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Previous Article | Next Article 
Journal of Bacteriology, November 1998, p. 6054-6058, Vol. 180, No. 22
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Physical and Genetic Map of the Pasteurella
multocida A:1 Chromosome
Meredith L.
Hunt,
Carmel G.
Ruffolo,
Kumar
Rajakumar, and
Ben
Adler*
Department of Microbiology, Monash
University, Clayton, Victoria 3168, Australia
Received 5 May 1998/Accepted 5 September 1998
 |
ABSTRACT |
A physical and genetic map of the Pasteurella multocida
A:1 genome was generated by using the restriction enzymes
ApaI, CeuI, and NotI. The positions
of 23 restriction sites and 32 genes, including 5 rrn
operons, were localized on the 2.35-Mbp single circular chromosome.
This report presents the first genetic and physical map for this genus.
| |
TEXT |
The gram-negative, facultative
bacterium Pasteurella multocida is an important veterinary
pathogen with worldwide distribution. It is a member of the
Pasteurellaceae family (16), which includes the
genera Haemophilus, Actinobacillus, and
Lonepinella (15). Certain serotypes are the
etiological agents of a number of severe pasteurelloses, such as fowl
cholera in poultry, atrophic rhinitis in swine, and hemorrhagic
septicemia in cattle and buffalo. Despite much research into the
various diseases caused by P. multocida, there has been
little characterization of this organism at the molecular level, and
few of its genes have been characterized.
Here we describe the construction of a physical and genetic map of
P. multocida serotype A:1, an Australian fowl cholera
isolate, strain PBA100 (7). Restriction enzymes with GC-rich
recognition sequences were chosen, as the G+C content of P. multocida is between 40 and 43% (14). The
intron-encoded endonuclease CeuI, which recognizes a 26-bp
sequence found exclusively in the 23S rRNA gene (12, 23),
was used for restriction mapping and the analysis of the P. multocida rRNA (rrn) operons.
Restriction fragment analysis and estimation of genome size.
High-molecular-weight DNA was purified by the method of Smith and
Cantor (21), except that the detergent Brij 58 was omitted from the lysis solution. The enzymes ApaI (Boehringer
Mannheim), NotI, and CeuI (both from New England
Biolabs) were used in physical mapping of the P. multocida
genome according to the manufacturers' instructions. Double digestions
were performed as two consecutive 16-h digests, with CeuI
digestion always performed second.
The resulting restriction fragments were separated by
pulsed-field gel electrophoresis (PFGE) in 1% agarose gels
in 0.5× Tris-borate-EDTA buffer (20) at 14°C with a
contour-clamped homogeneous electric field apparatus (CHEF DRII;
Bio-Rad). A range of conditions for electrophoresis was used to
visualize and size the macrorestriction fragments. Typically, fragments
between 50 and 500 kb were separated by using a linear ramp time of 10 to 60 s for 24 h at 200 V. Larger restriction fragments were
observed by using longer pulse times of 10 to 150 s and 180 V for
24 h.
PFGE profiles resulting from single and double restriction digestions
are shown in Fig. 1A. The sizes of the
resulting macrorestriction fragments estimated from a number of
pulsed-field gels run under different conditions to optimize the
separation of bands are listed in Table
1. When standard agarose gel
electrophoresis was used to visualize restriction fragments under 20 kb, only the 9-kb NF band was detected (Fig. 1B). The ApaI
and ApaI/CeuI restriction profiles appeared
identical (Fig. 1A, lanes 5 and 6), indicating the close linkage of the
five CeuI sites to five ApaI sites. No evidence
of extrachromosomal elements was found in the strain studied by using
either a standard alkaline lysis plasmid preparation or the method of
Kado and Liu (8) for the extraction of large plasmids. Based
on these data, the P. multocida A:1 genome was estimated to
be 2.35 Mbp.
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FIG. 1.
(A) PFGE of P. multocida DNA fragments
produced after digestion with CeuI (lane 1),
NotI/CeuI (lane 2), NotI (lane 3),
NotI/ApaI (lane 4), ApaI (lane 5), and
ApaI/CeuI (lane 6). The positions of standard DNA
size markers (in kilobases) are shown on the left. Electrophoresis was
performed in 1% agarose with a pulse time of 10 to 80 s at 200 V
for 24 h. In this figure, a single band represents each of the
ApaI fragment pairs, AA/AB, AD/AE, and AF/AG (lane 5). (B)
Standard agarose gel electrophoresis, showing the migration of P. multocida genomic DNA after NotI digestion, to
visualize the 9-kb NF restriction fragment. The positions of
HindIII-digested lambda DNA size markers (in kilobases)
are shown on the right. The originals were scanned with a
Hewlett-Packard ScanJet 4cse by using the Adobe Photoshop 2.5.1 LE
program and exported into Deneba Canvas 3.5.4 for presentation.
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View this table:
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TABLE 1.
Sizes of restriction fragments observed by PFGE after
digestion of P. multocida A:1 (PBA100) genomic DNA with
restriction enzymes as indicated
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|
Construction of the physical and genetic map.
Single and
double restriction digestion, partial ApaI digestion,
Southern hybridization using homologous and heterologous gene
probes, the generation of linking clones, and reciprocal hybridization
using macrorestriction fragments as probes were used to generate a
physical and genetic map of the P. multocida A:1 chromosome.
All hybridization, probe labeling, and chemiluminescence detection
steps were performed according to the Dig System User's Guide
(Boehringer Mannheim). Hybridizations with homologous probes were
performed under conditions of high stringency at 68°C, whereas those
with heterologous probes were performed at 55°C under
medium-stringency conditions consisting of two 5-min washes at room
temperature in 2× SSC (1× SSC is 0.15 M NaCl plus 0.015 M sodium
citrate)-0.1% sodium dodecyl sulfate (SDS) and two 15-min washes at
37°C in 1× SSC-0.1% SDS.
A small number of NotI and ApaI linking clones
were constructed by digesting 1 µg of genomic DNA to completion with
BamHI, EcoRI, or HindIII.
Restriction digestion products were self-ligated and digested
with either NotI or ApaI. The resulting linear
fragments were then cloned into NotI- or
ApaI-digested pBluescript II KS (Stratagene) and used as
probes in Southern hybridization experiments. The linkages NA-NE1,
NB-NC2, and NC1-ND were established by using the isolated
NotI linking clones. These linkages were found to occur in
the AE and CC fragments, the AD and CD fragments, and the AC and CA
fragments, respectively.
A number of the ApaI linking clones isolated were of limited
use in linkage analysis, as they hybridized to multiple ApaI fragments, all CeuI fragments, and NotI fragments
NA, NB, and NC. The remaining ApaI linking clone linked AA
with AG, and this linkage was found to lie within the CB and NA
fragments. This approach thus definitively identified overlapping
groups of restriction fragments between the three restriction enzymes.
Reciprocal hybridization experiments using macrorestriction fragments
as probes extended the linkage data and allowed for the placement of
fragments into a circular genomic map. However, because AA and AG
occurred entirely within NA and CB, their order could not be determined
by reciprocal hybridization or linker probe data alone. Partial
ApaI restriction digestion was used to determine the
orientations of these fragments. ApaI partial fragments of
790 and 415 kb, which may comprise AA-AC (800 kb) and AG-AE (408 kb),
respectively, were observed. If the ApaI fragments were
present in the order AC-AG-AA-AE, a 688-kb fragment representing the
linkage AA-AE and a 520-kb fragment representing AC-AG would be
expected. Although a 680-kb fragment was seen, no partial fragment in
the vicinity of 520 kb was observed. This suggested that the most
likely arrangement of these fragments was AC-AA-AG-AE.
Gene probes (Table 2) were hybridized to
single and double digests of P. multocida genomic DNA. This
led to the positioning of genes which covered much of the genome onto
the physical map and provided further evidence for the overlapping
linkage groups of restriction fragments, hence permitting a more
precise alignment of the three restriction maps with respect to each
other. The combined physical and genetic map is shown in Fig.
2A.
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FIG. 2.
(A) Physical and genetic map of the 2.35-Mbp circular
chromosome of P. multocida A:1 PBA100. The positions of the
ApaI, CeuI, and NotI restriction sites
are shown, and fragment names are indicated. The genes are positioned
on the map to the minimum region localized by hybridization. The order
of genes given in a particular region is arbitrary and does not
necessarily represent the actual order of genes in that area. The genes
groEL, rpsF, and tonB can be localized
only to the 95-kb AI fragment, as it is not known to which NE fragment
these genes belong. Asterisk, putative location of the origin of
replication, linked to gidA. The arrows indicate the
presumed 5' 3' direction of transcription of the rrn
operons given the gene order rrs-rrl-rrf. (B) Determination
of rrn gene position and orientation on the P. multocida chromosome. (Top) Diagrammatic representation of a
ribosomal operon and the positions of heterologous D. nodosus probes 1, 3, and 4 and homologous rrs gene
probe 2. The approximate positions of ApaI and
CeuI sites in the P. multocida rrn operons are
indicated. (a) PFGE-resolved restriction fragments of P. multocida DNA obtained by using running conditions of 20 to
60 s at 200 V for 24 h. The positions of standard DNA size
markers (in kilobases) are shown on the left. (b through e) Resulting
Southern hybridization profiles obtained by using the probes indicated
above. In all panels, lanes 1, 2, and 3 represent CeuI,
NotI, and ApaI restriction digestion fragments,
respectively. The originals were scanned with a Hewlett-Packard ScanJet
4cse by using the Adobe Photoshop 2.5.1 LE program and exported into
Deneba Canvas 3.5.4 for presentation.
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|
Location, orientation and operon structure of the P. multocida A:1 rrn genes.
The intron-encoded
endonuclease CeuI has been found to cut exclusively in the
rrl genes of many bacteria (12). Thus, the five
restriction fragments generated indicated that PBA100 has five copies
of the rrl gene. To determine if rRNA genes in P. multocida were organized into operons, heterologous rrn
probes from Dichelobacter nodosus, probe 1, probe 3, and
probe 4 (11), and a homologous PCR-derived 16S rRNA probe,
probe 2, with the primers 5'-AGAGTTTGATCCTGGCTCAG-3' and
5'-GGTTACCTTGTTACGACTTC-3', which bind to conserved regions
of the 16S rRNA gene, were used in Southern hybridization analysis
(Fig. 2B). With all rrn probes used, an invariant
NotI hybridization profile of NA, NB, and NC was seen,
indicating that rrn genes resided only on these
NotI restriction fragments. The linkage of the five
CeuI fragments to five ApaI fragments was
apparent from the similarity of the ApaI and
ApaI/CeuI digests (Fig. 1) and the resulting
physical map. Hybridization results, taken in conjunction with the
physical mapping data, indicated that the rrs genes in
P. multocida traverse ApaI sites. This was
confirmed by the isolation of ApaI linking clones that
hybridized to the same set of NotI fragments (NA, NB, and
NC), many ApaI restriction fragments, and all
CeuI fragments. One such clone, a 5.5-kb
EcoRI-generated ApaI linking clone, was partially sequenced, revealing the presence of an rrs
gene containing a single ApaI site and both rrl
and rrf genes. Considering the sequencing data and the
rrn hybridization profiles, P. multocida rRNA
genes appear to be organized into five operons, with the gene order of
these operons, like that of many other eubacteria, being
rrs-rrl-rrf. CeuI and
ApaI/CeuI digestion of these linking clones
indicated the presence of a unique CeuI site and
demonstrated an ApaI/CeuI fragment of either 2.9 or 3.1 kb, thus indicating the presence of two classes of
rrn loci with different spacing of the ApaI and
CeuI restriction sites. The direction of
transcription of each operon, designated rrnA through
rrnE, was ascertained from hybridization analysis
(Fig. 2).
Genetic organization.
This study, which positions 23 restriction sites and 32 genetic markers onto a 2.35-Mbp circular
chromosome, details the first physical and genetic map for the species
P. multocida and the genus Pasteurella. Key
genetic markers such as gidA, the five rrn
operons, recA, and groEL have been positioned
onto the chromosome. The genome size derived in this study places
P. multocida in bacterial genome group 2 as defined by Cole
and Saint Girons (2), which includes genomes between 1.5 and
3 Mbp. This group includes a range of human and animal pathogens, such
as the gram-positive bacteria Streptococcus pneumoniae and
Staphylococcus aureus and the gram-negative bacteria
Campylobacter jejuni, Neisseria gonorrhoeae, and
Haemophilus influenzae (2).
Several features of genome organization common among many
bacteria appear to be conserved in P. multocida. The
gidA gene, encoding the glucose-inhibited division
protein, is adjacent to the origin of replication, oriC, in
Pseudomonas putida, Pseudomonas aeruginosa,
Escherichia coli, Bacillus subtilis, and the
closely related strain H. influenzae Rd (3, 22).
If gidA is also linked to the origin of replication in
P. multocida, then genes involved in transcription, as in
many other bacteria, map close to the origin: greB and
atpG are both located on the same fragment as
gidA, and rpoB and aspS occur within
approximately 285 kb of this site (Fig. 2A).
The rrn operons of P. multocida A:1 strain PBA100
occur in two unequal groups, transcribed divergently from the putative
site of oriC, which may itself be linked to the
rrnA operon. This is a common feature of many bacterial
chromosomes, in which the rrn genes are often located within
one-third to one-half of the chromosome (17). The operons
rrnA, rrnB, rrnC, and rrnD,
which are transcribed in the same direction away from the presumed
location of oriC, lie within a 735-kb region (31% of the
chromosome). In many bacteria, a single rrn operon is
transcribed divergently from the other rrn loci. However, in
PBA100 the single divergently transcribed rrnE operon is
located at an unusually large distance of almost 980 kb away from the
putative origin of replication, with the result that the five
rrn operons of P. multocida are spread over a
much greater proportion of the chromosome than is common in other bacteria.
Varying degrees of genome structure conservation are seen within and
between bacterial genera and species (4). A comparison of the genetic maps of the Pasteurellaceae members
P. multocida and H. influenzae Rd
revealed both similarities and differences, but no long-range
colinearity of gene order was found. The conservation of gene order
among some bacteria is often most marked close to the origin
(9). Local gene order and similar genome locations were
apparent for the orthologous genes greB and
HI0568. An order and spacing of these two genes in P. multocida similar to those in H. influenzae Rd were
determined from sequence analysis of pPBA1211 (Table 2). These genes
mapped to the macrorestriction fragment AF, which contained the
putative location of oriC.
The yaeL-oma87-skp-firA region of P. multocida
(18, 19) was identified as another region of local
conservation of gene order, aligning with the H. influenzae
Rd genes yaeL-D15-skp-firA (3). However, these
orthologues have different chromosomal locations. Differences in gene
positions are also apparent when the clustering together of
murCG and ptfA within a 125-kb region, the
clustering of aroA and lapB within a 180-kb
region, and the close proximity of tonB to
groEL and rpsF in the P. multocida genome are taken into consideration. In H. influenzae Rd, these groups of genes are separated by much greater
distances. Despite the fact that the genome of P. multocida
is 520 kb larger, there was no evidence for the occurrence of multiple
lapB and tbpI loci, such as are found in H. influenzae Rd. Also, P. multocida has only five
rrn operons, which are arranged differently from the six rrn operons of H. influenzae Rd.
Differences between these Pasteurellaceae members are not
unexpected when the different growth requirements of these two
pathogens and the different diseases they cause are considered.
Additionally, different NotI profiles have been reported
previously for other P. multocida isolates (24).
We have also observed differing CeuI profiles in other
serotype A:1 isolates and some isolates of heterologous serotypes (data
not shown), indicating that P. multocida exhibits
significant intraspecies heterogeneity. The marked differences between
restriction fragment profiles may be the result of a heterogeneous
group of organisms being grouped together as a single species.
Alternatively, while no extrachromosomal elements were found in PBA100,
a variety of bacteriophages and plasmids have been characterized
in other P. multocida isolates (1, 5). Hence, the
tools for genome plasticity are present in the P. multocida species.
This genomic map provides a basis for the study of genomic organization
in P. multocida. Comparative analysis of the ApaI and CeuI profiles of P. multocida isolates
will be useful in tracking the number and arrangement of the
rrn loci. The placement on the map of more
virulence-associated genes and the future use of this map in
comparative studies with other P. multocida isolates of the same or different serotypes will provide greater insights into the genomic architecture of P. multocida and
may begin to answer questions about the molecular basis for the
differences in host predilection and pathogenicity in this diverse species.
| |
ACKNOWLEDGMENTS |
We are grateful to Ian McPherson and Vicki Vallance for their
excellent technical assistance. We also thank Dario Diberardino for the
16S rRNA primers and Sharon La Fontaine for helpful discussions.
This work was supported by research grants from the Chicken Meat
Research and Development Council of Australia and the Australian Research Council.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Microbiology, Monash University, Clayton, Victoria, Australia 3168. Phone: 61-3-9905-4815. Fax: 61-3-9905-4811. E-mail:
Ben.Adler{at}med.monash.edu.au.
Present address: Department of Biological Sciences, University of
Wisconsin-Parkside, Kenosha, Wis.
| |
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Journal of Bacteriology, November 1998, p. 6054-6058, Vol. 180, No. 22
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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