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Applied and Environmental Microbiology, August 2000, p. 3310-3329, Vol. 66, No. 8
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
A Genomic Sample Sequence of the Entomopathogenic
Bacterium Photorhabdus luminescens W14: Potential
Implications for Virulence
Richard H.
Ffrench-Constant,1,*
Nicholas
Waterfield,1
Valerie
Burland,2
Nicole T.
Perna,2
Phillip J.
Daborn,1
David
Bowen,3 and
Frederick
R.
Blattner2
Department of Biology and Biochemistry, University of Bath,
Bath, BA2 7AY, United Kingdom,1 and
Laboratory of Genetics,2 and
Department of Entomology,3 University of
Wisconsin-Madison, Madison, Wisconsin 53706
Received 6 March 2000/Accepted 25 May 2000
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ABSTRACT |
Photorhabdus luminescens is a pathogenic bacterium that
lives in the guts of insect-pathogenic nematodes. After invasion of an
insect host by a nematode, bacteria are released from the nematode gut
and help kill the insect, in which both the bacteria and the nematodes
subsequently replicate. However, the bacterial virulence factors
associated with this "symbiosis of pathogens" remain largely obscure. In order to identify genes encoding potential virulence factors, we performed ~2,000 random sequencing reads from a P. luminescens W14 genomic library. We then compared the sequences obtained to sequences in existing gene databases and to the
Escherichia coli K-12 genome sequence. Here we describe the
different classes of potential virulence factors found. These factors
include genes that putatively encode Tc insecticidal toxin complexes,
Rtx-like toxins, proteases and lipases, colicin and pyocins, and
various antibiotics. They also include a diverse array of secretion
(e.g., type III), iron uptake, and lipopolysaccharide production
systems. We speculate on the potential functions of each of these gene classes in insect infection and also examine the extent to which the
invertebrate pathogen P. luminescens shares potential
antivertebrate virulence factors. The implications for understanding
both the biology of this insect pathogen and links between the
evolution of vertebrate virulence factors and the evolution of
invertebrate virulence factors are discussed.
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INTRODUCTION |
Photorhabdus luminescens
is an insect-pathogenic gram-negative proteobacterium that forms a
"symbiosis of pathogens" with insect-pathogenic nematodes
(52). In this symbiosis the bacteria are carried in the guts
of entomopathogenic nematodes belonging to the family Heterorhabditidae
(members of a different group of bacteria, Xenorhabdus spp.,
are carried in the guts of members of a different group of nematodes,
the Steinernematidae). Upon invasion of an insect host by a nematode,
the bacteria are released from the gut directly into the open blood
circulatory system of the insect, the hemocoel (52). Here
the bacteria are thought to release a wide variety of potential
virulence factors, including high-molecular-weight toxin complexes
(Tc), lipopolysaccharide (LPS), proteases, lipases, and a range of
different antibiotics (52). Inferences concerning the
involvement of these factors in killing of the insect or in overcoming
the insect immune system, however, often result merely from
documentation of secretion of the factors into bacterial culture
supernatants. Studies examining the precise role of virulence factors
during the infection process in insects have not been performed, and
studies of Photorhabdus mutants are rare. As a prelude to
genetic analysis of potential virulence factors in P. luminescens, we were interested in obtaining a sample sequence of
strain W14 in order to document the classes of genes present and to
begin to design suitable experiments for analysis of the genes based on
a likely idea of their functions.
The relative advantages of sample sequence analysis versus full-scale
analysis of a finished bacterial genome have been discussed elsewhere
(119). However, there are several points relevant to the
current discussion, as discussed briefly below. First, a sample sequence can be completed at a fraction of the cost of completion of a
full genome. Second, a surprisingly high percentage of the genome can
be captured even with a 1× sample sequence. Given the current
uncertainty concerning the exact genome size of P. luminescens, the percent coverage obtained in this study is hard
to estimate; however, McClelland and Wilson (119) suggested
that a 1× genome equivalent for the 4.78-Mbp Salmonella
typhi genome would require only 12,000 reads of 400 bases. Such
coverage would ensure that almost every cistron was represented in the
sample sequence. The 2,000 reads reported here obviously do not give
this level of coverage, but, as shown below, even the limited sample
sequence obtained revealed ample evidence concerning the types of
virulence systems that P. luminescens may employ in its
complex life cycle.
Although few potential P. luminescens virulence factors have
been examined in detail (either biochemically or genetically), we can
attempt to predict the likely role of bacterial virulence systems in
killing an insect, in overcoming an insect immune system, or in
facilitating bacterial and/or nematode growth. It is thought that once
P. luminescens is released from the nematode gut into the
insect hemocoel, it plays multiple roles in helping the nematode overcome its host (52). To do this, the bacteria need to
overcome both the cellular (hemocytic) and peptide-mediated
(antibacterial polypeptide) components of the insect immune system.
Furthermore, the bacteria stop the insect from feeding and probably
render its tissues suitable for consumption by both the bacteria and the nematodes. Anti-insect virulence mechanisms might, therefore, include, but not be limited to, toxins active against the insect gut
and/or hemocytes and enzymes (such as proteases) capable of both
degrading insect tissue and disabling the antibacterial peptides also
associated with the insect immune system. Equally important in its role
in overcoming an insect host, P. luminescens must ensure
that the insect cadaver does not act as a breeding ground for
opportunistic soil bacteria, fungi, and/or other species of nematodes.
We might, therefore, expect P. luminescens to secrete a wide
range of antimicrobial, antifungal, and nematicidal compounds, as
previously documented by other workers (52). The aim of the present study was, therefore, to identify genes that encode likely virulence factors as a prelude to a functional analysis of the genes
via targeted knockout and assay of the resulting mutants in the host
infection process. Not only should such an analysis allow us to
elucidate how the virulence factors act on the insect, but the gene
sequences may also provide an indication of the evolution and potential
origins of the virulence factors.
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MATERIALS AND METHODS |
Genomic library construction and sequencing.
Genomic DNA
from P. luminescens W14 was size selected to obtain 1- to
2-kb fragments and then cloned into M13 Janus as previously described
(28, 115). DNA templates were purified from library clones
and sequenced by using dye terminator-labeled fluorescent cycle
sequencing (model ABI377 automated sequencer; Applied Biosystems Division, Perkin-Elmer). Single sequencing reads (average length, ~400 bp) were obtained for one end of 2,122 clones. Sequences were
truncated to exclude the phage arms and multiple cloning site and were
then submitted to the BLASTX servers at the National Center for
Biotechnology Information. Clones giving hits to either Tc-, protease-,
or Rtx-like-encoding genes were then sequenced from the other end or
"flipped."
Comparison with Escherichia coli K-12.
Trimmed
(vector removed and high-quality trim with SeqManII) P. luminescens sequence reads were searched against the DNA and protein sequences of E. coli MG1655 by using BLASTN and
BLASTX with a local server. The output was parsed and sorted to give three subsets of data with different levels of identity. No alignment length criteria were imposed on the output. The results, therefore, included short alignments and multiple hits for many sequences, all of
which were legitimate similarities.
Nucleotide sequence accession number.
The nucleotide
sequence determined in this study has been deposited in the
DDBJ/EMBL/GenBank database under accession no. AQ989457-AQ991805.
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RESULTS AND DISCUSSION |
Comparison with E. coli K-12.
The results of the
comparison of P. luminescens sequences with E. coli K-12 sequences are shown in Fig.
1. Even though the number of query
sequences was relatively small (<0.5× genome coverage), we clearly
observed that there is significant conservation of sequences,
particularly protein sequences, between the two genomes, which is
consistent with the relatively close phylogenetic relationship of the
two organisms (both are members of the family
Enterobacteriaceae). Regions of the genome conserved in
Escherichia and Photorhabdus strains begin to
define the components of the putative ancestral chromosome of members
of the gamma subdivision of the class Proteobacteria. The
large excess of hits at the protein level compared to the DNA level at
all stringencies suggests that the divergence between orthologous
sequences is sufficient to obscure true matches at the nucleotide
level. Even the number of protein hits changed extensively as we varied
the criteria for a significant match. Thus, we were reluctant to choose
an arbitrary cutoff for determining orthology (as has been done for
other sample sequence comparisons) and instead describe three different
levels of stringency below. This form of presentation provides not only
a sense of the absolute number of sequences that are similar but also a
sense of the strength of the similarities. It should be noted that
although the hits are distributed, albeit unevenly, around the K-12
map, this does not necessarily indicate that there is colinearity, and
indeed the sizes of the two genomes are probably different, which could account for some of the gaps and sparse regions in Fig. 1. In all,
1,133 W14 clones exhibited no significant matches in even the
lowest-stringency analysis (E < E
05),
and from this we inferred that approximately 53% (1,133 of the 2,122 clones examined) of the P. luminescens genome is clearly distinct from the genome of E. coli K-12.
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FIG. 1.
Graphic display of sample sequence similarities to
E. coli K-12 nucleotide and protein sequences, generated
from a BLAST search of P. luminescens sequences performed
with K-12. The three concentric sets of data show nucleotide (outer
ring) and protein (inner ring) hits plotted at the coordinates of the
K-12 target. From the outside, the three data sets show hits with BLAST
expected value (E) limits of <10e05 (2,765 protein and 729 nucleotide hits), <10e20 (1,227 protein
and 376 nucleotide hits), and <10e40 (664 protein and
234 nucleotide hits), respectively. The positions of the genetic
markers ori, ter, and rrnA through
rrnH are shown as landmarks to orient the circle. The figure
was generated by using the program Genescene (DNASTAR).
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Old and new toxin complex (tc) loci.
We previously cloned and sequenced four Tc-encoding loci,
tca, tcb, tcc, and tcd,
from P. luminescens W14 (22); each of these loci
encodes a different high-molecular-weight insecticidal Tc (Tca, Tcb,
Tcc, and Tcd, respectively). The Tc proteins are secreted into the
supernatant by P. luminescens grown in liquid culture
(23). Despite the fact that the Tc toxins exhibit both oral
and injectable activity against a range of insects (22, 23),
their precise role as potential virulence factors in the infection
process remains to be determined. However, one of the complexes, Tca,
has highly specific histopathological effects on the lepidopteran
midgut (18), suggesting that Tca proteins may be used by the
bacterium to destroy the insect midgut and effectively stop feeding. In
the sample sequence analysis, BLASTX searches gave 19 hits for the four
known tc loci (22), but 27 additional sequences
(Table 1) were also identified that could not be ascribed to the previously identified tc loci after
careful examination of the sequence chromatographs (Fig.
2A). This suggests that there are other
tc-like loci in the P. luminescens W14 genome in
addition to those already reported. The matches with new
tc-like loci were classified as tca-like (3 hits), tcc-like (13 hits), or tcb/tcd-like (11 hits; tcb and tcd are close homologs of one another).
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FIG. 2.
Diagrams showing the relative locations of hits to known
tc loci and new tc-like loci. (A) Locations of
individual sequencing reads (arrows above the diagrams) and their
associated contigs and BLASTX matches (boxes below the diagrams). Note
that the predicted amino acid sequences for tcb and
tcd are sufficiently similar that we could not distinguish
matches with either locus. (B) One example of a difference in genomic
organization of a new tc-like locus inferred from a small
contig and adjacent flipped sequence. Note that two TccC-like BLASTX
matches are located next to a TcaC-like ORF with a phage remnant in
between (see text). aa, amino acid.
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The hypothesis that there are more than four
tc loci in the
W14 genome was confirmed by several other lines of evidence. First,
extended sequencing of DNA surrounding the
tcdA locus
revealed
not only the presence of a second open reading frame (ORF)
immediately
downstream of
tcdA (designated
tcdB)
but also the presence of
a second
tccC-like locus further
downstream from the
tcdAB locus
(unpublished results). As
suggested by the sample sequence, this
proves that there are at least
two copies of
tccC in the W14 genome.
Second, sequencing of
the opposite ends of flipped
tc-containing
clones showed
that some of the new
tc-like loci occupy novel genomic
positions beyond the positions established for the four known
loci. For
example, clone 02349 is a
tccA-like sequence whose flip
(clone 02349f) is a
lon protease, and clone 01515 is a
tccB-like
sequence whose flip is an exochitinase. Clone
00763 contains a
tccC-like sequence which forms a contig
with three other clones
(00763f, 00339, and 02380), which also contain
a
yfiP-encoded
lipase. Finally and perhaps most
interestingly, one sequence (00357)
contains both
tccC-like
and
tcaC-like sequences but has phage
sequences inserted
between them (Fig.
2B shows the implied genomic
organization of this
contig). The abundance and potential implications
of phagelike
sequences in the
P. luminescens W14 genome are discussed
below. However, together, the sequence and inferred position data
provide firm evidence that additional
tc loci are present in
the
W14 genome. The implications for the potentially increased variety
of encoded insecticidal Tc toxins remain
unclear.
Antibiotics and antibiotic resistance.
Having destroyed the
insect gut, presumably by using the tc-encoded Tc
(18), P. luminescens must then defend the insect cadaver from a wide range of other colonizing organisms, such as
bacteria (including other strains of P. luminescens), fungi, and/or nematodes. It seems reasonable to assume that during this process P. luminescens W14 deploys a range of antimicrobial
agents, such as antibiotics and antifungal agents, as documented for
other Photorhabdus strains and also Xenorhabdus
strains (52), in order to maintain a bacterial monoculture
in the insect cadaver. Thus, in the sample sequence one of the largest
classes of hits was hits for polyketide synthetase-like genes. This
class of genes is responsible for nonribosomal synthesis of a diverse
array of compounds involved in processes ranging from fatty acid
synthesis to antibiotic production (including production of inhibitors
of eukaryotic protein phosphatases [41]). Even if we
took into account the effects of the large sizes of some of the
polyketide synthetase loci (up to 28 kb of repeated subunits), these
classes of hits were still some of the predominant classes of hits in the sample sequence, accounting for 3.7% (80 hits) of the total sequences. Of the matches with polyketide synthetase-like sequences, 31 were with a syringomycin synthetase from Pseudomonas
syringae pv. syringae (Table 2).
Interestingly, the syringomycin synthetase gene cluster is thought to
provide a link between prokaryotic and eukaryotic peptide synthetases
(62), while syringomycin itself has a wide range of
antibacterial and antifungal properties. Deployment of similar
antibiotics by P. luminescens W14 may, therefore, help
maintain a bacterial monoculture in an insect cadaver. Furthermore, it
is interesting to note that P. luminescens also contains a sequence that is similar to tolaasin (another lipodepsipeptide), which
is used for self-protection in Pseudomonas tolaasii, which implies that W14 may employ this peptidoglycan-associated lipoprotein in self-protection against its own antibiotics. In addition to potentially deploying broad-spectrum antibiotics to repel other organisms that might colonize the insect cadaver, strain W14 also contains sequences similar to colicin activity proteins (CeaAB), colicin transport proteins (BtuB), and pyocin immunity proteins (S3). A
sequence similar to colicin lysis protein was not found, although there
was a match with a similar VlyS lysis protein S from lambda phage
(BLASTX E value, 2e-16). Although the role of the colicin-
or pyocin-like sequences in P. luminescens remains to be
determined, they may be used to produce toxins and antitoxins designed
to kill non-self bacteria.
In addition to genes for specific mechanisms for antibiotic production
and self-protection, the W14 genome contains numerous
sequences that
exhibit homology to genes for other antibiotic
resistance mechanisms.
These sequences include genes involved
in resistance to penicillin
(penicillinase and penicillin-binding
protein), bicyclomycin, and a
range of other antibiotics (tetracycline,
rifampin, and kasugamycin)
via a variety of different mechanisms
(Table
3). Most notable in this respect are the
large number
of sequences that exhibit homology to genes for different
multiple-drug-like
export systems, including Emr-like and Mdl-like
systems that export
drugs ranging from chloramphenicol to acriflavin.
These multiple-drug
export systems are also very similar to the
hemolysin B export
systems, as discussed below, and begin to describe a
large family
of exportlike genes in the
P. luminescens
genome. Also present
are sequences similar to cation resistance genes
in other enteropathogenic
bacteria, notably sequences that encode
resistance to tellurite
(TelA) in
E. coli plasmid RK2 (Table
3).
Rtx-like homologs.
Another large class of database matches
comprises sequences similar to both Rtx-like and hemolysin A-like
toxins and their associated export systems (Table
4). The RTX (repeats in toxin) toxins are
cytolytic toxins that are virulence factors in many pathogenic
gram-negative bacteria (182). The RTX elements of other
gram-negative bacteria share certain aspects of genomic organization,
including the presence of three elements: an exported protein
(RtxA-like), an ATP-binding cassette ABC protein (RtxB-like), and a
membrane fusion protein (RtxD-like). Figure
3 shows the sequences similar to
each of these elements alongside the loci to which they are most
similar as determined by BLASTX searches. This figure shows that the
Photorhabdus sample sequence contains sequences similar to
the sequences of RtxA and RtxB of Vibrio cholerae, ShlA and
ShlB of Serratia marcescens, EthA and EthB of Erwinia
tarda, and HecA and HecB of Erwinia chrysanthemi. We also discerned sequences similar to both HlyB and CvaA/CvaB of E. coli, which are involved in hemolysin secretion and colicin V
secretion, respectively. Notably, even if we took into account the
large predicted ORF size (size of rtxA, ~12 kb), there
were still 24 hits with RtxA-like sequences alone, suggesting that more
than one locus may be present. Furthermore, BLASTX E values were highly significant (e-25 to e-78), suggesting that there is a high
level of amino acid conservation. We also observed that there is a
sequence similar to TolC which is unlinked but is required both for
hemolysin export and for colicin V export (58). We can only
speculate as to the number of loci that these sequences correspond to
and to the likely role of the encoded toxins in P. luminescens infection. However, given the propensity of Rtx-like toxins to attack host phagocytes (182), we postulate that
the sequences may be important in attacking the insect cellular immune system, the hemocytes. This hypothesis could be tested by deleting the
toxin loci or their export machinery and examining the infection process in their presence and absence.
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TABLE 4.
Rtx-like operon homologs, including proteins exported by
these operons and their accompanying export machinery and activating
and modulating proteinsa
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FIG. 3.
Inferred genomic organization of different putative
Rtx-like operons (rtx, shl, eth,
hec, hly, and cva) from the sample
sequence. The relative predicted positions of sequencing hits are shown
below each predicted locus, and the range of percent identity values is
shown. The putative operons are shaded in order to indicate their
potential functions as either an exported protein, a activity
regulator, an ATP-binding protein, or a membrane fusion protein.
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In addition to an RtxA-like export system, we also found evidence of
other Rtx-like export systems, including an Rtx-like
metalloprotease
and its accompanying export machinery. The Rtx-like
metalloprotease
itself is similar to PrtA-encoded metalloproteinase
A of
E. chrysanthemi, while its associated export machinery is
similar to
the LipBCD-like ABC transporter of
S. marcescens, which
also
exports a protease. Between the protease and its associated
ABC
transporter there is a small protease inhibitor (as confirmed
by our
extended sequencing of the operon). This genomic organization
of an
Rtx-like metalloprotease and its associated LipBCD-like
transporter
shows that
P. luminescens uses different combinations
of
Rtx-like genes to export virulence factors and stresses the
potential
importance of these systems for anti-insect
virulence.
Other putative virulence factors.
In addition to the specific
Tc-like and Rtx-like toxins discussed above, we also identified a wide
range of other sequences related to a diverse array of genes that are
potentially involved in infection and virulence. These genes include
genes that encode factors involved in bioluminescence, other proteases,
lipases, hemmaglutinins, chitinases, and other toxins, such as non-Rtx hemolysins and ADP-ribosyltransferases (Table
5). They also include genes involved in
two-component sensor systems that have previously been implicated in
regulation of virulence both in Photorhabdus strains and in
other bacteria.
Bioluminescence (from which
P. luminescens obtained its
specific epithet) occurs shortly after bacteria invade an insect,
but
its biological role is unclear. The genes that encode the
luciferase
beta subunit and NAD(P)H-flavin reductase, which reduces
flavin
mononucleotide for bioluminescence, have previously been
cloned, and
hits to these genes were highly significant (BLASTX
E
values, 1e-39 to 3e-66), which again confirmed the quality and
coverage
of the sample sequence. Compared to other classes of
potential
virulence factors, we found several sequences similar
to sequences of
non-RTX-like proteases and lipases, which have
previously been
implicated in virulence. One of these, triaglycerol
lipase 1, has been
cloned previously, and hits to this sequence
were highly significant
(BLASTX
E values, 4e-13 to 9e-86). Other
proteins, like the
Lys-X cysteine protease of
Porphyromonas gingivalis,
have
been implicated in virulence during soft-tissue infections
(
109). Another subclass of hits in this category are hits to
matrix metalloprotease-like sequences. These are interesting because
one of the proteins, limunectin (from the horseshoe crab,
Limulus sp.), binds bacterial cells, fixed amebocytes, and
extracellular
matrix molecules (
113). If
Photorhabdus cells do indeed make
a similar protein, the
protein may play some role in bacterial
aggregation, previously termed
nodulation (
52), or in attachment
to host cells. Other hits
to proteins potentially involved in
host cell binding included hits to
several hemagglutinins. For
example, deletion of the filamentous
hemagglutinin locus in
Bordetella pertussis results in loss
of binding to ciliated eukaryotic host
cells (
148). As well
as degrading host cells via proteolytic
activity, much of the insect
exoskeleton is composed of chitin.
Therefore, hits to chitinases
(
N-acetyl-beta-glucosaminidase)
probably indicate that there
are several chitin-degrading enzymes,
notably an enzyme similar to the
chB-encoded chitinase of
S. marcescens and a
chitinase C-like product of an insect (
Glossina morsitans)
S
endosymbiont (Table
5).
In addition to the Tc and Rtx-like toxins discussed above, W14 also
appears to contain several non-Rtx hemolysins and other
classes of
toxins. One of the non-Rtx hemolysins, hemocyte erythrocyte
lysis
protein 2 from
Prevotella intermedia, is notable in that
searches of DNA and protein databases have not previously revealed
any
significant homologies (
14); the
Photorhabdus
homology reported
here is, therefore, possibly such a match. Other
classes of toxins
include two ADP-ribosyltransferases and cytotoxic
necrotizing
factor 2, all of which are cytotoxins. The
ADP-ribosyltransferases
are like exotoxin A from
Clostridium difficile and
Pseudomonas aeruginosa.
Although the BLASTX
E values for these hits are of
low
significance (0.05 and 0.8), the narrow ranges of homology
values
indicate that the levels of predicted amino acid identity
are high
(44% [17 of 38 residues] and 32% [24 of 73 residues],
respectively). Cytotoxic necrotizing factor 2 from
E. coli
acts
on the small GTP-binding protein Rho involved in actin
cytoskeleton
assembly and causes stress fiber formation in target cells
(
137).
It is also interesting that there was a hit to
halovibrin from
Vibrio fisheri, which is a member of a novel
class of ADP ribosyltransferases
with no significant sequence homology
to other ADP ribosyltransferases
(
147). In relation to
potential ADP ribosyltransferase regulation,
the sample sequence had a
highly significant (BLASTX
E value,
6e-50) hit to ExsA, the
exoenzyme S synthesis regulatory protein
(
53). Exoenzyme S
is another ADP ribosyltransferase that is
distinct from exotoxin A and
is secreted by
P. aeruginosa, and
ExsA is an AraC-like
transcriptional regulator of its production.
This sequence is also
similar (BLASTX
E value, 2e-44) to the VirF
virulence
regulon transcriptional regulator which controls the
yop
regulon (see below). Finally, with regard to other non-Tc
toxins, there
were two low-scoring hits to the delta-endotoxins
from
Bacillus
thuringiensis, whose significance is
uncertain.
Hits on other potential virulence factors included matches to Vac, Vap,
and Kic-like proteins. There were hits on VacB from
both
E. coli and
Haemophilus influenzae. Disruption of this
gene
in enteroinvasive
E. coli results in reduced expression
of virulence
phenotypes, suggesting that it is necessary for full
expression
of virulence (
172). We also found sequences
similar to both VapD
and VapZ from
Dichelobacter nodosus.
These are virulence-associated
proteins homologous to ORFs found on the
F plasmid of
E. coli (
86). Furthermore, we found
a KicA-like sequence; this protein
is thought to suppress the killing
function of the
kicB gene product
(
49). The
putative KicA-like protein in
P. luminescens may,
therefore,
function as a toxin-antitoxin system for killing non-self
bacteria,
like the colicins and pycocins discussed
above.
The sample sequence revealed five sequences that exhibit similarity to
known two-component sensors: EnvZ, CheA, ExpA, BaeS,
and TctE. Of
these, only EnvZ and CheA have been characterized
in detail. The
ompR-envZ regulatory system has been shown to contribute
to
virulence in a number of enteric bacterial pathogens. For example,
an
isogenic
ompR mutant of
Yersinia enterocolitica
exhibited increased
sensitivity to high osmolarity, high temperature,
and low pH and
also offered partial protection against wild-type
challenge in
a murine yersiniosis model (
43). The
ompR and
envZ signal transduction
genes have also
been cloned from another entomopathogenic nematode-associated
bacterium,
Xenorhabdus nematophilus (
168).
Deletion of
envZ in
a
Xenorhabdus strain suggests
that the gene regulates some outer
membrane proteins during the
stationary growth phase, implying
that it has a potential role in
virulence (see below). The CheA
protein is required to initiate the
response of the flagellar
motor to the binding of stimulatory ligands
to chemoreceptors
during bacterial chemotaxis. The hit to ExpA is of
great interest
as this protein and its relatives appear to play a key
role in
regulating expression of a range of secreted virulence factors
in different gram-negative bacteria. The relatives include SirA
in
Salmonella typhimurium, ExpA in
Erwinia spp., and
GacA in
Pseudomonas spp. For example, in
S. typhimurium SirA is needed for expression
of the type III
secretion apparatus. Furthermore, upon sensing
of a mammalian
microenvironment, SirA phosphorylation initiates
a cascade of
transcription factor synthesis that leads not only
to invasion gene
transcription but also to Ssp secretion and bacterial
epithelial
invasion (
78). Deletion of such a locus from a
Photorhabdus strain would, therefore, allow us to test the
hypothesis that
a similar system is effective for sensing the insect
hemocoel
and subsequently initiating virulence-associated
transcription.
Locomotion, attachment, and invasion.
During its complex life
cycle, a Photorhabdus strain not only needs to detect which
environment it is in (e.g., nematode gut versus insect hemocoel) but
presumably also needs to recognize specific surfaces for attachment and
potentially invasion. Although we have little understanding of when and
where Photorhabdus strains go during the insect infection
process, we do know that their titers in the hemolymph change rapidly
(52) and that during the infection process the insect midgut
is specifically destroyed (18). Thus, we do not know if the
bacteria replicate in the insect hemocytes or if they invade the gut
directly. However, even in the absence of substantial information
concerning the basic biology of these organisms, we can make inferences
about the likely infection process based on the array of genes that they carry which are putatively involved in locomotion and
tissue-specific attachment and/or invasion. Most notable in the latter
case are two hits to the attachment invasion locus
(ail) found in Yersinia spp. (Table
6). In Y. enterocolitica this
locus is responsible for the ability of the pathogen to cross the
epithelium of the gut on its way to replicate in the
reticuloendothelial system. Again, although we have no direct evidence
that a putative homolog plays a similar role in Photorhabdus
strains, we can test whether P. luminescens W14 can invade
the gut (presumably from the hemocoel, not the lumen) and, if it can,
whether deletion of the ail-like locus interferes with this
ability. With respect to attachment, we also found a sequence similar
to intimins, which are proteins homologous to the invasins of
Yersinia spp. and which play a role in attachment and
effacing of the brush border membrane (54).
Another class of proteins involved in recognition of specific tissues
is the class that includes the fimbriae and the associated
adhesins. It
has been hypothesized that in
X. nematophilus fimbriae
are
involved in establishment of the specific association between
the
bacterium and the nematode gut (
52). In the
Photorhabdus sample sequence, we detected numerous
matches with sequences encoding
fimbrial type 1 subunits,
fimbrial chaperones, and the outer membrane
ushers associated with
fimbrial export and assembly (Table
6).
Although it is difficult to
predict from these sequence matches
the likely fimbrial composition of
P. luminescens W14, we found
both
mrpC-like and
mrpD-like loci, which encode the outer membrane
usher and
fimbrial chaperone from the Mrp (mannose-resistant,
Proteus-like) fimbriae of
Proteus mirabilis,
respectively, and
also FimD-like ushers and FimC-like chaperones from
E. coli. The
FimD sequence also exhibits similarity to S
fimbrial adhesins,
filamentous hemaglutinin A, and bovine colonization
factor, implying
that it may also play a role in virulence-associated
adhesion.
A second indication that there is another group of genes
involved
in a diverse array of functions that include fimbrial
biogenesis,
protein secretion, and DNA uptake (
68) is the
presence of sequences
similar to those encoding a prepilin type of
leader peptidase.
Again, the significance of the presence of these
sequences in
Photorhabdus sp. is not clear, but this topic
warrants further
investigation.
Flagella are important in bacterial locomotion, and phase I
Xenorhabdus cells exhibit swarming motility when they are
grown
on suitable solid media (
52). Correspondingly,
extracts from
phase I variants appear to contain flagellar filaments
(flagellin),
whereas phase II cells do not (
52). Although
the molecular mechanism
of this defect in flagellin synthesis is
unclear, we found several
ORFs in both
fli-like and
flh-like operons in
P. luminescens W14
(Table
6).
These ORFs include the FliD-like hook-associated protein
2 previously
cloned from
X. nematophilus (
59), which is
differentially
transcribed in the two phase variants. Previous
experiments have
shown that insertion of a transposon into the
flgN gene of
P. mirabilis resulted in a mutant
which was still motile but had
lost the ability to swarm
(
64). This suggests that specific
flagella are independently
responsible for the swarming and motility
phenotypes. Identification of
the genes encoding these two classes
of flagella in
P. luminescens may, therefore, enable us to elucidate
not only what
types of flagella are produced by the bacterium
but in which phase
variants they are expressed and what function
they
perform.
Finally, we found three different sequences that potentially encode
outer membrane proteins (Omp). The outer membrane protein
composition
of
X. nematophilus changes as the organism enters
the
stationary phase of growth, and the outer membrane proteins,
which are
thought to form pores, may be responsible for functions
that are
necessary for survival under stress conditions (
52).
For
example, expression of cloned
ompF of
S. marcescens is increased
in
E. coli under
high-osmolarity conditions (
73). It has also
been
hypothesized that the
X. nematophilus outer membrane
proteins
play a role in specific interactions with the nematode host
(
52).
Production of these proteins is regulated by EnvZ, as
discussed
above.
Secretion and transport.
One of the most striking features of
P. luminescens grown in a liquid culture is the large number
of proteins that are secreted into the supernatant. Some of these
proteins have been well characterized, including the Tc toxins,
proteases, and lipases discussed above. However, most of the secreted
proteins are poorly characterized, and, perhaps equally importantly,
their mechanisms of export are not known. Thus, for example, the
mechanism and timing of secretion of the Tc toxins in the insect host
remain obscure. Below we discuss sequences similar to different types
of secretion machinery, notably type III-like secretion systems and ABC
transporters. We observed a series of hits to the Yop type III
secretion system of Yersinia species, including sequences
similar to both Yop proteins, Ysc secretion proteins, and Syc
Yop-specific chaperones (Table 7). The
yop virulon enables Yersinia cells to survive and
multiply in the lymphoid tissues of their hosts (36). The
Yop proteins are encoded on the pYV plasmid at the low-calcium-response
locus, and virulent Yersinia cells secrete these virulence
determinants when they are incubated at 37°C in the absence of
Ca2+ ions. The Yop proteins themselves are involved in
contact-dependent delivery of toxins and effector molecules. Thus, in
P. luminescens they could potentially be responsible for
delivering toxins to either the gut or the insect hemocytes. As
discussed above, the virF virulence regulon transcriptional
regulator (BLASTX E value, 2e-44) (Table 5) regulates
production of Yop proteins. This gene is, therefore, a very interesting
candidate for knockout in P. luminescens, as its loss may
alter the pathogenesis of Photorhabdus cells with different
insect tissues and potentially ascribe a function to the presence of
the Yop-like sequences in strain W14.
In addition to contact-dependent secretion, the ABC transporters
represent a large family of transporter systems with a diverse
array of
functions, including transport of peptides, amino acids,
sugars, and
metal ions. We, therefore, catalogued some of the
sequences similar to
ABC-like transporters (Table
7), and below
we discuss some of their
potential functions in
P. luminescens.
There were several
sequences similar to peptide and amino acid
transporters. Two potential
homologs, OppA and ProU, are of special
interest. OppA is located in
the periplasm and is required for
uptake of peptide antibiotics in
E. coli and
S. typhimurium (
66).
ProU,
the product of the
proU locus (also found in both
E. coli and
S. typhimurium), is a high-affinity glycine
betaine transport
system which plays an important role in survival
under osmotic
stress conditions (
163). There were also
several sequences similar
to various sugar transporters and their
transcriptional regulators.
Central among these was the bacterial
phosphoenolpyruvate-dependent
phosphotransferase system (PTS), which
catalyzes cellular uptake
and subsequent phosphorylation of
carbohydrates and also plays
a crucial role in the global regulation of
various metabolic pathways
(
177). The presence of PTS-like
sequences in
Photorhabdus cells
is potentially important
because chitin-degrading bacteria, such
as
Vibrio furnissii,
rely on PTSs in the chitin catabolic cascade
(
21), and
P. luminescens may therefore utilize a similar system
for
degrading insect
chitin.
Polysaccharide biosynthesis.
Another striking feature of the
P. luminescens culture supernatant is the large amount of
LPS present. LPS production has been directly implicated in virulence
in P. luminescens, as it has been in a wide range of other
bacteria. For example, in B. pertussis the LPS is
biologically active and is both toxic and immunogenic (5).
LPS can also act as a recognition or binding site for extracellular
agents. Thus, core LPS can act as a binding site for bacteriocins
(alongside the outer membrane proteins OmpA and OmpF, as discussed
above), while the trsG operon (Table
8) is required for biosynthesis of the
bacteriophage Phi R1-37 receptor structures (158). The lipid
A-core component of LPS is synthesized by sequential addition of sugars
and fatty acids, and several sequences similar those involved in LPS
biosynthesis were found in the sample sequence. These include
envA (lpxC), which encodes an enzyme necessary
for synthesis of the lipid A moiety (94), and
rfaC, which is required for LPS inner-core synthesis
(31). We also found genes likely to encode polysaccharide
export functions, such as rcsF, which confers a mucoid
phenotype (57), and wza, which encodes an outer
membrane lipoprotein probably responsible for colanic acid
(extracellular polysaccharide) export (161). Finally, genes
encoding pullulanaselike proteins (starch-debranching enzymes) are also
present; these proteins may play a role in recycling of the cell wall.
Iron acquisition and transport.
As iron is often a
rate-limiting growth factor in the host, many pathogenic bacteria have
high-affinity iron-binding systems which can capture iron from host
iron chelators. Thus, P. luminescens W14 has sequences which
predict proteins similar to those involved in biosynthesis, transport,
and reception of the siderophore yersiniabactin. Yersiniabactin (Ybt)
has a high affinity for ferric iron, and similar siderophore-dependent
iron transport systems are found in Yersinia pestis,
Yersinia pseudotuberculosis, and Y. enterocolitica (140). A similar system may, therefore,
also be used by P. luminescens. The irp1 and
irp2 genes are required for yersiniabactin synthesis, as is
ybtE, which encodes yersiniabactin dihydroxybenzoate ligase (Table 9). Transport of the
iron-yersiniabactin complex back into the cell requires the
TonB-dependent surface receptor FyuA, which may also be present in
P. luminescens W14. This receptor is highly conserved and is
found in all pesticin-sensitive bacteria, including E. coli
(146). The sample sequence also contained hits to an R4-like
ferric siderophore receptor from E. coli, which may perform
a similar function in P. luminescens, and a putative operon
(pvcABCD) involved in synthesis of the chromophore moiety of
the P. aeruginosa siderophore pyoverdine (162).
View this table:
[in this window]
[in a new window]
|
TABLE 9.
Iron assimilation: ferric siderophore biosynthesis and
transport and regulation of iron and other metals
|
|
P. luminescens, like
Yersinia spp., also appears
to contain alternative iron and hemin transport systems, as indicated
by
hits to genes similar to
yfeE, the
yfeABCD
ferric iron uptake
operon regulator, and members of the
hmu
hemin utilization system.
The latter system is essential in
Y. pestis for utilization of
free hemin and heme-protein complexes,
which are the bacterium's
sole sources of iron (
71).
P. luminescens also contains sequences
similar to members of
both the
feo iron(II) (
80) and
fec
iron(III)
(
159) transport systems. Finally, like numerous
other gram-negative
bacteria,
P. luminescens also has a
sequence similar to the
fur gene sequence. This gene is
involved in iron regulation, and in
the presence of excess iron, the
fur gene product generally represses
expression of
iron-regulated genes (
140). Together, these sequences
suggest that scavenging and transporting iron are important in
P. luminescens, as they are in many pathogenic
bacteria.
Extrachromosomal elements.
Like the genomes of other bacteria,
the P. luminescens sample sequence contains many sequences
similar to sequences found in a wide range of phage and insertion
sequence elements. These sequences are important because they may begin
to explain how P. luminescens, an insect pathogen, acquired
virulence factors previously associated only with vertebrate
pathogenicity, such as sequences similar to the low-calcium-response
stimulon from Yersinia discussed above. Numerous hits to
tail proteins from P2-like bacteriophages (46) (P2, P4, 186, and HP1) and a range of other phage-related proteins were observed
(n = 51). There were also 10 hits (BLASTX P
values, 0.01 to 2e-86) to products of the integrase
(int) gene, which controls phage site-specific integration.
Notably, in the range of phage homologies there were hits (although
with relatively low significance [BLASTX E values, 0.3 to
5e-15]) to three different ORFs (ORFs 16, 20, and 25) of the P. aeruginosa cytotoxin converting phage Phi CTX (cholera toxin). We
note that the rtx gene cluster is physically linked to the
CTX toxin element in the V. cholerae genome
(112). Therefore, it will be interesting to investigate
whether this element is linked with the rtxA-like sequences
found in P. luminescens W14, suggesting that it could have
been responsible for horizontal transfer of the toxin-encoding genes.
Numerous transposon-like sequences were also found (n = 33), including 10 hits to a transposase from plasmid ColIb-P9
(BLASTX E values, 1e-04 to 4e-86). Again, although these
sequences indicate that transfer events occurred, it is not known how
long these transposons have been present and if any of them have
retained functionality. Finally, the P. luminescens W14
genome contains numerous sequences related to sequences involved in
plasmid maintenance and stability (Table
10). However, we cannot at this stage
distinguish which of these sequences are plasmid encoded (plasmids have
been found previously in Xenorhabdus spp. [103]) and which are chromosomal. The presence of
these sequences, therefore, raises the possibility of plasmid
maintenance in P. luminescens W14 but is not strictly
indicative.
Conclusions.
P. luminescens has a life cycle which
introduces it into a diverse array of environments, and in only one of
these environments, the insect environment, is the bacterium
pathogenic. The sample sequence of strain W14 revealed sequences
similar to the sequences of a diverse array of potential virulence
factor-encoding genes, including the genes for several classes of
toxins, proteases, lipases, and LPS. It also gave us some indication of
the diversity of the transport and metabolic systems present.
Furthermore, Photorhabdus spp. also seem to share potential
virulence factors (Yops, a yersiniabactin-like siderophore, and the
low-calcium-response stimulon) with distantly related vertebrate
pathogens, such as members of the genus Yersinia. This
hypothesis is supported by the presence of numerous phagelike and
transposon-like sequences in the P. luminescens genome. The potential for horizontal transfer raises the intriguing possibility that the virulence factors present in invertebrate pathogens may also
be present in vertebrate pathogens. Given the far greater diversity of
invertebrates and, potentially, their associated pathogens, this raises
interesting questions about the diversity and origins of potential
vertebrate virulence factors. In relation to P. luminescens
itself, complete elucidation of the genome sequence of strain W14 and
other strains should allow us to begin to understand the roles of
individual genes via targeted disruption and to begin to compare the
diversity of virulence factors found in different invertebrate
pathogens. Our findings are consistent with the hypothesis of Burland
et al. (30), who hypothesized that all of the pathogenic genes shared by enteric bacteria form a pool or "pathosphere"; however, here we emphasize that the pool must be extended to include both invertebrate and vertebrate pathogens. Furthermore, as
invertebrates evolved before vertebrates, this also raises the
interesting possibility that pathogens such as P. luminescens include the progenitors of virulence factors in
vertebrate pathogens.
| |
ACKNOWLEDGMENTS |
This work was supported by grants to R.F.C from the BBSRC, the
Wellcome Trust (JIF), and DowAgroSciences, which we thank for their
interest and support.
We thank all of the technical staff of the Wisconsin Genome Project for
their help with sequencing and assembly. We thank David Clarke for
comments on the manuscript.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Biology and Biochemistry, South Building, University of Bath, Bath, BA2 7AY, United Kingdom. Phone: 44 1225 826261. Fax: 44 1225 826779. E-mail: bssrfc{at}bath.ac.uk.
| |
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Applied and Environmental Microbiology, August 2000, p. 3310-3329, Vol. 66, No. 8
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Copyright © 2000, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
