
strains (see Table S1) share the sequence of the strain at the branch. Bar, sequence variation considering the models for
nucleotide substitution and tree-shape used in the maximum-likelihood analysis.
93.7 % within Pasteurella species B (CCUG 19794T and
F12_tonsilmale) and 59.0 % to the type strain of P. canis,
the closest related species of the genus Pasteurella (Fig. S2)
(recN sequences are not available for other type strains of
Pasteurella sensu stricto).
Phylogenetic analysis (Fig. 1; Figs S1 and S2) showed that
all isolates were closely related to the reference strain
(P683T) of Pasteurella species B and, since most isolates
originate from the oral cavity of a diverse group of animals
and clinical isolates have been associated with bite wounds,
it is suggested that these bacteria are representatives of a
novel species, Pasteurella oralis sp. nov. Members of this
taxon were originally isolated from a cat and human bite
wounds inflicted by a dog. Subsequent investigations have
extended the reservoir to include a diversity of zoo animals
in addition to bats (this investigation; Mühldorfer et al.,
2011). Although P. oralis was demonstrated in Atelerix
albiventris, investigation of a colony of Erinaceus europaeus
did not demonstrate that they were carriers of P. oralis.
Currently, it cannot be confirmed that the taxon is related
to particular hosts.
The phenotypic properties of the novel species correspond
with those of members of the genus Pasteurella (Mutters
et al., 1985b) including the presence of Q-8 and DMK-8,
oxidase-positive, lack of X factor requirement and alkaline
phosphatase reaction.
Description of Pasteurella oralis sp. nov.
Pasteurella oralis (o.ra9lis. L. n. os oris mouth; L. fem. suff.
-alis suffix denoting pertaining to; N.L. fem. adj. oralis
pertaining to the mouth, of the mouth).
On blood agar, colonies are circular, slightly raised and
regular with an entire margin. The surface of the colonies is
smooth, shiny and opaque with a greyish tinge. Colonies
demonstrate a diameter of approximately 1.5 mm after
aerobic incubation for 24 h at 37 uC. The consistency of
the colonies is unguent-like and colonies do not adhere to
the agar. All isolates are both non-haemolytic and CAMPnegative. Non-symbiotic growth is observed and isolates
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are positive in the porphyrin test. Cells are coccobacilli to
rod-shaped and stain Gram-negative. Cells are non-motile
at both 22 and 37 uC. The catalase and oxidase tests are
positive, whereas negative reactions are obtained in the
Simmons citrate test, acid is not formed from mucate and
an alkaline reaction is not obtained from malonate.
Negative reactions are also observed for the H2S/TSI test,
tolerance to KCN, methyl red, Voges–Proskauer, gas from
nitrate, arginine dehydrolase, lysine decarboxylase, phenylalanine deaminase, gelatinase, growth on Tween 20 and
80, gas from (+)-D-glucose and growth on McConkey
medium. Can reduce nitrate. Positive reactions are
obtained in tests for alanine aminopeptidase and alkaline
phosphatase, but negative for urease. Positive for ornithine
decarboxylase and indole formation. Acid is formed from
xylitol, (2)-D-ribose, (+)-D-xylose, dulcitol, (2)-D-fructose, (+)-D-galactose, (+)-D-glucose, (+)-D-mannose,
sucrose, trehalose, maltose and dextrin. Acid is not formed
from glycerol, meso-erythritol, (2)-D-adonitol, (+)-Darabitol, (+)-L-arabinose, (2)-L-xylose, (2)-D-arabinose,
myo-inositol, (2)-D-mannitol, (2)-D-sorbitol, (+)-Lrhamnose, (+)-D-fucose, (2)-L-fucose, (2)-L-sorbose,
cellobiose, lactose, (+)-melibiose, (+)-melezitose, raffinose, (+)-D-glycogen, inulin, aesculin, amygdalin, arbutin,
gentiobiose, salicin, (+)-turanose and b-N-CH3-glucosamide. Positive for a-glucosidase by PNPG (4-nitrophenyla-D-glucopyranoside). Negative for b-galactosidase performed with ONPG (o-nitrophenyl-b-D-glucopyranoside),
b-glucosidase by NPG (4-nitrophenyl-b-D-glucopyranoside), a-fucosidase by ONPF (2-nitrophenyl-a-L-fucopyranoside), a-galactosidase, b-glucuronidase by PGUA
(4-nitrophenyl-b-D-glucopyranosiduronic acid) and amannosidase and b-xylosidase test by ONPX (2-nitrophenyl-b-D-xylopyranoside). Characters separating this species
from previously named species of Pasteurella include
urease and ornithine decarboxylase activities, and production of acid from (+)-D-xylose, (2)-D-mannitol, maltose
and dextrin (Table 1). Previous investigations of the type
strain (MCCM 00102T) have shown Q-8, MK-8 and DMK8 as quinones (Engelhard et al., 1991; Kainz et al., 2000)
(Table S3). Polyamines in the type strain were reported as
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1399
H. Christensen and others
diaminopropane, putrescine, cadaverine, sym-norspermidine, spermidine and spermine (Busse et al., 1997). In the
type strain, the major fatty acids were reported as C16 : 0,
C16 : 1v7c and C14 : 0, with minor amounts of C18 : 0,
C18 : 1v9c and traces of C20 : 4cis5, C14 : 0 3-OH, C20 : 1
trans11, C20 : 0, C16 : 1C, C15 : 0, C14 : 5 and C12 : 0 (Engelhard
et al., 1991).
Christensen, H. & Bisgaard, M. (2006). The genus Pasteurella. In The
The type strain is P683T (5CCUG 19794T5CCM 7950T
5strain 23193T5MCCM 00102T), isolated from a cat bite of
a human in 1981 in Czechoslovakia. The DNA G+C content
was reported as 40.0 and 38.9 mol% for strains P683T and
P809, respectively (Mutters et al., 1985b).
Christensen, H., Bisgaard, M., Bojesen, A. M., Mutters, R. & Olsen,
J. E. (2003). Genetic relationships among avian isolates classified as
Prokaryotes, 3rd edn, vol. 6, pp. 1062–1090. Edited by M. Dworkin,
S. Falkow, E. Rosenberg, K.-H. Schleifer & E. Stackebrandt. New
York: Springer.
Christensen, H., Bisgaard, M., Angen, Ø. & Olsen, J. E. (2002). Final
classification of Bisgaard taxon 9 as Actinobacillus arthritidis sp. nov.
and recognition of a novel genomospecies for equine strains of
Actinobacillus lignieresii. Int J Syst Evol Microbiol 52, 1239–1246.
Pasteurella haemolytica, ‘Actinobacillus salpingitidis’ or Pasteurella
anatis with proposal of Gallibacterium anatis gen. nov., comb. nov.
and description of additional genomospecies within Gallibacterium
gen. nov. Int J Syst Evol Microbiol 53, 275–287.
Christensen, H., Bisgaard, M., Angen, Ø., Frederiksen, W. & Olsen,
J. E. (2005). Characterization of sucrose-negative Pasteurella multo-
Acknowledgements
Excellent technical assistance was contributed by the technicians Pia
Mortensen and Katrine Madsen. We would like to express our thanks
to Dr Hans-Jürgen Busse, University of Veterinary Medicine, Vienna
for guidance with the fatty acids and quinone data and to Professor
Jean P. Euzeby, Ecole Nationale Veterinaire, Toulouse, France for
help with the scientific name.
cida variants, including isolates from large-cat bite wounds. J Clin
Microbiol 43, 259–270.
Christensen, H., Kuhnert, P., Busse, H.-J., Frederiksen, W. C. &
Bisgaard, M. (2007). Proposed minimal standards for the description
of genera, species and subspecies of the Pasteurellaceae. Int J Syst Evol
Microbiol 57, 166–178.
Christie, R., Atkins, N. E. & Munch-Petersen, E. (1944). A note on a
lytic phenomenon shown by group B streptococci. Aust J Exp Biol
Med Sci 22, 197–200.
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