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Journal of Bacteriology, May 1999, p. 3310-3316, Vol. 181, No. 10
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
NahY, a Catabolic Plasmid-Encoded Receptor Required
for Chemotaxis of Pseudomonas putida to the Aromatic
Hydrocarbon Naphthalene
Ann C.
Grimm
and
Caroline S.
Harwood*
Department of Microbiology, The University of
Iowa, Iowa City, Iowa 52242
Received 13 January 1999/Accepted 8 March 1999
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ABSTRACT |
Pseudomonas putida G7 exhibits chemotaxis to
naphthalene, but the molecular basis for this was not known. A new
gene, nahY, was found to be cotranscribed with
meta cleavage pathway genes on the NAH7 catabolic plasmid
for naphthalene degradation. The nahY gene encodes a
538-amino-acid protein with a membrane topology and a C-terminal region
that resemble those of chemotaxis transducer proteins. A P. putida G7 nahY mutant grew on naphthalene but was not
chemotactic to this aromatic hydrocarbon. The protein NahY thus appears
to function as a chemoreceptor for naphthalene or a related compound.
The presence of nahY on a catabolic plasmid implies that
chemotaxis may facilitate biodegradation.
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TEXT |
The ability of bacteria to recognize
and swim toward aromatic hydrocarbons is possibly an important
prelude to their degradation, but this has not been proven. Recently we
reported that naphthalene, a polyaromatic hydrocarbon and a U.S.
Environmental Protection Agency priority pollutant (8), is a
chemoattractant for Pseudomonas putida G7 (5).
Naphthalene is produced in large quantities by the petrochemical
industry as a bulk chemical for use in organic syntheses and has been a
model compound for studies of biodegradation because it is relatively
easily metabolized by soil bacteria (11, 21). The genes
required for its complete degradation are typically located on large
self-transmissible catabolic plasmids and, in the case of the catabolic
plasmid NAH7, have been shown to reside within the boundaries of a
defective transposon (17, 20). A mutant derivative of
P. putida G7 (G7.C1) that was cured of NAH7 was not
chemotactic to naphthalene. Moreover, a 25-kb subclone of the 83-kb
NAH7 plasmid conferred on P. putida G7.C1 the ability to
grow on naphthalene but did not restore naphthalene chemotaxis to the
strain (5). This suggested that an additional gene or genes
required for naphthalene chemotaxis might be present on NAH7. Here, we
describe work on the molecular basis for chemotaxis to naphthalene and
report the identification of a chemotaxis protein transducer gene on
the catabolic plasmid NAH7.
Bacterial strains and experimental procedures.
P. putida
G7 and its plasmid NAH7-cured derivative, P. putida G7.C1,
were obtained from D. T. Gibson at the University of Iowa.
P. putida G7.C1(pHG100) has been previously described
(5). Cells were grown in Luria broth (1a) or
minimal mineral salt medium (7) supplemented with a carbon
source. Succinate was used as a growth substrate at a final
concentration of 10 mM. Naphthalene was provided as a carbon source by
the direct addition of naphthalene crystals to liquid minimal medium,
due to the limited solubility of this compound. Liquid cultures were
grown at 30°C with shaking at 250 rpm.
The bacterial strains and plasmids used are described in Table
1. Antibiotics were added when necessary
at the following concentrations: kanamycin, 100 µg/ml; gentamicin, 10 µg/ml; and tetracycline, 50 µg/ml for P. putida and 25 µg/ml for Escherichia coli. Plasmids were introduced into
P. putida from E. coli S17-1 by conjugation.
Mating mixtures were spread on minimal medium containing succinate and
either kanamycin, gentamicin, or both. In the case of plasmid pHG97,
which was used to create the nahY mutant P. putida G7 Y1, exconjugants were screened for sensitivity to
gentamicin to ensure that the suicide delivery vector, pSUP102-Gm, had
been lost. A gentamicin-susceptible (Gms)
kanamycin-resistant (Kmr) colony was then passaged on a
minimal medium plate containing succinate and kanamycin for about a
week to allow for complete loss of any wild-type NAH7 plasmid that
might still be present in the strain.
Southern analysis was carried out with the Genius hybridization kit
according to the manufacturer's instructions (Roche Molecular
Biochemicals, Inc., Indianapolis, Ind.). Plasmids were isolated
from
E. coli and
P. putida with the Qiagen (Santa
Clarita, Calif.)
miniprep spin or midiprep system. Nucleotide
sequencing was performed
by the University of Iowa DNA Core Facility.
Sequence data were
analyzed with software from Textco, Inc. (West
Lebanon, N.H.),
Genetics Computer Group (Madison, Wis.), and the
National Center
for Biotechnology Information (Bethesda, Md.).
Reverse transcriptase PCR (RT-PCR) was used to determine if
nahX and
nahY were cotranscribed with
nahJ, a structural gene
of the lower naphthalene degradation
pathway. RNA was isolated
from naphthalene-grown cells by using the SV
Total RNA isolation
system from Promega (Madison, Wis.). Cells were
sonicated after
being resuspended in lysis buffer to improve RNA yield.
RT-PCR
was performed with the Access RT-PCR system from Promega
according
to the manufacturer's instructions. The primers used for
RT-PCR
were SH-R2 (5'-GCGCCGACTAGCATTAAAAG-3') and Sal3R-2
(5'-CGCCCAGTTGTACATCCTC-3')
for the region from
nahJ to
nahX. Primers NahXN
(5'-CCATGATCATCTCGACCCTCGAAAC-3')
and NahYN2
(5'-CGTCATAGGCACGCTTTGATTCC-3') were used for the region
from
nahX to
nahY.
Chemotaxis to naphthalene was tested by a modified capillary assay
(
5) and also by the agarose-in-plug assay described
by Yu
and Alam (
23). Chemotaxis to salicylate was tested only
with
the agarose-in-plug assay. Cells used in these assays were
grown on
naphthalene as a sole source of carbon and energy to
mid-logarithmic
phase, harvested, and resuspended in chemotaxis
buffer (100 mM
potassium phosphate [pH 7.0], 20 µM EDTA). Cells
were motile in
chemotaxis buffer for at least 1 h in the absence
of an exogenous
energy source. With the capillary method, the
open end of a
buffer-filled 1-µl capillary tube was packed with
finely ground
crystals of naphthalene and introduced into a chamber
containing a
suspension of motile cells. Chemotaxis was determined
microscopically
and defined as the accumulation of a cloud of
cells around the tip of
the capillary tube over a period of 10
to 20 min. With the
agarose-in-plug method, a blob of melted agarose
containing an
attractant, either crystals of naphthalene or 50
mM salicylate, was
placed between a microscope slide and a glass
coverslip that was laid
across two strips of plastic to form a
bridge. After the agarose
solidified to form a plug, a suspension
of cells was introduced into
the space between the slide and coverslip
so that it flooded around the
plug. Cells that responded to the
naphthalene or salicylate formed a
dense band, visible to the
naked eye, about 0.5 mm from the plug within
a period of 5 min.
Cells did not respond to a plug of agarose prepared
with chemotaxis
buffer alone. Soft agar swarm plates were used to
assess chemotaxis
to succinate, 4-hydroxybenzoate, and benzoate, as
described previously
(
2).
The NAH7 plasmid contains a gene or genes necessary for
chemotaxis to naphthalene.
To determine whether plasmid NAH7
included genes that were required for chemotaxis to naphthalene, we
started with a strain [P. putida G7.C1(pHG100)] that
we had previously constructed which was cured of the NAH7 plasmid
but could grow on naphthalene because it carried all of the upper and
most of the lower naphthalene pathway genes on pHG100, a subclone of
NAH7 (5) (Fig. 1). We presume
that ortho cleavage genes located on the chromosome allowed the strain to circumvent the need for all of the lower pathway genes.
This strain did not exhibit chemotaxis to naphthalene. We then
introduced additional subclones of NAH7 into strain G7.C1(pHG100) on a
compatible plasmid and tested for naphthalene chemotaxis. Naphthalene
chemotaxis was restored by a subclone (pHG59) that contained
a 5.9-kb EcoRI fragment that mapped immediately
adjacent to the 25-kb EcoRI fragment used to make pHG100
(Fig. 2). Introduction of the vector
pBBR1-MCS2, used to construct pHG59, into strain G7.C1(pHG100) did not
restore chemotaxis to naphthalene. Strain G7.C1 carrying only pHG59
sometimes exhibited a weak chemotactic response to naphthalene.
However, a consistently strong response was seen only when pHG100 was
present together with pHG59 in strain G7.C1.
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FIG. 1.
The naphthalene catabolic plasmid and degradation
pathway in P. putida G7. (A) NAH7. The region of NAH7
involved in naphthalene degradation is indicated by
arrows. Two subclones made from NAH7, pHG100 and pHG59, are shown. Only
EcoRI sites in or around the naphthalene degradation genes
are shown (E, EcoRI). (B) Naphthalene catabolic
pathway. The meta pathway, which converts catechol to
acetyl-coenzyme A (acetyl-CoA) and pyruvate, is encoded on the
NAH7 plasmid.
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FIG. 2.
Chemotactic responses of Pseudomonas strains
to naphthalene in modified capillary assays. Naphthalene chemotaxis was
restored when pHG59 was introduced into P. putida
G7.C1(pHG100). Cells were grown on naphthalene. The results are shown
in both photographic (top) and schematic (bottom) form. Naphthalene
crystals are visible inside the mouths of the capillary tubes. The
accumulation of a cloud of cells around the mouth of a capillary tube
over time indicates a chemotactic response.
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Genes present on the chemotaxis-complementing clone.
Nucleotide sequencing of pHG59 revealed several genes on the 5.9-kb
EcoRI insert that had not previously been described (Fig. 3). As expected, several lower
naphthalene pathway genes required for the degradation of the
intermediate salicylate via a meta cleavage pathway were
found, their locations having previously been roughly mapped to the
region of the 5.9-kb EcoRI fragment (21). The
order of the genes nahOMKJ was slightly different from that
previously reported based on an analysis of Tn5 mutations in
this region (21). The sequences of the nahO and
nahM genes, encoding acetaldehyde dehydrogenase and
4-hydroxy-2-oxovalerate aldolase, respectively, from the naphthalene
catabolic plasmid pWW60-22 had already been reported (10).
The deduced amino acid sequences of the nahK and
nahJ genes show a high level of identity (about 90%) to
those of homologous meta pathway genes involved in phenol
and toluene degradation (6, 12). nahJ encodes
4-oxalocrotonate tautomerase, and nahK encodes
4-oxalocrotonate decarboxylase.
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FIG. 3.
Plasmid pHG59. (A) Restriction and gene map of pHG59.
Sufficient sequencing was done to determine the locations of the starts
and stops of all the genes illustrated. B, BsiWI; E,
EcoRI; N, NsiI; P, PstI; Sa,
SalI; Sm, SmaI. Not all SalI or
NsiI sites are shown. (B) Subclones of pHG59. Plasmid pHG97
(see Table 1 for construction details) was derived from a 4-kb
SmaI-EcoRI fragment of pHG59. A kanamycin
resistance cassette was introduced into the NsiI sites of
this 4-kb fragment. The second clone, pHG125, contains nahY
and was used for complementation analysis. (C) Transcript analysis of
nahJ, nahX, and nahY. The intergenic
regions between nahJ and nahX and between
nahX and nahY that were amplified by RT-PCR are
shown.
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Downstream of
nahOMKJ were two new genes that we have termed
nahX and
nahY. nahX is predicted to encode a
140-amino-acid protein
that resembles (38% amino acid identity) a
Sphingomonas sp. protein
(CmpX) of undefined function. It
may be noteworthy that CmpX is
encoded by an open reading frame that is
also located among plasmid-borne
meta cleavage genes
(
22).
nahY shows 28% deduced amino acid identity with PctB, a
membrane-bound transducer protein from
Pseudomonas
aeruginosa that
functions in chemotaxis to amino acids
(
16). The 538-amino-acid
predicted NahY protein has several
features that are conserved
among chemotaxis transducer proteins, also
known as methyl-accepting
chemotaxis proteins (MCPs). These include two
predicted membrane-spanning
regions, one near amino acid 10 and the
other near amino acid
200.We assume, based on homology with other MCPs,
that the intervening
sequence is located in the cellular periplasm.
Residues 375 to
425 of NahY are about 70% identical to the
chemotaxis-signaling
domain of transducer proteins from
E. coli and
Salmonella typhimurium (
15). This
region, predicted to be in the cytoplasm, is highly
conserved among
chemotaxis transducer proteins from diverse bacteria.
The C-terminal
cytoplasmic regions of MCPs have two domains on
either side of the
signaling domain that contain glutamate or
glutamine residues which are
either methylated, demethylated (glutamate),
or deamidated (glutamine)
as part of the adaptation phase of chemotaxis
(
15). In the
region corresponding to the methylation region
designated K1 in the
enteric transducers, NahY has two glutamine
residues, one at position
291 and the other at position 296, that
align to within one amino acid
residue of the first two methylation
sites of the
E. coli
transducers Tsr, Tar, and Trg. NahY has a
glutamate at position 304 that aligns exactly with a glutamine
that has been shown to serve as a
site of methylation in each
of the
E. coli MCPs. There
appears to be only one potential methylation
site in the portion of
NahY that corresponds to the R1 methylation
region. This is a glutamate
at position 506 that aligns with glutamates
that are methylated in the
E. coli MCPs. The last five amino acids
(NWETF) of the major
E. coli and
S. typhimurium chemotaxis transducers
serve as a methyltransferase binding sequence (
18). NahY
lacks
this
sequence.
Immediately downstream of
nahY was a region of DNA that was
almost identical to the left inverted repeat of Tn
4655, a
transposon
previously reported to be part of the NAH7 plasmid
(
17).
RT-PCR showed that
nahJ,
nahX, and
nahY were cotranscribed in naphthalene-grown cells. This
suggests that
nahX and
nahY may
be part of the
lower naphthalene pathway operon of
NAH7.
Construction of a nahY mutant.
The deduced
structural characteristics of NahY suggested that it might serve as a
catabolic plasmid-encoded chemoreceptor for naphthalene. To test this,
we constructed a mutant strain (G7 Y1) in which the 3' end of
nahY, including the domain that is highly conserved in
transducer proteins, was replaced with a kanamycin resistance cassette
(Table 1). Southern hybridization analysis was used to confirm the
strain construction and to show that P. putida G7 Y1
contained no detectable wild-type copies of nahY. The
nahY mutant strain grew on naphthalene at the same rate as
its wild-type parent, but naphthalene-grown cells of the mutant were
not attracted to naphthalene (Fig. 4).
The chemotaxis defect appears to be specific to the attractant
naphthalene, as the nahY mutant had a wild-type chemotactic
response to succinate, benzoate, salicylate, and 4-hydroxybenzoate
(data not shown). The unstimulated-swimming patterns of the
nahY mutant were the same as those of wild-type cells, as
judged by microscopic observation. Neither the wild type nor the mutant
increased its swimming speed in response to the addition of any of the
attractants tested. Wild-type nahY, supplied on a
broad-host-range plasmid, complemented the naphthalene chemotaxis
phenotype of P. putida G7 Y1 in trans (Fig. 4).
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FIG. 4.
NahY is necessary for naphthalene chemotaxis, as
determined by capillary assay. The mutant P. putida G7 Y1 is
not chemotactic to naphthalene, but the mutation is complemented by the
introduction of pHG125, a clone containing nahY. The
wild-type strain also exhibited a positive response to naphthalene by
the agarose-in-plug method, whereas the nahY mutant strain
G7 Y1 did not (data not shown). Cells were grown on naphthalene.
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NahY is a catabolic plasmid-encoded chemoreceptor.
The
phenotype of the nahY mutant and the deduced amino acid
sequence of NahY suggest that this protein is likely to function by
binding naphthalene or a related compound on its periplasmic face to
initiate chemosensory signaling in a manner analogous to that of other
bacterial transducer proteins. Members of this family of proteins have
been best studied in E. coli and S. typhimurium, where they bind amino acids or sugars and initiate sensory signal transduction by altering the activity of CheA, an associated histidine kinase. CheA-P phosphorylates a response regulator protein, CheY, that
interacts with rotational "switch" proteins in the flagellar motor.
This causes a change in swimming behavior such that cells migrate
towards chemoattractants (15). A cluster of genes whose products are homologous to five of the six soluble proteins required for chemotaxis in E. coli have recently been identified in
P. putida (2), suggesting that the two species
process sensory information to effect chemotaxis in similar ways.
Although NahY has a signaling domain, potential methylation sites, and
a membrane topology typical of chemotaxis transducer
proteins, it does
not show a high degree of overall amino acid
identity with other MCPs.
This is particularly evident if one
compares the predicted N-terminal
periplasmic domains of transducers
and transducer-like proteins (Fig.
5). The presumed periplasmic
sensing
domain of NahY is clearly an outlier, rather distantly
related to the
N-terminal sensing domains of other bacterial and
archaeal transducer
proteins. This raises the possibility that
NahY may have distinct
chemosensing characteristics. In fact,
several features of NahY
chemoreceptor function remain to be explored.
We still do not know, for
example, exactly what NahY senses and
whether it functions alone or in
concert with NahX. We have been
unable to consistently demonstrate
naphthalene chemotaxis in a
P. putida strain that carries
the
nahY gene in
trans without naphthalene
degradation genes also being present. This may suggest that a
metabolite of naphthalene, rather than naphthalene itself, is
the
chemoattractant. If this is the case, then such a metabolite
is likely
to be an intermediate of the upper naphthalene degradation
pathway,
since the
nahY mutant is not defective in chemotaxis
to
salicylate, the starting compound of the lower pathway.
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FIG. 5.
Phylogenetic tree of the predicted N-terminal
periplasmic domains of selected bacterial transducer proteins
constructed by the AllAll program of the Computational Biochemistry
Research Group (1). The proteins included, sources, and
National Center for Biotechnology Information Entrez protein accession
numbers are as follows: Tap, MCP IV (dipeptide chemoreceptor) from
E. coli, 2506839; Tcp, methyl-accepting chemotaxis citrate
transducer from S. typhimurium, 400235; Tsr, MCP I (serine
chemoreceptor) from E. coli, 400233; Tar, MCP II (aspartate
chemoreceptor protein) from E. coli, 2506837; Trg, MCP III
(ribose and galactose chemoreceptor protein) from E. coli,
2506838; PctC, chemotaxis transducer protein (amino acid chemoreceptor)
from P. aeruginosa, 2626833; PctB, chemotaxis transducer
protein (amino acid chemoreceptor) from P. aeruginosa,
2626836; McpA, methyl-accepting chemoreceptor (presumed) from
Rhodobacter capsulatus, 2126470; HtrII, sensory rhodopsin II
transducer (methyl-accepting phototaxis protein II) from
Halobacterium salinarium, 3023997; McpA, MCP (amino acid
chemoreceptor) from Bacillus subtilis, 730002; McpB, MCP
(amino acid chemoreceptor) from B. subtilis, 730003; TlpB,
MCP (amino acid chemoreceptor) from B. subtilis, 730959;
YvaQ, methyl-accepting chemotaxis-like protein from B. subtilis, 2635882; McpB, methyl-accepting chemoreceptor (presumed)
from R. capsulatus, 2126471; DcrH, methyl-accepting
chemoreceptor (presumed) from Desulfovibrio vulgaris,
887858; HlyB, hemolysin secretion protein precursor from Vibrio
cholerae, 123206; NahY, chemotaxis transducer protein for
naphthalene from P. putida, AF100302.
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That
nahY is located on the NAH7 catabolic plasmid and
cotranscribed with genes for naphthalene degradation suggests that
chemotaxis may be an important adjunct to biodegradation. The
availability of
nahY mutants should facilitate work to
critically
test the possibility that chemotaxis to aromatic
hydrocarbons
may enhance their biodegradation in natural
environments.
Nucleotide sequence accession number.
The nahKJXY
sequences have been assigned GenBank accession no. AF100302.
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ACKNOWLEDGMENTS |
This work was supported by grant MCB9603551 from the National
Science Foundation.
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FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Microbiology, The University of Iowa, Iowa City, IA 52242. Phone: (319) 335-7783. Fax: (319) 335-7679. E-mail:
caroline-harwood{at}uiowa.edu.
Present address: National Exposure Research Laboratory, U.S.
Environmental Protection Agency, Cincinnati, OH 45268.
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Journal of Bacteriology, May 1999, p. 3310-3316, Vol. 181, No. 10
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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