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Journal of Bacteriology, September 1999, p. 5833-5837, Vol. 181, No. 18
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Pathways of Assimilative Sulfur Metabolism in
Pseudomonas putida
Paul
Vermeij and
Michael A.
Kertesz*
Institute of Microbiology, Swiss Federal
Institute of Technology, ETH-Zentrum, CH-8092 Zürich, Switzerland
Received 17 May 1999/Accepted 12 July 1999
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ABSTRACT |
Cysteine and methionine biosynthesis was studied in
Pseudomonas putida S-313 and Pseudomonas
aeruginosa PAO1. Both these organisms used direct sulfhydrylation
of O-succinylhomoserine for the synthesis of methionine but
also contained substantial levels of O-acetylserine sulfhydrylase (cysteine synthase) activity. The enzymes of the transsulfuration pathway (cystathionine 
-synthase and cystathionine 
-lyase) were expressed at low levels in both pseudomonads but were
strongly upregulated during growth with cysteine as the sole sulfur
source. In P. aeruginosa, the reverse transsulfuration pathway between homocysteine and cysteine, with cystathionine as the
intermediate, allows P. aeruginosa to grow rapidly with methionine as the sole sulfur source. P. putida S-313 also
grew well with methionine as the sulfur source, but no cystathionine -lyase, the key enzyme of the reverse transsulfuration pathway, was
found in this species. In the absence of the reverse transsulfuration pathway, P. putida desulfurized methionine by the
conversion of methionine to methanethiol, catalyzed by methionine
-lyase, which was upregulated under these conditions. A transposon
mutant of P. putida that was defective in the
alkanesulfonatase locus (ssuD) was unable to grow with
either methanesulfonate or methionine as the sulfur source. We
therefore propose that in P. putida methionine is converted
to methanethiol and then oxidized to methanesulfonate. The sulfonate is
then desulfonated by alkanesulfonatase to release sulfite for
reassimilation into cysteine.
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INTRODUCTION |
In most microorganisms, the major
route for the biosynthesis of cysteine is the sulfate assimilation
pathway. This process has been best characterized for enteric bacteria
(15) where it involves uptake and activation of inorganic
sulfate followed by stepwise reduction to sulfide. The sulfide is then
condensed with O-acetyl-L-serine, catalyzed by
O-acetyl-L-serine sulfhydrylase (CysK/CysM), to
yield cysteine (15). In enteric bacteria, this process is
controlled by the CysB protein, a LysR-type transcriptional activator,
which is required for the expression of the corresponding genes,
grouped together as the cys regulon (15).
Recently, it has been demonstrated that the genes involved in the
uptake and utilization of taurine (2-aminoethanesulfonate) and other
alkanesulfonates in Escherichia coli and of methanesulfonate
and aromatic sulfate esters in Pseudomonas aeruginosa are
also members of this regulon (14, 23, 24).
In enteric bacteria, methionine biosynthesis is not a part of the
cys regulon, although this pathway, the transsulfuration pathway, begins with cysteine. In this pathway, cysteine displaces the
succinyl moiety of O-succinyl-L-homoserine to
yield cystathionine, catalyzed by cystathionine -synthase (MetB).
This is then followed by a straightforward -elimination that
converts cystathionine to homocysteine, pyruvate, and ammonia,
catalyzed by cystathionine -lyase. Homocysteine is subsequently
methylated to methionine by either metE or metH
gene products. By contrast, yeasts, Rhizobium spp.,
Leptospira spp., P. aeruginosa, and all
gram-positive bacteria examined (Bacillus,
Brevibacterium, Corynebacterium, and
Arthrobacter spp.) use a direct sulfhydrylation for
methionine biosynthesis involving the immediate transfer of sulfide
onto an O-acyl-L-homoserine to yield
homocysteine, catalyzed by homocysteine synthase (MET25/MetZ) (1,
2, 8, 20, 21). Saccharomyces cerevisiae and P. aeruginosa use homocysteine both as the direct precursor for
methionine biosynthesis and for the conversion to cysteine via the
reverse transsulfuration pathway. They also contain the normal
transsulfuration pathway, allowing them to grow equally well on either
cysteine or methionine as the sole sulfur source.
Recently, it was demonstrated that Pseudomonas syringae
synthesizes methionine via the transsulfuration pathway (1),
although the acylated homoserine intermediate appears to be
O-acetyl-L-homoserine (1) rather then
O-succinyl-L-homoserine, as is the case in E. coli (15) and P. aeruginosa
(8). This pathway followed by P. syringae most
closely resembles the pathway in Neurospora crassa
(16) and is distinct from the one in P. aeruginosa. In this paper, we report that Pseudomonas
putida synthesizes both cysteine and homocysteine primarily by
direct sulfhydrylation and that, although the organism grows well with
methionine as the sulfur source, it does not contain the reverse
transsulfuration pathway.
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MATERIALS AND METHODS |
P. putida S-313 (29) and P. aeruginosa PAO1 (11) were cultivated in a sulfur-free
succinate-salts medium, as previously described (13), at 30 and 37°C, respectively. For the cultivation of P. aeruginosa, all the naturally occurring amino acids (40 µg
· ml
1), except methionine and cysteine, were added to
the medium. E. coli MC4100 (3) was grown in a
sulfur-free M63 medium (25) at 37°C. Sulfur sources were
added as described in the text (250 µM). Growth curves were
determined in microtiter plates with 150 µl of culture by using a
SPECTRAmax Plus microtiter plate reader with SOFTmax PRO software
(Molecular Devices). Overnight cultures were washed and diluted
100-fold in sulfur-free succinate-salts medium and pipetted (75 µl)
into the wells of a microtiter plate. Subsequently, 75 µl of minimal
medium containing a 500 µM concentration of the appropriate sulfur
source was added to each well. The plate was prewarmed at 30°C for 20 min and placed in the SPECTRAmax Plus. The optical density at 600 nm
was measured every 5 min. Before every measurement, the plate was
shaken for a period of 30 s to ensure aerobic growth conditions.
Cell extracts for enzyme assays were prepared from cells grown in
5-liter Erlenmeyer flasks containing 500 ml of medium, harvested in the
mid-exponential growth phase as described by Hummerjohann et al.
(12), and stored at 
20°C in the presence of 20%
glycerol until further use. Cystathionine -lyase was measured by the
method of Uren (22) and was always tested immediately, since
the enzyme activity was lost upon freezing. Cystathionine -lyase was
assayed as 2-oxobutanoic acid formation from L-homoserine
or as cysteine formation from cystathionine (17).
O-Acetyl-L-serine sulfhydrylase (cysteine
synthase) activity was assayed according to Nagasawa and Yamada
(18). The amount of cysteine formed was determined by using
the ninhydrin reaction (9).
O-Succinyl-L-homoserine sulfhydrylase
(homocysteine synthase) activity was tested by the same method
described for cysteine synthase with
O-succinyl-L-homoserine as the substrate, with
the exception that the homocysteine formed was quantified by using the
nitroprusside reaction (28). Cystathionine -synthase was assayed in the same reaction mixture as that used for cysteine synthase
with 1 mM (final concentration) L-cysteine. The
disappearance of L-cysteine was measured by using the
ninhydrin reaction (9). Methionine -lyase was measured by
the method of Esaki and Soda (7). Taurine desulfonation was
followed by assaying the 2-oxoglutarate-dependent dioxygenase as
previously described (6), with the exception that
5,5'-dithio-bis-(2-nitrobenzoate) (DTNB; 50 µM) was added to the assay mixture and sulfite release was measured continuously at
412 nm. The two-component alkanesulfonate mono-oxygenase activity (SsuED/MsuED) was tested routinely with DTNB as previously described (5). The alkanesulfonatase assays were incubated on an
Eppendorf Thermomixer (30°C; 450 rpm). Total protein in cell extracts
was determined with the Bio-Rad protein reagent, using bovine serum albumin as the standard.
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RESULTS AND DISCUSSION |
Direct sulfhydrylation reactions for cysteine and homocysteine
biosynthesis in P. putida and P. aeruginosa.
The
ability of P. aeruginosa PAO1 and P. putida S-313
to transfer sulfide directly onto acylserine or acylhomoserine
acceptors was tested in extracts of cells cultivated with a variety of
different sulfur sources. Both organisms exhibited significant cysteine synthase activity (Table 1), a feature
which had previously been thought to be absent in P. aeruginosa (8). Although the cysteine synthase
activities were much lower (20- to 50-fold) than those measured for
E. coli, they were high enough to lead to sufficient cysteine production to support the growth rates observed (approximately 60 nmol/min/mg of protein). Here, it is perhaps interesting to note
that analysis of the data emerging from the Pseudomonas Genome Project
(19) revealed that P. aeruginosa carries
homologues of the E. coli cysK (64% amino acid identity)
and cysM (66% amino acid identity) genes on its chromosome,
encoding O-acetyl-L-serine sulfhydrylases A and
B, respectively. O-Succinyl-L-homoserine sulfhydrylase activity was also found at similar levels in both pseudomonads but not in E. coli, as expected. The direct
sulfhydrylation to homocysteine has been previously characterized in
P. aeruginosa (8), and the homocysteine synthase
activity was found to be encoded by the metZ gene. A
mutation in this gene could be complemented with the E. coli
metB gene (8), encoding cystathionine -synthase, an
enzyme which normally uses
O-succinyl-L-homoserine and cysteine for
cystathionine synthesis. This suggests the presence of a cysteine pool
independent of the reverse transsulfuration pathway in P. aeruginosa, which is consistent with our finding that this species can synthesize cysteine directly from sulfide and
O-acetylserine and not only via homocysteine.
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TABLE 1.
O-Acetyl-L-serine sulfhydrylase
and O-succinyl-L-homoserine sulfhydrylase
activities in cell extracts of P. aeruginosa PAO1, E. coli MC4100, and P. putida S-313 during growth with
various sulfur sourcesa
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To test the importance of the transsulfuration pathway for
P. putida and
P. aeruginosa, we tested the cell extracts
for cystathionine
-lyase activity (Table
2), which cleaves cystathionine into
homocysteine and serine, and for cystathionine
-synthase activity
(data not shown). The activities of these enzymes in
P. putida and
P. aeruginosa were low compared to those
observed in
E. coli.
In the pseudomonads, they were up to
10-fold higher during growth
with cysteine, whereas in
E. coli, the enzyme activity was always
high, except when methionine
was used as the sulfur source. Earlier
work on the
metZ gene
had already shown that the transsulfuration
pathway in
P. aeruginosa is probably not very active (
8), as
is the
case in yeast.
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TABLE 2.
Cystathionine -lyase, cystathionine -lyase, and
methionine -lyase activities in cell extracts of P. aeruginosa PAO1, E. coli MC4100, and P. putida S-313 during growth with various
sulfur sourcesa
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Together, these results suggest that
P. putida S-313 and
P. aeruginosa PAO1 utilize the sulfhydrylation of
O-acetyl-
L-serine
for the synthesis of cysteine
and the direct sulfhydrylation pathway
for the synthesis of methionine.
Both pathways are expressed simultaneously.
Under most growth
conditions, cysteine is not converted to methionine
via cystathionine
and homocysteine. However, when cysteine is
supplied as the sole sulfur
source, cystathionine
-lyase and
cystathionine
-synthase are
expressed, allowing a direct cysteine-to-methionine
conversion to
occur. Although direct sulfhydrylation has now been
found in a growing
number of microorganisms (
2,
4,
8,
20), the reverse
transsulfuration pathway (homocysteine to cysteine)
is still found only
in
P. aeruginosa and
S. cerevisiae. We were
therefore interested in how
P. putida S-313 converts
methionine
to cysteine during growth with the former as the sole sulfur
source.
Methionine-to-cysteine conversion in P. putida.
When
methionine is provided as the sole sulfur source for bacterial growth,
two main metabolic pathways are known that allow conversion of this
compound to cysteine. The methionine may be desulfurized to yield an
inorganic sulfur moiety which enters the cysteine biosynthetic pathway
via the normal sulfate assimilation route. Alternatively, the sulfur
may be retained on the carbon skeleton and the methionine converted to
cysteine via demethylation to homocysteine and subsequent reverse
transsulfuration via cystathionine (Fig.
1).
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FIG. 1.
Pathways of cysteine and methionine biosynthesis in
P. aeruginosa and E. coli. Enzymes: 1, O-acetyl-L-serine sulfhydrylase; 2, cystathionine -synthase; 3, cystathionine -lyase; 4, methionine
synthase; 5, O-succinyl-L-homoserine
sulfhydrylase; 6, S-adenosylmethionine
synthase-methyltransferases-S-adenosylhomocysteine
hydrolase pathway; 7, cystathionine -synthase; 8, cystathionine
-lyase. The dotted arrow indicates the putative utilization of
methionine by E. coli via inorganic sulfate.
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Enteric bacteria, such as
E. coli, which use the former
pathway, grow poorly with methionine as the sulfur source. In the
presence of selenate, growth with methionine is completely halted.
This
has been taken as evidence that methionine utilization in
E. coli proceeds by desulfurization of the methionine molecule
to
yield inorganic sulfate, since selenate is a known inhibitor
of sulfate
uptake and ATP sulfurylase in bacteria and therefore
acts as an
inhibitor of the sulfate assimilation pathway. In
P. aeruginosa, by contrast, growth is rapid with methionine and is
not inhibited by selenate (
10), supporting the presence of a
direct transsulfuration
pathway.
Like
P. aeruginosa,
P. putida grows equally well
with methionine as with other sulfur sources (Fig.
2). Growth with methionine
was slowed but
not halted in the presence of 1 mM selenate, a
concentration which
stopped growth with sulfate completely (Fig.
2). We therefore initially
postulated that
P. putida also contains
the reverse
transsulfuration pathway, allowing a direct methionine-to-cysteine
conversion. To confirm the presence of the reverse transsulfuration
pathway in
P. putida, we measured the key enzyme of this
pathway,
cystathionine
-lyase (Table
2). High levels of this enzyme
were
found in
P. aeruginosa during growth with all sulfur
sources tested,
but no activity was found in cell extracts of
P. putida or
E. coli. This ruled out the possibility of a
direct methionine-to-cysteine
conversion in
P. putida.
However, during growth with methionine,
we found that methionine lyase
activity was approximately 10-fold
upregulated in
P. putida
(Table
2), and we therefore propose
that under these conditions
methionine is converted into methanethiol,
2-oxobutyrate, and ammonia
by the methionine
-lyase. Subsequently,
methanethiol can then be
converted, via an unknown pathway, to
methanesulfonate, which is then
desulfonated to yield sulfite.
A mini Tn
5 transposon mutant
of
P. putida S-313, SN34, which was
isolated for its
inability to grow with sulfonates as the sulfur
source (
27),
also grew very slowly with methionine, confirming
an interconnection
between alkanesulfonate and methionine utilization
in this species.
Complementation of this mutant with the
P. putida ssuED
genes, which encode a reduced flavin mononucleotide-dependent
alkanesulfonatase (
26), restored growth with both
methanesulfonate
and methionine to wild-type levels.
P. aeruginosa contains a second
sulfonatase operon
(
msuEDC) which is involved in methanesulfonate
desulfonation
(
14), and though it is not yet clear whether
P. putida also contains this second operon, our results suggest that
in
P. putida methanesulfonate desulfonation is catalyzed
primarily
by the
ssuED gene products.
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FIG. 2.
Growth of P. putida S-313 on various sulfur
sources in the absence or presence of 1 mM selenate. Growth was
measured in microtiter plates in a SPECTRAmax instrument, as described
in Materials and Methods. O.D.600, optical density at 600 nm.
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Conversion of methionine to cysteine via methanesulfonate and sulfite
is not expected to be inhibited by selenate, since this
compound
affects only the upper pathway of sulfate assimilation.
Unexpectedly,
growth with methanesulfonate was completely halted
in the presence of 1 mM selenate (Fig.
2), and so the inhibitory
effect of selenate on the
broad-substrate-range alkanesulfonate
sulfonatase SsuED was tested in
cell extracts with pentanesulfonate
or methanesulfonate as the
substrate (Table
3). Selenate led
to
approximately 50% inhibition of this enzyme in extracts of
P. putida and
P. aeruginosa. In
E. coli, the
same effect was seen
for pentanesulfonate cleavage (methanesulfonate is
not a substrate
of the
E. coli enzyme), and this was
confirmed with the purified
E. coli SsuED enzyme. This level
of inhibition is consistent with
the reduction in the
P. putida growth rate with methionine that
was found when selenate
was added (Fig.
2). The observed complete
inhibition by selenate of the
growth of
P. putida with methanesulfonate
(Fig.
2) is
therefore probably due to inhibition of methanesulfonate
uptake. As a
comparison, we also tested 2-oxoglutarate-dependent
taurine dioxygenase
(TauD) with and without 1 mM selenate. All
three strains used in this
study exhibited low TauD activity when
grown with sulfate and cysteine
and high TauD activity when grown
with other sulfur sources, as
previously reported (
24), and
the activity was not affected
by selenate at all (data not shown).
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TABLE 3.
Alkanesulfonate desulfonation activities and inhibition
of alkanesulfonatase activity by selenate in cell extracts of P. aeruginosa PAO1, E. coli MC4100, and P. putida S-313 during growth with various
sulfur sourcesa
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In this study, we have demonstrated that
P. putida and
P. aeruginosa are capable of methionine biosynthesis through
either
transsulfuration or direct sulfhydrylation, although the direct
sulfhydrylation pathway is strongly favored. In both organisms,
the
transsulfuration pathway was found to be poorly active and
cysteine is
normally not converted to methionine, except when
the organism is grown
with cysteine as the sole sulfur source.
The pathways found for the
synthesis of methionine and cysteine
in
P. putida S-313
(Fig.
3) resemble those of
P. aeruginosa. However,
compared to the latter organism,
P. putida lacks the reverse transsulfuration
pathway, raising the
question of whether
P. aeruginosa has acquired
this pathway
during evolution or
P. putida has lost it.
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FIG. 3.
Proposed pathways for the biosynthesis of cysteine and
methionine in P. putida S-313. The conversion of
methanethiol to methanesulfonate is still hypothetical. Dotted arrows
indicate that the transsulfuration pathway is not very active in
P. putida S-313. Enzymes: 1, O-acetyl-L-serine sulfhydrylase; 2, cystathionine -synthase; 3, cystathionine -lyase; 4, methionine
synthase; 5, O-succinyl-L-homoserine
sulfhydrylase; 9, methionine -lyase; 10, methanesulfonatase
(SsuED/MsuED). APS, adenosine-5'-phosphosulfate; PAPS,
3'-phosphoadenosine-5'-phosphosulfate.
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ACKNOWLEDGMENTS |
This work was supported by the Swiss Federal Office for Education
and Sciences (grant no. BBW 97.0190) as part of the EC program SUITE
(ENV4-CT98-0723).
The purified SsuD and SsuE proteins from E. coli were a kind
gift from E. Eichhorn.
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FOOTNOTES |
*
Corresponding author. Mailing address:
Mikrobiologisches Institut, ETH-Zentrum/LFV, CH-8092 Zürich,
Switzerland. Phone: 41 1 632 33 57. Fax: 41 1 632 11 48. E-mail:
kertesz{at}micro.biol.ethz.ch.
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Journal of Bacteriology, September 1999, p. 5833-5837, Vol. 181, No. 18
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Abstract
Introduction
