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Previous Article | Next Article 
Journal of Bacteriology, September 2000, p. 5256-5261, Vol. 182, No. 18
Department of Microbiology, The University of
Sydney, Sydney, N.S.W. 2006, Australia
Received 8 March 2000/Accepted 21 June 2000
O antigen is part of the lipopolysaccharide present in the outer
membrane of gram-negative bacteria. Escherichia coli and Salmonella enterica each have many forms of O antigen, but
only three are common to the two species. It has been found that, in general, O-antigen genes are of low GC content. This deviation in GC
content from that of typical S. enterica or E. coli genes (51%) is thought to indicate that the O-antigen DNA
originated in species other than S. enterica or E. coli and was captured by lateral transfer. The O-antigen
structure of Salmonella enterica O35 is identical to that
of E. coli O111, commonly found in enteropathogenic E. coli strains. This O antigen, which has been shown to be
a virulence factor in E. coli, contains colitose, a
3,6-dideoxyhexose found only rarely in the
Enterobacteriaceae. Sequencing of the O35-antigen gene
cluster of S. enterica serovar Adelaide revealed the
same gene order and flanking genes as in E. coli O111. The divergence between corresponding genes of these two gene clusters at
the nucleotide level ranges from 21.8 to 11.7%, within the normal
range of divergence between S. enterica and E. coli. We conclude that the ancestor of E. coli and
S. enterica had an O antigen identical to the O111 and O35
antigens, respectively, of these species and that the gene cluster
encoding it has survived in both species.
Lipopolysaccharide, an important
component of the outer membrane of gram-negative bacteria, usually
consists of three distinct regions: lipid A, core oligosaccharide, and
O-specific polysaccharide (O antigen). O antigens consist of repeats of
an O unit of generally two to six sugars. The genes for O-antigen
synthesis are normally grouped together on the chromosome in a gene
cluster which maps close to gnd in both Escherichia
coli and Salmonella enterica. We, among others, have
undertaken an extensive study of the genetic basis of O-antigen
variation by sequencing and identifying the O-antigen genes, mostly in
S. enterica and E. coli (see article by Reeves
[34, 35] for review). It has been found that, in general, O-antigen genes are of low G+C content (usually less than
40%). We suggested that this deviation in G+C content from that of
typical S. enterica or E. coli genes (51%)
indicates that the O-antigen DNA originated in species other than
S. enterica or E. coli and was captured by
lateral transfer (16). By sequencing and comparison of
O-antigen gene clusters, we and others have previously found evidence
that DNA recombination events between O-antigen gene clusters within
S. enterica (9, 47) and between E. coli and Klebsiella (41) played a role in
the formation of new O-antigen forms. We also found evidence for an
interspecies transfer of an entire O-antigen gene cluster (J. G. Shepherd, L. Wang, and P. R. Reeves, submitted for publication).
The O antigens of S. enterica and E. coli are
extremely diverse, with 54 and 190 known forms, respectively,
recognized in their typing schemes (23, 32) (includes
Shigella strains in E. coli on the basis of high
sequence similarity [8, 10, 13, 28, 33]). In a few
instances, there is a serological cross-reaction between E. coli and S. enterica serotypes due to the presence of
the same or a similar sugar in their O antigens (11).
However, there are only three cases in which the O-antigen structures
have been shown to be identical in the two species: E. coli
O111 and S. enterica O35 (18), E. coli
O55 and S. enterica O50 (18, 22), and E. coli O157 and S. enterica O30 (31). It is
noteworthy that in E. coli, all three O antigens are
associated with enteropathogenic E. coli (EPEC) and
sometimes enterohemorrhagic E. coli (EHEC) strains.
Nonetheless, there is no obvious relationship between the three
O-antigen structures other than that O111 and O55 both contain
colitose, and there is no close relationship between the gene clusters
for E. coli O111 and O157. (The sequence of O55 is not
known.)
The low proportion of forms present in both species suggests that there
has been extensive turnover of O antigens, presumably by lateral gene
transfer since divergence of the two species, because the majority of O
antigens, found in only one of the species, must have been gained or
lost by one of them since divergence. This may well be due to selection
by the host immune system, because the surface-exposed O antigen is
highly immunogenic and the antibody has been shown to be protective,
providing strong selection for O antigens not previously seen by the
usual host of any given clone. This may account both for the
maintenance of many different O-antigen forms and, due to changes in
environmental circumstances, for the turnover of forms present in a species.
It is believed that E. coli and S. enterica
diverged from a common ancestor about 140 million years ago (29,
30). The very small proportion of O antigens common to both
suggests that most of the polymorphism arose after the divergence. We
present here the genetic basis for the identity of O antigens shared
between S. enterica O35 and E. coli O111. There
are three possible explanations for the presence of a common O antigen,
and one could distinguish between them by comparison of the sequences
of the two O-antigen gene clusters. The first possibility is that the
two gene clusters are derived from a common ancestral gene cluster
present in the ancestor of E. coli and S. enterica: one would expect the two gene clusters to share overall
organization and have a high level of identity, with sequence
divergence in the range of that for E. coli and S. enterica housekeeping genes. The second possibility is that the
two gene clusters were assembled separately after the divergence of
E. coli and S. enterica or acquired from
different sources: the two gene clusters need not have the same gene
cluster structure and could be highly divergent in sequence. The third possibility is that the two gene clusters were separately transferred from a common source into E. coli and S. enterica
after the species diverged or were recently transferred from one to the
other: the two gene clusters would have a common organization of genes
and a higher level of DNA identity. We have already cloned and
sequenced the E. coli O111 gene cluster (5, 6,
44). In this study, we sequenced the O-antigen gene cluster and
flanking genes from an O35 S. enterica serovar Adelaide
strain and compared this sequence with that of E. coli O111.
Sequencing the O-antigen gene cluster of S. enterica
O35 (serovar Adelaide).
Oligonucleotides which bind to the 5' end
of the gnd gene
(5'-CACTGCCATACCGACGACGCCGATCTGTTGCTTGG) and the middle of
the JUMPstart sequence (5'-ATTGGTAGCTGTAAGCCAAGGGCGGTAGCGT)
were used for PCR amplification of the O-antigen gene cluster
from S. enterica serovar Adelaide strain M274. Long PCR was
carried out by using the Expand Long Template PCR System from
Boehringer. The PCR cycles were as follows: denaturation at 94°C for
10 s, annealing at 65°C for 30 s, and extension at 68°C
for 15 min. The 39-bp JUMPstart sequence is present upstream of many
polysaccharide gene clusters (15), and the gnd
gene is present downstream of typical O-antigen gene clusters of
E. coli and S. enterica.
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
The Escherichia coli O111 and Salmonella
enterica O35 Gene Clusters: Gene Clusters Encoding the Same
Colitose-Containing O Antigen Are Highly Conserved
ABSTRACT
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Comparison of the two O-antigen gene clusters.
The O antigens
of E. coli O111 and S. enterica O35 contain
colitose, D-glucose, D-galactose, and
N-acetyl-D-glucosamine (18). There
are 11 genes in the E. coli O111 gene cluster (Fig.
1) (44), and in the S. enterica O35 gene cluster, we found the same 11 genes in the same
order (Fig. 1). There are five genes (manB, manC,
gmd, wbdK, and wbdJ) of the putative
GDP-colitose pathway. ManB, ManC, and Gmd have functions established
biochemically which lead to 4-keto-6-deoxy GDP-mannose, an intermediate
in other pathways, while WbdK and WbdJ are proposed on the basis of
homologies to complete the synthesis of GDP-colitose (44).
There are three presumptive sugar transferase genes (wbdH,
wbdL, and wbdM) for synthesis of the O unit: the
O-unit flippase gene (wzx), the O-antigen polymerase gene
(wzy), and gmm (originally named wbdI)
(44).
|
4 × 10
35) after several iterations. The Wzx
proteins of E. coli O111 and S. enterica O35 B
grouped with putative Wzx proteins of E. coli O157 (GenBank
entry AF061251), S. enterica B (GenBank entry X56793),
E. coli O16 (GenBank entry U09876), and E. coli O113 (GenBank entry AF172324), and also distantly related Wzx proteins,
but no other proteins were retrieved (E-value, 4 × 1020) after several iterations. The S. enterica B wzy and wzx genes have been
identified biochemically, and the motif searches give very strong
support to the original identifications.
With the exception of gmm, these genes are those expected
for synthesis of the repeat unit plus the expected flippase and polymerase genes. The gmm gene encodes GDP-mannosyl
hydrolase (12), which would remove GDP-mannose from the
GDP-colitose pathway. Notably, in addition to manB,
manC, and gmd, gmm is found in the gene cluster for E. coli O157 (46) and the
colanic acid gene clusters in E. coli and S. enterica (39; G. Stevenson, R. Lon, and P. R. Reeves, submitted for publication), which all contain fucose. The
GDP-fucose pathway has been fully characterized. It starts with
fructose-6-phosphate, which is converted by the enzyme encoded by
manA (a housekeeping gene) into mannose-6-phosphate. Enzymes
encoded by manB and manC then convert
mannose-6-phosphate into GDP-mannose. The next enzyme in the GDP-fucose
pathway is Gmd (GDP-D-mannose 4, 6-dehydratase), which
produces 4-keto-6-deoxymannose, and the final steps to make
GDP-L-fucose are catalyzed by Fcl. The GDP-colitose
synthesis and GDP-fucose pathways diverge after gmd, and so
share the first three steps (44). This distribution suggests
that gmm is involved in some form of regulation in E. coli and S. enterica GDP-sugar pathways that continue
beyond GDP-mannose. However, gmm is not present in the
GDP-fucose pathway of the Yersinia enterocolitica O8 pathway
(48). All enzymes in the GDP-fucose pathway have previously
been defined biochemically (2, 39).
Comparison of the proteins encoded by the two gene clusters (Fig. 1)
showed that the proteins of the six GDP-colitose-related genes had
identity levels of between 87.3 and 94.9%; the three potential
transferases, WbdH, WbdL, and WbdM, had identity levels of 74.9 to
82.8%; and the O-antigen flippase and polymerase had identity levels
of 82.5 and 74.9%, respectively.
The intergenic regions between galF and the first O-antigen
gene (wbdH) are 540 and 519 bp in length, respectively, in
S. enterica O35 and E. coli O111. These two
sequences share about 64% identity. There are stronger similarities
between the two sequences in the 39-bp JUMPstart sequence (located
about 200 bp 5' to wbdH) and a region of 20 bp just upstream
of wbdH. The JUMPstart sequence is involved in the
expression of O-antigen gene clusters (45), and there are
only 4 base substitutions in this region. Two segments of 20 bp,
located 5 and 4 bp upstream of the start of wbdH in S. enterica O35 and E. coli O111, respectively, are identical between these two strains, except for a single base present
in O35, but absent in O111.
The intergenic regions between the last O-antigen genes
(wbdM) and gnd are 180 and 177 bp in length in
S. enterica O35 and E. coli O111, respectively,
and share about 74% identity. The last 49-bp fragments of these two
regions share 91% identity. This 49-bp segment is part of the
regulatory region for gnd and was previously reported to be
conserved among E. coli strains and between E. coli and S. enterica strain LT2 (3, 4).
Evolutionary origins of these two gene clusters. Like many O-antigen gene clusters, the O111 cluster is of low GC content and is thought to have been introduced into E. coli by lateral gene transfer (5, 44). The S. enterica O35 gene cluster encoding the same O antigen also has a low GC content, and the same argument applies. The two gene clusters also have the same organization and are clearly closely related.
E. coli and S. enterica diverged about 140 million years ago (29, 30), and typical homologous proteins are, on average, 93% identical in the two species, ranging from 76.3 to 100% (38). The identity between proteins encoded by the E. coli O111 and S. enterica O35 antigen genes ranges from 74.5 to 94.9%, so our sequence data are consistent with the two gene clusters being in the common ancestor of E. coli and S. enterica. The two O-antigen gene clusters are of low GC content, the averages for E. coli O111 being 44.55, 32.73, and 22.98% for codons 1 (P1), 2 (P2), and 3 (P3) and 44.65, 32.17, and 21.85% for O35, with overall GC contents being 0.334 and 0.329, respectively. It is most likely that the ancestral gene clusters were assembled in a low-GC-content organism and later underwent lateral gene transfer to the ancestor of E. coli and S. enterica. We attempted to use the expected changes in GC content after lateral transfer to provide an independent estimate of time since transfer to E. coli or S. enterica. Bacterial species display wide variation in overall GC content, but the genes within any particular species are generally similar in base composition. For example, Sueoka (40) found that in E. coli, more than 82% of genes have a similar GC content (20), and Muto and Osawa (27) presented plots for the GC content of each codon base (P1, P2, and P3) against the genomic GC content, using average data for each species. The three plots are quite different, because each codon position is under different constraints. DNA transferred by lateral transfer would begin with the base composition of the donor genome at the time of the transfer, but would then be subject to the same mutational process affecting all genes in the recipient genome and over time would ameliorate to reflect the DNA composition of the new genome. The bases at the three codon positions would adjust at different rates due to different constraints on base change, and during this adjustment process, known as amelioration, they would not conform to the usual relationship for GC content at the three codon positions. This principle can be used to estimate time since lateral transfer. Sueoka (40) (using data from Muto and Osawa) looked at genes from species with different GC contents and plotted regression of P1 and P2 against P3. The value for P3 was taken to represent the equilibrium value for that species, because at most codons, the third base can be substituted for by the transition alternative without a change of amino acid, and hence in general without a significant effect on fitness. The regression lines reflect the long-term equilibrium between mutational drive for change in GC content and the constraints of the effect on amino acid composition. We superimposed the data for the O111 and O35 gene clusters on the Sueoka (40) regression plots (Fig. 2). The value of P3 is higher than predicted by the Sueoka regression line for the observed value for P1 or P2. This is as expected for genes which have had time for random genetic drift after transfer from a low-GC-content species to a species with GC content of about 0.5, as found in E. coli, S. enterica, and, presumably, their ancestor.
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Distribution of the E. coli O111 or S. enterica O35 O antigen. It is interesting that the E. coli O111 or S. enterica O35 O antigen, which we now believe to have been in both E. coli and S. enterica since divergence, is currently known for its association with EPEC and EHEC pathogenic forms of E. coli, which are generally thought to have arisen recently in evolutionary terms, with key genes involved in pathogenicity present on plasmids. It seems probable that the O111 antigen was in E. coli before the arrival of these plasmids and hence was not in strains occupying a niche involved in the EPEC or EHEC mode of pathogenesis.
The situation for O35 of S. enterica is also interesting. There are 46 different O antigens present in 2,422 serovars of S. enterica (32, 36). Seven subspecies in S. enterica have been defined by biotyping, and, with few exceptions, phylogenetic trees constructed for individual genes match the subspecies tree (7, 42). The distribution of each O antigen among the subspecies varies, with many found predominantly in one or two subspecies (36). Fifty-four of the 2,422 serovars carry the O35 O antigen, with 22, 7, 5, and 20 serovars in subspecies I, II, IIIa, and IIIb, respectively. Taking into account that there are 1,430, 478, 95, and 319 serovars, respectively, in the four subspecies, it is clear that O35 has a major presence in subspecies IIIa and IIIb, where it is found in 5 and 6% of serotypes, respectively. This may indicate that the O35 antigen has been in S. enterica subspecies IIIa and IIIb serovars for a long time and only recently was transferred into subspecies I and II serovars. Subspecies IIIa and IIIb serovars are generally associated with cold-blooded vertebrates, and subspecies I and II are associated with warm-blooded animals. It appears that antigen 35 has relatively recently transferred to subspecies I and II, where it is a significant antigen, with serovar Adelaide the 45th most frequently isolated S. enterica subspecies I serovar around the worldwide in a survey of isolates from 1934 to 1975 (17).General conclusion. Comparison of the gene clusters for the O antigen known as O35 in the S. enterica scheme and O111 in the E. coli scheme indicates that this O antigen was present in the common ancestor of E. coli and S. enterica and has been retained in both species, while most O antigens are present in one or the other species only. It remains for further work to establish if the other two O antigens present in both species were also in the common ancestor. The current distribution of this antigen in S. enterica suggests that it is involved in relatively recent adaptations, so that its long-term survival does not imply continuity of any given niche over the long period of time that this O antigen has been present in this lineage.
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ACKNOWLEDGMENTS |
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We thank Kanella Andrianopoulos for technical assistance.
This study was supported by the Australian Research Council.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Microbiology, The University of Sydney, Sydney, N.S.W. 2006, Australia. Phone: (612) 351 2536. Fax: (612) 351 4571. E-mail: reeves{at}angis.org.au.
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