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Journal of Bacteriology, January 2000, p. 207-210, Vol. 182, No. 1
0021-9193/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Localized Reversible Frameshift Mutation in the
flhA Gene Confers Phase Variability to Flagellin Gene
Expression in Campylobacter coli
Simon F.
Park,1,*
Desmond
Purdy,2 and
Stephen
Leach2
School of Biological Sciences, University of
Surrey, Guildford, GU2 5XH,1 and Centre
for Applied Microbiology and Research, Porton Down, Salisbury, SP4
OJG,2 United Kingdom
Received 3 August 1999/Accepted 14 October 1999
 |
ABSTRACT |
Phase variation of flagellin gene expression in Campylobacter
coli UA585 was correlated with high-frequency, reversible
insertion and deletion frameshift mutations in a short homopolymeric
tract of thymine residues located in the N-terminal coding region of the flhA gene. Mutation-based phase variation in
flhA may generate functional diversity in the host and environment.
| |
TEXT |
Campylobacter jejuni and
Campylobacter coli are now recognized as the commonest
causal agents of acute bacterial enteritis worldwide (23).
The spiral shape and the characteristic motility, imparted by a single
polar flagellum, of these bacteria are important in their ability to
colonize the viscous mucous blanket lining the intestinal tract
(14). The immune response mounted against the
Campylobacter flagella leads to partial protection against challenge by this pathogen (19), and consequently, events
which lead to the loss of the flagellum may provide campylobacters with a mechanism to escape the host immune response. Such events would also
allow the cell to save energy under circumstances where motility is not
necessary. In this context, some strains of Campylobacter have been shown to undergo both antigenic variation of flagellum expression (6) and phase variation, involving the
bidirectional transition between flagellate and aflagellate phenotypes
(2, 5, 15, 17). Since the basis for this variation is
unknown we sought to characterize the genetic mechanisms governing this process in C. coli.
Isolation of nonmotile phase variants.
C. coli UA585,
originally isolated from a diarrheic pig, was a generous gift from
D. E. Taylor (University of Alberta, Edmonton, Canada). Phase
variants of C. coli UA585 were isolated as described previously (15). After incubation of the phase variants in
Luria-Bertani broth (21) for 48 h at 42°C, plate
counts derived from the cultures revealed equal numbers of motile
(large, swarming morphology) and nonmotile (pinpoint morphology)
colonies. After isolation the nonmotile phase variants could be
maintained as stable cultures. One such nonmotile phase variant
designated C. coli NM3 was chosen for further study.
When cells of C. coli UA585 were grown to exponential phase
in Mueller-Hinton broth (Oxoid-Unipath, Basingstoke, United Kingdom) and assessed for phase variation as described above, the flagellate to
aflagellate transition occurred at a rate of 3 × 10
4 per cell. Transition from the nonmotile to motile
phenotype during exponential growth occurred at a rate of 7 × 106 per cell.
flaA transcription and flaB transcription
are repressed in nonmotile phase variants.
Expression of both FlaA
and FlaB, constituting the Campylobacter flagellin, in the
nonmotile phase variant NM3 was monitored by using a hipO
reporter of gene expression (18). Accordingly, gene fusions,
to both flaA and flaB, were constructed with the fla-hipO integrational vector pHIP108 (18). The
nature of the integrative event in the transformants derived from
pHIP108 and NM3 was confirmed by PCR with the discriminatory primers
FLA1 and FLAB (18). Strains of C. coli NM3 in
which pHIP108 had integrated into either flaA or
flaB were designated CCSFP1231 and CCSFP1241, respectively.
Strains CCSFP1211 and CCSFP1221, which contain flaA- and
flaB-hipO fusions and are derived from the motile parental
strain C. coli UA585 (18), gave rise to 42 and
7.8 U of hippuricase activity, respectively, when expression from the
marker gene fusions was assessed (Table
1). The 5.3-fold difference in levels of expression from flaA and flaB was expected and
has been discussed previously (9, 16, 18). Levels of
expression from the flaA- and flaB-hipO fusions
in the nonmotile variant C. coli NM3 were 13- and 16-fold
lower, respectively, than those monitored from the corresponding
fusions in the motile parental strain. However, in control experiments,
when hipO expression from the same constitutively expressed
hipO fusion, present in either the nonmotile variant CCHP21
or the parental strain (CCHP20) (18), was measured,
hippuricase activity was expressed at broadly equivalent levels. Thus,
the repression of flaA and flaB expression in
C. coli NM3 is a consequence of genetic events which lead to
the specific reduction in transcription from both flaA and
flaB.
Genetic complementation of the locus conferring nonmotility.
We next sought to identify the locus conferring phase variability to
flagellin gene expression, using a genetic complementation strategy.
Genomic libraries based in Campylobacter shuttle plasmids proved unsuitable for this purpose, as the plasmids were unstable in
C. coli. Consequently, we developed a novel procedure to
allow the complementation of the motility mutation. We reasoned that if
the integrational vector pSP105 (4) were integrated randomly into the chromosome of the motile parental strain of C. coli, then in some transformants the integration of the plasmid
would occur proximal to the locus that confers motility to the parental strain but is altered in the nonmotile variant. In effect, this would
locate a tetracycline antibiotic resistance marker close to the
corresponding locus. Thus, if chromosomal DNA derived from a library of
pSP105 integrants were used to transform the nonmotile variant NM3, any
resulting transformants which had acquired tetracycline resistance and,
concomitantly, motility should have been derived from transforming DNA
in which the antibiotic marker was closely linked to the locus
controlling motility.
A library was generated by introducing BglII-digested
C. coli UA585 chromosomal DNA into the corresponding
BamHI site of the integrational vector pSP105
(4). The library was then introduced into the same strain by
natural transformation, and 5.2 × 105 transformants
were recovered. These transformants were pooled, and the chromosomal
DNA, containing randomly integrated pSP105 derivatives, was extracted.
This DNA was next introduced into C. coli NM3 by natural
transformation. Subsequently, a number of transformants that both were
tetracycline resistant and displayed motility were recovered. One
transformant in which tetracycline resistance was clearly linked to the
ability to confer motility was designated CCNMR7 and chosen for further study.
Identification of the mutational basis governing phase
variability.
Plasmid DNA containing the sequences flanking the
site of integration in CCNMR7 was resolved directly from chromosomal
DNA by using NcoI as has been described previously (4,
20). Subsequently, a series of subcloning experiments, using
pSP105 as the cloning vector, localized the locus affecting motility to
a 3.0-kb EcoRI fragment contained in pEMR1 (Fig.
1). The nucleotide sequence of the DNA
insert in this vector was determined and found to correspond to a
region of DNA containing the flhA gene which has been
characterized previously in C. jejuni (12, 13).
Since this region contains four open reading frames, the locus
responsible for controlling motility in the phase variants was
localized by PCR-based cloning strategy (Fig. 1). DNA fragments
generated by PCR using chromosomal DNA from the motile parental strain
as the template were cloned into the integrational vector pSP105, and
the ability of the resulting constructs to confer motility to C. coli NM3 was assessed. In this manner, a 415-bp fragment of DNA,
internal to the flhA gene, was found to restore motility to
the nonmotile variant NM3. As a control to rule out PCR artifacts this
region was amplified by PCR with the primers RPS1 and FLH7 (Fig. 1),
chromosomal DNA from both the motile parental strain and the nonmotile
variant, and three separate reactions to generate fragments for each
chromosomal target. The resulting fragments were cloned into pSP105 to
generate the derivatives pRFT7.1 to -3 and pRNT7.1 to -3, respectively. These plasmids were next introduced into nonmotile derivative C. coli NM3, and the effects on the phenotype were assessed. As anticipated, the plasmids pRFT7.1 to -3, but not pRNT7.1 to -3, conferred motility to this strain, confirming that the DNA inserts represented the chromosomal DNA sequences responsible for the corresponding motility status of the strains from which the fragments were originally amplified. Analysis of the inserted DNA sequences, derived from the motile parental strain, in all three pRFT7 derivatives revealed the presence of a poly T tract containing eight T residues 148 bp downstream of the ATG translational start. In comparison, analysis
of the inserted DNA sequences in all three pRNT7 derivatives, containing DNA derived from the nonmotile variant C. coli
NM3, showed the sequences to be identical to those obtained from the motile parental strain, except for the presence of a deletion, resulting in only seven T residues in the poly T tract. This deletion results in the formation of an in-frame TAG stop causing the premature termination of flhA and the consequent abrogation of its
expression (Fig. 2). A revertant motile
variant derived from C. coli NM3 was also shown to have
corrected the deletion and had restored the poly T tract to eight
residues (data not shown).
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FIG. 1.
Localization of the locus responsible for
phase-variation in C. coli. The plasmid pEMR1 contains a
3.0-kb EcoRI insert from the C. coli UA585
chromosome that confers motility to the nonmotile phase variant NM3.
PCR was used to amplify DNA fragments corresponding to the various
parts of the flhA region. The sites for primer binding are
designated by arrowheads. The primers used were RPS1 (5'
GGATCCGGCCGAATCCAAAGCCATGATAGA 3'), ORF3 (5'
GGATCCCCAACAATAGTCAAGCTTTTAGCT 3'), FLH3 (5'
GGATCCTAAAATTTCAACTTTGAGTATATCGTT 3'), FLH7 (5' GGATCC
TTTGTTTACCCGGCATCGCATCAA 3'), and FLH8 (5' GGATCC
CCTCATCTTTGCTTGCACCAGTGA 3'). All PCR products were cloned into
the integrative vector pSP105 as BamHI fragments. The
ability of the corresponding plasmids to confer motility was assessed
by introducing them into strain MN3 by natural transformation, and each
plasmid was determined to be motile (+) or nonmotile ( ).
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FIG. 2.
Mutational basis generating phase variation of FlhA
expression. Two versions of the FlhA protein as derived from C. coli UA585 (A) and NM3 (B) are represented by the bars. Below each
representation of the protein is the nucleotide sequence which governs
its expression. The poly T tract underlined results in expression of
either full-length FlhA (eight T's) or a truncated version (seven
T's) as a consequence of the deletion of a single T residue, resulting
in the generation of an in-frame termination codon. The nucleotides are
numbered from the ATG start of flhA. The nucleotide
sequences corresponding to flhA containing poly T tracts of
eight and seven residues appear in the GenBank database under accession
no. AF171083 and AF171084, respectively.
|
|
Conclusion.
High-frequency phase variation of flagellin gene
expression in C. coli UA585 was correlated with insertion
and deletion mutations in a short poly T tract in the flhA
gene. FlhA is a member of the LcrD/FlbF family, whose members are all
integral cytoplasmic membrane proteins involved in the regulation or
secretion of surface or extracellular proteins (7). In
particular, mutations in flhA homologues result in the loss
of expression of flagellin-related genes. Indeed, inactivation of this
gene in C. jejuni resulted in the failure to synthesize
flagellin (13). It is clear from the present study that
inactivation of the flhA gene can occur naturally by a
localized frameshift mutation which leads to nonmotility in C. coli, and that this phenotype is, at least partly, a consequence of the failure of cells to transcribe either flaA or
flaB. The precise function of FlhA is unknown, and it is not
clear whether its involvement in controlling the motility of cells is
direct or indirect. In Salmonella typhimurium, for example,
regulation of flagellin gene expression may be coupled to the
expression of other components involved in flagellum formation
(8). Consequently, mutations in genes encoding proteins in
the flagellum basal body or switch complex lead indirectly to the
repression of flagellin genes. In contrast, in Helicobacter
pylori, which is closely related to C. coli, while
inactivation of the flhA gene leads to repression of FlaA
and FlaB expression, the mechanism of this inactivation is thought to
be independent of the feedback mechanism described above for S. typhimurium, and accordingly, a more direct role for FlhA in the
regulation of expression of flagellum components is envisaged
(21).
Whichever mechanism leads to the abrogation of flaA and
flaB expression, it is clear that the end result is a
significant reduction in macromolecular synthesis within the cell and a
conservation of its biosynthetic capacity under circumstances when
motility is not necessary. Furthermore, flagellum phase variation may
provide C. coli with the possibility of escaping the host
immune response against the flagellum.
Translational variation caused by frameshift mutations has been shown
to be a widespread mechanism for generating selective phase variation
in virulence-associated products in a number of bacterial pathogens
(3, 11, 24, 26). This is the first report demonstrating that
this process also operates to generate functionally variant cells in
campylobacters. Interestingly, the flhA gene sequences of
C. jejuni 81-176 (12, 13) and NCTC 11168 (http://www.sanger.ac.uk/Projects/C_jejuni) do not contain the eight-T
homopolymeric tract of the C. coli gene sequence, and
consequently phase variation of flagellin gene expression in this
species may occur by a different mechanism.
Given the high A+T ratio of the Campylobacter spp.
(1) it is likely that the genome contains numerous poly A/T
tracts and that, therefore, localized hypermutation in short
homopolymeric tracts is a process which operates at a number of other
sites on the C. coli genome. Indeed, a preliminary analysis
of the genome sequence of C. jejuni, a close relative of
C. coli, reveals the presence of at least 25 polymorphic
regions that correspond to repeat structures, which may represent
potential frameshift mutator elements
(http://www.sanger.ac.uk/Projects/C_jejuni). The presence of these
short sequence repeats may, in part, contribute to the high degree of
phenotypic and genomic variability reported for campylobacters
(25). The frequency of slipped-strand mispairing, and thus
mutation at these sequences, may also be influenced by DNA repair
systems. For instance, Escherichia coli strains with mutations in mismatch repair activity are more prone to strand slippage
events (10). The presence of a MutS homologue in C. jejuni, as indicated by analysis of the genome sequence
(http://www.sanger.ac.uk/Projects/C_jejuni), suggests that the
capacity for mismatch repair exists. At present, however, it is not
clear whether this operates in all strains and what effect it has on
the frequency of phase variation.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: School of
Biological Sciences, University of Surrey, Guildford, GU2 5XH, United
Kingdom. Phone: 44 (0)1483 879024. Fax: 44 (0)1483 300374. E-mail:
s.park{at}surrey.ac.uk.
| |
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Journal of Bacteriology, January 2000, p. 207-210, Vol. 182, No. 1
0021-9193/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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