Next Article 
Applied and Environmental Microbiology, July 2001, p. 2873-2882, Vol. 67, No. 7
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.7.2873-2882.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
MINIREVIEW
Oxidation of Reduced Inorganic Sulfur Compounds by
Bacteria: Emergence of a Common Mechanism?
Cornelius G.
Friedrich,*
Dagmar
Rother,
Frank
Bardischewsky,
Armin
Quentmeier, and
Jörg
Fischer
Lehrstuhl für Technische Mikrobiologie,
Fachbereich Chemietechnik, Universität Dortmund, D-44221
Dortmund, Germany
 |
THE SULFUR-OXIDIZING PROKARYOTES |
Biological oxidation of hydrogen
sulfide to sulfate is one of the major reactions of the global sulfur
cycle. Reduced inorganic sulfur compounds (referred to below as sulfur)
are exclusively oxidized by prokaryotes, and sulfate is the major
oxidation product. Sulfur oxidation in members of the
Eukarya is mediated by lithoautotrophic bacterial
endosymbionts (44).
The sulfur-oxidizing prokaryotes are phylogenetically diverse (Fig.
1). In the domain Archaea
aerobic sulfur oxidation is restricted to members of the order
Sulfolobales (21, 58), and in the domain
Bacteria sulfur is oxidized by aerobic lithotrophs or by
anaerobic phototrophs. The nonphototrophic obligate anaerobe Wolinella succinogenes oxidizes hydrogen sulfide to
polysulfide during fumarate respiration (41). The ecology,
physiology, and biochemistry of sulfur-oxidizing bacteria have been
reviewed previously. The neutrophilic chemolithotrophic bacteria have
been reviewed by Kelly et al. (31, 32, 35) and Takakuwa
(63), the acidophilic sulfur-oxidizing bacteria have been
reviewed by Harrison (23) and Pronk et al.
(46), and the molecular genetics of
Acidithiobacillus ferrooxidans has been reviewed by Rawlings
and Kusano (49). The sulfur metabolism of phototrophic
bacteria has been reviewed by Brune (9, 10) and
Trüper and Fischer (65). The physiology and genetics
of both phototrophic and lithotrophic sulfur-oxidizing prokaryotes have been discussed recently (18).
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FIG. 1.
Phylogenetic tree based on 16S rRNA gene sequence
analysis of P. pantotrophus and different sulfur-oxidizing
bacteria. Bar = 1 inferred nucleotide change per 100 nucleotides.
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Prokaryotes oxidize hydrogen sulfide, sulfur, sulfite, thiosulfate, and
various polythionates under alkaline (57), neutral, or
acidic conditions (23). Aerobic sulfur-oxidizing
prokaryotes belong to genera like Acidianus
(18), Acidithiobacillus (36), Aquaspirillum (19), Aquifex
(25), Bacillus (2),
Beggiatoa (60), Methylobacterium
(15, 34), Paracoccus, Pseudomonas (19), Starkeya (33),
Sulfolobus (58), Thermithiobacillus (36), Thiobacillus, and Xanthobacter
(19) and are mainly mesophilic. Phototrophic anaerobic
sulfur-oxidizing bacteria are mainly neutrophilic and mesophilic
(10, 65) and belong to genera like
Allochromatium (formerly Chromatium
[26]), Chlorobium, Rhodobacter, Rhodopseudomonas, Rhodovulum, and Thiocapsa (9).
Lithoautotrophic growth in the dark has been described for
Thiocapsa roseopersicina, Allochromatium vinosum, and other
purple sulfur bacteria, as well as for purple nonsulfur bacteria like
Rhodovulum sulfidophilum (formerly Rhodobacter sulfidophilus) (24), Rhodocyclus
genatinosus, and Rhodopseudomonas acidophila (39,
56). This capacity may be based on related biochemical
mechanisms of sulfur oxidation in lithotrophic and phototrophic bacteria.
Autotrophic bacteria fix carbon dioxide either via the reductive
pentose phosphate cycle or via the reductive tricarboxylic acid cycle.
Methylotrophic bacteria fix formaldehyde either via the ribulose
monophosphate route or via the serine pathway (16, 61).
Reductant released from sulfur oxidation is used in lithotrophic bacteria for aerobic respiration and carbon dioxide reduction, while in
anaerobic phototrophic bacteria reductant is used mainly for carbon
dioxide fixation. Sulfur oxidation by methylotrophic bacteria has been
observed upon growth with methylated sulfur compounds, such as dimethyl
sulfide (34). Few reports have focused on the
sulfur-oxidizing potential of these organisms (15, 16, 61,
62) due to the major interest in their methylotrophic characteristics.
Two groups of sulfur-oxidizing lithotrophic bacteria have been
distinguished previously; members of one group are able to utilize
polythionates, and members of the other group are not able to do this
(18, 35). On the basis of physiological and biochemical
data, at least two major pathways have been proposed for different
sulfur-oxidizing bacteria: (i) the sulfur oxidation pathway and (ii)
the S4 intermediate pathway involving polythionates (35). Here we discuss the sox gene cluster of
Paracoccus pantotrophus and the biochemistry and functions
of the encoded proteins. On the basis of our analysis, together with
available genomic data, we concluded that different metabolic reactions
merge into a common mechanism in lithotrophic and phototrophic
sulfur-oxidizing bacteria.
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THE SULFUR-OXIDIZING SYSTEM OF P. PANTOTROPHUS |
sox gene cluster.
P. pantotrophus
(48) is a gram-negative, neutrophilic, facultatively
lithoautotrophic bacterium that is able to grow with thiosulfate or
with molecular hydrogen as an energy source and with a large variety of
carbon sources. The gene cluster of P. pantotrophus coding
for sulfur-oxidizing ability (Sox) comprises at least two
transcriptional units with 15 genes. Seven genes, soxXYZABCD, code for proteins essential for sulfur oxidation
in vitro. These genes and soxFGH are induced by thiosulfate
(11, 20, 42, 51a, 69, 70). Four open reading frames
(ORFs), ORF1, ORF2, and shxVW, are located upstream of
soxX (Fig. 2), and the
shxVW ORFs are cotranscribed (F. Bardischewsky and C. G. Friedrich, submitted for publication).
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FIG. 2.
Schematic map of the sox gene cluster of
P. pantotrophus and identified or putative sox
genes of other sulfur-oxidizing bacteria. ORFs predicting homologous
proteins are indicated by the same color. ORFs that encode proteins not
homologous to Sox proteins of P. pantotrophus are white. The
numbers indicate the positions of putative sox genes in the
complete genomes. Accession numbers of the ORFs are given in Table 1.
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The Sox proteins of
P. pantotrophus are located in the
periplasm, as shown by selective extraction of periplasmic proteins
(
20), and signal peptides have been predicted for all of
the
proteins except SoxZ (Table
1). The
Sox proteins are transported
to the periplasm either
via the Sec system or via the Tat system.
Twin arginine motifs in the
signal peptides are diagnostic for
protein transport via the Tat system
(
6,
8,
68) and are
predicted for SoxY, SoxB, SoxC, SoxF,
SoxG, and possibly SoxH
(Table
1). The SoxY and SoxZ proteins do not
contain a prosthetic
group, redox center, or metal (
20),
and SoxZ is likely to be
cotransported through the cytoplasmic membrane
by SoxY in hitchhiker
fashion, as previously shown for the
heterodimeric hydrogenases
of
Escherichia coli
(
51) and
Ralstonia eutropha (
7).
ORF1 predicts a transcriptional regulator of the ArsR family, and ORF2
predicts a periplasmic thioredoxin. Both of these ORFs
are oriented
divergent to the
sox gene cluster (Fig.
2).
shxV predicts a protein with six transmembrane channel-forming helices
and a
conserved cysteine at helices 1 and 4. ShxV is structurally
related to
CcdA of
P. pantotrophus, which is involved in cytochrome
c biogenesis. CcdA mediates transport of reductant from the
cytoplasm
to the periplasm for rereduction of the periplasmic
apoprotein
prior to heme addition. Disruption of
ccdA
results in a complete
deficiency of
c-type cytochromes,
which in turn affects metabolic
reactions involving
c-type
cytochromes, including sulfur oxidation
(
4). Disruption of
shxV by the
-kanamycin interposon disables
mutant GB
V
so that it cannot grow lithotrophically with thiosulfate
and with
molecular hydrogen. Cytochrome
c formation is not affected
in GB
V, demonstrating that ShxV has a function distinct from
that of
CcdA. Addition of cysteine to the medium restores growth
of strain
GB
V with hydrogen but not growth of this strain with
thiosulfate.
However, the thiosulfate-oxidizing activity of mixotrophically
grown
GB
V is increased about 20-fold by 0.3 mM cystine and 2-fold
by 0.3 mM cysteine, suggesting that there is a periplasmic oxidation
reaction.
shxW predicts a periplasmic thioredoxin that is unusual
with
respect to the predicted distribution of
-strands and
-helices,
which very likely specify its role either in a redox reaction
or for
transport of reductant (Bardischewsky and Friedrich,
submitted).
The
soxEFGH genes are located downstream of
soxD
(Fig.
2). These genes are coexpressed with the
sox
structural genes, and
thiosulfate-induced formation of SoxFGH has been
demonstrated.
However, a function could not be determined for these
proteins
since an in-frame deletion in
soxF and
complementation did not
reveal obvious phenotypes of the mutants
(
51a).
Biochemistry of the Sox system of P. pantotrophus.
Seven sox structural genes code for four proteins. SoxXA,
SoxYZ, SoxB, and SoxCD are required for sulfur-dependent cytochrome c reduction. SoxXA is a heterodimeric c-type
cytochrome; SoxX (molecular mass, 14,834 Da) is a monoheme subunit, and
SoxA (molecular mass including the heme moieties, 30,452 Da) is a
diheme subunit. SoxYZ is composed of SoxY and SoxZ, which have
predicted molecular masses of 10,977 and 11,718 Da, respectively.
Neither SoxY nor SoxZ contains a cofactor or metal. The molecular mass
of SoxY as determined by electrospray mass spectrometry (11,094 Da)
differs from the predicted molecular mass of the mature protein by 117 Da (20). Thiosulfate covalently bound to SoxY accounts for
112 Da of the difference, and the higher molecular mass suggests that such an adduct is formed. In native gradient polyacrylamide gel electrophoresis gels SoxYZ appears as a heterodimer and as a 50-kDa 22 heterotetramer, and two forms of the
heterodimer that have molecular masses of 29 and 31 kDa are observed
(20).
The monomeric SoxB protein contains two manganese atoms
(
70), and the predicted molecular mass (58,611 Da) is
identical
to the molecular mass determined by electrospray mass
spectrometry.
Previous differences between the predicted and determined
molecular
masses (
20) were resolved by analysis of the
almost complete
primary sequence and the N-terminal 32-pyroglutamate,
which also
identified the cleavage site of the signal peptidase (G. Grelle,
unpublished
data).
SoxCD is an
22 heterotetramer (molecular
mass, 190,000 Da); SoxC is the molybdenum cofactor-containing subunit
(molecular
mass, 43,897 Da), and SoxD is the diheme
c-type
cytochrome (molecular
mass including the two heme moieties, 38,815 Da)
(
47).
soxE predicts a diheme
c-type cytochrome
(molecular mass of the mature protein, 23,616 Da), and it is thought
that SoxE is
associated with SoxF (
70).
soxF
encodes a 42,832-Da monomeric
flavoprotein that includes a flavin
moiety, as determined by electrospray
mass spectrometry
(
51a). The primary sequence of SoxF is very
similar to the
primary sequence of FccB (
70), the flavoprotein
of
flavocytochrome
c-sulfide dehydrogenase of the phototrophic
bacterium
A. vinosum (
71). SoxF does not
exhibit sulfide dehydrogenase
activity and appears not to be associated
with a cytochrome (
51a).
soxG codes for a
29,657-Da polypeptide with two zinc binding motifs.
The homodimeric
SoxG molecule contains 0.90 atom of zinc per subunit.
soxH
codes for a 32,317-Da protein with a zinc binding motif and
another
metal binding motif. By using homodimeric SoxH it has
been determined
that there is 0.29 atom of zinc and 0.20 atom
of copper per subunit
(
51a).
Catalytic properties of the Sox system of P. pantotrophus.
The Sox system reconstituted from SoxXA,
SoxYZ, SoxB, and SoxCD mediates thiosulfate-, sulfite-, sulfur-, and
hydrogen sulfide-dependent cytochrome c reduction, and each
of the proteins alone is catalytically inactive (20, 51a).
Thiosulfate is oxidized by the system according to equation 1,
and sulfite is oxidized according to equation 2. Sulfite is also
oxidized without SoxCD. This result excludes a function as a sulfite
dehydrogenase and suggests a novel function for this molybdoenzyme:
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(1)
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(2)
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Without SoxCD 2 mol of electrons is produced per mol of
thiosulfate, and addition of SoxCD increases the yield to eight
electrons
(
20). Since no free intermediate of sulfur
oxidation is observed,
we suggest that SoxCD acts as a dehydrogenase at
a protein-bound
sulfur atom, and this protein is designated sulfur
dehydrogenase.
This suggestion is in accordance with the phenotype of a
mutant
with an in-frame deletion in
soxC that is not able to
grow lithotrophically
with thiosulfate but is still able to oxidize
thiosulfate, although
at a low rate (
51a,
70).
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SOX SYSTEMS OF OTHER SULFUR-OXIDIZING BACTERIA |
Oxidation of hydrogen sulfide to sulfur.
Phototrophic bacteria
like Rhodobacter capsulatus, Pelodictyon luteolum, and some
Chlorobium species anaerobically oxidize hydrogen sulfide to
sulfur in the light. In vitro, hydrogen sulfide is oxidized to sulfur
by some phototrophic and chemotrophic bacteria via a flavocytochrome
c-sulfide dehydrogenase (equation 3) (22, 66)
and a sulfide-quinone reductase (equation 4) (53).
Flavocytochrome c of A. vinosum is not required
for phototrophic growth with hydrogen sulfide, as shown by disruption
of the cytochrome subunit fccA, since no obvious phenotype
is observed for a fccA:: mutant
(50).
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(3)
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(4)
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Therefore, it has been suggested that sulfide-quinone reductase is
essential for growth of
A. vinosum with hydrogen sulfide
(
50). Sulfide-quinone reductase has been shown to be
essential
for phototrophic growth of
R. capsulatus with
hydrogen sulfide
(
53). Hydrogen sulfide is the only sulfur
substrate that
R. capsulatus utilizes for phototrophic
growth which is oxidized
to sulfur, while
A. vinosum
oxidizes hydrogen sulfide to sulfate
(
18). Thus, the
enzyme systems that oxidize hydrogen sulfide
to sulfur and to sulfate
are probably
different.
SoxF of
P. pantotrophus is not required for oxidation of
reduced inorganic sulfur compounds in vitro (
20).
Moreover, a mutant
with an in-frame deletion in
soxF grows
with thiosulfate, just
as the wild-type does (
51a). Two
flavoprotein homologues have
been observed in different genomes of
sulfur-oxidizing bacteria
(Fig.
2). Since the functions of these
homologues are unknown,
it is not known if they can complement each
other.
Sulfide-quinone reductase has been characterized from
Chlorobium (
55),
R. capsulatus
(
54), and the cyanobacterium
Oscillatoria limnetica (
3). Sulfide-quinone reductase activity is
also present
in
P. pantotrophus (
52), but it
does not account for lithotrophic
hydrogen sulfide oxidation since an
insertional mutant with a
mutation in the
soxB gene is not
able to oxidize hydrogen sulfide
and thiosulfate (
11).
Oxidation of sulfur to sulfate.
The first
thiosulfate-oxidizing enzyme system analyzed in detail (equation 1) was
that of Paracoccus versutus (formerly Thiobacillus versutus [30]). This system (reviewed in reference
35) is composed of enzyme A (molecular mass, 16,000 Da),
enzyme B (60,000 Da), hexameric cytochrome c551
(260,000 Da) with 43,000-Da subunits, which is intimately associated
with sulfite dehydrogenase (44,000 Da), and homodimeric cytochrome
c552.5 (35). An important study has
demonstrated that enzyme A binds thiosulfate to sulfite as a
competitive inhibitor (40). In spite of differences in the subunit compositions of enzyme A, cytochrome
c552.5, and cytochrome c551-sulfite dehydrogenase compared to SoxYZ,
SoxXA, and SoxCD, respectively, the similar partial primary sequences
of P. versutus Sox proteins (20, 69) suggest
that the system is similar to that of P. pantotrophus with
respect to structure and function (18):
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(5)
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(6)
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(7)
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(8)
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From other sulfur-oxidizing bacteria different enzymes involved in
oxidation or hydrolysis of inorganic sulfur compounds
have been
characterized (equations
5 to 7). The reactions, however,
do not
involve oxidation of sulfur to sulfate. From
Acidianus brierleyi a sulfur oxygenase was described (
17), and
from
Acidianus ambivalens a sulfur oxygenase-reductase was
described (
37,
38).
The two proteins probably function
identically and produce sulfite,
hydrogen sulfide, and thiosulfate from
sulfur and molecular oxygen
(equation
8). No link to energy metabolism
has been reported (
38),
and the significance of a sulfur
oxygenase-reductase in energy
metabolism is not clear. This enzyme has
not been detected in
Bacteria.
Sulfite oxidoreductase oxidizes sulfite to sulfate (equation
2) and has
been characterized from
Starkeya novella and some
members of
the
Eukarya (
28,
64). Sulfite oxidoreductase is
present in
S. novella at high specific activity, and its
function
clearly differs from that of SoxCD. Thiosulfate dehydrogenase
oxidizes thiosulfate to tetrathionate (equation
5) and is present
in
various litho- or phototrophic sulfur-oxidizing bacteria (
9,
31). Trithionate hydrolase yields thiosulfate and sulfate. In
general, polythionate hydrolysis yields polysulfide sulfate esters
[O
3S-S-(S-)
x]
2
, and these
esters decompose spontaneously to sulfur and thiosulfate
(
59).
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ANALYSIS OF GENOME SEQUENCES |
Proteins homologous to the Sox proteins of P. pantotrophus were found in members of the domain
Bacteria but not in members of the domain
Archaea. From the complete genome of Sulfolobus solfataricus only a periplasmic sulfite dehydrogenase was
predicted (J. van der Oost, personal communication). Proteins
homologous to the Sox proteins of P. pantotrophus were
detected in members of the domain Bacteria, such as the
thermophile Aquifex aeolicus (25), the
moderately thermophilic green bacterium Chlorobium tepidum (67), and the purple bacterium
Rhodopseudomonas palustris (65). For the
facultative methylotroph Methylobacterium extorquens (1, 45) essential Sox proteins were deduced from the
partial genome sequence (Table 1). Partial sox gene clusters
with the same order of genes as P. pantotrophus were
detected in S. novella and Pseudaminobacter
salicylatoxidans KCT001 (Fig. 2), both of which grow with
tetrathionate (29, 43). It was predicted that these
proteins are located in the periplasm and are transported to the
periplasm from the cytoplasm via either the Tat system or the Sec
system (6, 18, 68).
Analysis of genome data allows workers to differentiate the function of
SoxB and SoxC from the function of their homologues. SoxB proteins
exhibit significant identities to 5'-nucleotidases but are distinct
from these molecules on a protein phylogenetic tree (Fig.
3A). In view of the differences and since
phosphate is not involved in sulfur oxidation but is isosteric to
sulfate, we suggest that SoxB proteins function as sulfate
thiohydrolases but not as phosphatases.
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FIG. 3.
Phylogenetic relationships of SoxB and SoxC homologous
proteins of different bacteria. (A) Proteins that were identified as
SoxB homologues (B) and 5'-nucleotidases (N). (B) SoxC (C) and sulfite
oxidoreductase (S) homologous proteins The bar indicates the estimated
distance of accepted point mutations per 100 amino acids.
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It has been suggested that SoxC proteins act as dehydrogenases with the
protein-bound sulfur atom, while their homologues, sulfite
oxidoreductases (like SorA), oxidize free sulfite to sulfate. Both
types of enzymes are molybdenum hydroxylases, and the suggested different functions of SorA and SoxC coincide with the separate positions of the molecules on the protein phylogenetic tree (Fig. 3B).
sox genes of phototrophic sulfur-oxidizing
bacteria.
The sox gene cluster of R. palustris is similar to that of P. pantotrophus and
comprises 16 genes equivalent to ORF1, ORF2, shxVW, and
soxXAYZBCDEF1F2; soxF1
and soxF2 predict flavoproteins. Two
hypothetical genes are in the cluster, while a soxG
homologue is located at some distance. A second set of soxA
and soxYZ genes and a gene predicting a sulfatase are
located outside the sox gene cluster (Fig. 2). The
soxA gene in the sox cluster, RRPA00637, predicts
a monoheme, and the soxA gene outside the sox
gene cluster, RRPA02737, predicts a diheme cytochrome (Fig. 2; Table
1).
In a partial genome sequence of
C. tepidum a
sox
gene cluster comprising eight genes equivalent to
soxF1XYZAB followed by
a gene predicting a
thioredoxin was detected. A hypothetical gene
separated
soxB
and
soxA. Outside the cluster were genes predicting
two
flavoproteins, one SoxE homologue, and two sulfide-quinone
reductases.
Genes equivalent to
shxV,
shxW, and
soxCD essential
for lithotrophic growth of
P. pantotrophus with thiosulfate have
not been detected in the
incomplete genome sequence of
C. tepidum (Fig.
2).
In
A. vinosum a partial
sox gene cluster that
included
soxB and
soxXA was identified by using
PCR technology (
13). These
genes may be essential for
sulfur oxidation in this organism since
inactivation of
fccA
encoding the cytochrome subunit of flavocytochrome
c-sulfide
dehydrogenase and inactivation of the
aprBA locus encoding
adenosine-5'-phosphosulfate reductase did not affect hydrogen
sulfide
oxidation (
50) or sulfite oxidation (
12).
R. capsulatus oxidizes hydrogen sulfide to sulfur, and this
activity is linked to sulfide-quinone reductase. Disruption of
sqrA results in an inability to grow phototrophically with
hydrogen
sulfide. Thus, this system is clearly different from that
described
for other sulfur-oxidizing bacteria which oxidize inorganic
reduced
sulfur compounds to sulfate. From the available genome sequence
data for
R. capsulatus no Sox protein homologue except a
flavoprotein
has been
detected.
sox genes of lithotrophic sulfur-oxidizing
bacteria.
A. aeolicus is an obligately aerobic
chemolithotrophic bacterium. This organism requires molecular hydrogen
for lithoautotrophic growth and does not grow with thiosulfate alone.
However, thiosulfate increases the cellular yield, indicating that it
is used for energy conservation (25). The sox
gene cluster of A. aeolicus comprises 10 genes. A gene
predicting a thioredoxin is followed by genes equivalent to
soxYZAB and soxH. soxB and
soxH are separated by three ORFs; one of these ORFs predicts
a thiosulfate sulfur transferase (rhodanese), while two ORFs have
unknown functions. The sulfite dehydrogenase homologue-encoding gene is
separated from the sox gene cluster of A. aeolicus. Also, two genes predicting homologues of the
flavoprotein SoxF of P. pantotrophus and two putative
sqr genes are separated from the gene cluster (Fig. 2). The
incomplete genomic sequence of M. extorquens predicts that
there are 10 sox genes, 5 of which are incomplete, and these
10 genes are equivalent to shxV'W', soxXYZ, soxB', soxCD',
soxE, and soxG'. This finding suggests that M. extorquens is a sulfur-oxidizing bacterium. In fact, this organism
utilizes thiosulfate, which increases the cellular yield during
mixotrophic growth, and sulfur dehydrogenase (SoxCD) antigens are
detected in cells grown with thiosulfate but not in cells grown without
thiosulfate (J. Fischer and C. G. Friedrich, unpublished data).
In the tetrathionate-oxidizing organism
S. novella, soxC
predicting sulfur dehydrogenase has been identified together with
truncated
soxB' and
soxD' genes. The gene order
soxB'CD' is identical
to that in
P. pantotrophus
and may indicate that the gene clusters
are similar. The
sorAB genes encode sulfite oxidoreductase and
may be
separated from
soxB'CD' (Fig.
2; Table
1). The proposal
that
there are two thiosulfate-oxidizing systems in
S. novella was based on the presence of two sulfite dehydrogenase homologues,
SorAB and SoxCD (
29). The proposed different functions of
SoxCD
of
S. novella and SorAB bring into question whether
there are
two sulfur oxidation pathways and whether SorAB is the only
representative
of the second pathway. Moreover, induced
S. novella cells oxidize
sulfite at a high rate, which
P. pantotrophus is unable to do,
and the latter organism lacks
sulfite oxidoreductase activity
(
5,
11). In light of the
genomic data, a second pathway for
thiosulfate oxidation appears to be
unlikely, and confirmation
of this hypothesis will require inactivation
of either SorAB or
SoxCD in
S. novella.
In the tetrathionate-oxidizing organism
P. salicylatoxidans
KCT001 a
soxZ'AB' gene order is observed (Fig.
2). The
predicted
diheme
c-type cytochrome SoxA is highly homologous
to SoxA of
P. pantotrophus and the corresponding cytochromes
of other phototrophic
or lithotrophic sulfur-oxidizing bacteria (Table
1). A partial
soxZ gene is located upstream of
soxA, and downstream a truncated
ORF predicts a partial
leader peptide of SoxB. The order of these
genes is identical to the
order in
P. pantotrophus (Fig.
2). Disruption
of
soxA of
P. salicylatoxidans KCT001 results in an
inability
to grow with and to oxidize thiosulfate and tetrathiothionate
(
43), demonstrating that SoxA is essential for sulfur
oxidation
and that polythionates and thiosulfate may be oxidized to
sulfate
by the same
system.
Common Sox proteins of different sulfur-oxidizing bacteria.
The different Sox systems are located exclusively in the periplasm.
According to the available data, the sox genes appear to be
clustered, and homologues of SoxA, SoxB, SoxY, and SoxZ are present in
phototrophic, lithotrophic, and methylotrophic bacteria which oxidize
reduced sulfur compounds to sulfate (in M. extorquens a SoxA
homologue is missing from the incomplete genome sequence). The Sox
proteins share the novel motif of SoxY and conserved regions of SoxZ
and SoxB. The novel motif (V/I)KV(T/S)(V/I)GGC is located at the C
terminus of SoxY (Fig. 4), and the
cysteine residue is predicted to bind to the sulfur atom that is
oxidized to sulfate. This prediction is based on the difference between the determined molecular mass of SoxY and the molecular mass predicted from the nucleotide sequence and determined from the amino acid sequence (20).
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FIG. 4.
Predicted sulfur binding motifs of SoxY proteins and
conserved signatures of SoxZ proteins of different sulfur-oxidizing
bacteria. P. p., P. pantotrophus; R. p., R. palustris; C. t., C. tepidum; A. a., A. aeolicus; M. e., M. extorquens; AA, amino acid
sequence.
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SoxZ proteins contain two signatures, HXM(E/D)(T/S) GXK(D/T) and
SX(N/D)PY (Fig.
4). The cysteine residue present in SoxZ
of
P. pantotrophus and
M. extorquens appears not to be
required
for linkage of the proteins for cotransport through the
cytoplasmic
membrane since periplasmic SoxZ proteins from other sources
lack
this cysteine. Sulfur oxidation in both organisms is strictly
aerobic, while sulfur oxidation in phototrophic bacteria is anaerobic
and sulfur oxidation in
A. aeolicus is microaerophilic. Some
phototrophic
bacteria grow lithotrophically in the dark under
microaerophilic
conditions with reduced sulfur compounds (
27,
39). Therefore,
the cysteine residue of SoxZ may play a role in
coordination of
the Sox proteins or in aerobic sulfur oxidation. Some
SoxA homologues
are either monoheme or diheme cytochromes. The
difference may
also have significance for aerobic or anaerobic sulfur
metabolism
in phototrophic sulfur bacteria or for differences in the
initial
reaction of sulfur
oxidation.
| |
PROPOSAL OF THE MECHANISM OF SULFUR OXIDATION |
Functions of the Sox proteins.
The reconstituted Sox system
of P. pantotrophus performs sulfite-, thiosulfate-,
sulfur-, and hydrogen sulfide-dependent cytochrome c
reduction (20, 51a). Oxidation of sulfite by SoxXA, SoxYZ, and SoxB is consistent with the finding that SoxCD does not function as
a sulfite dehydrogenase but functions as a sulfur dehydrogenase (20, 51a). The c-type cytochrome SoxXA may (i)
act as a specific electron mediator, (ii) fuse SoxY with the sulfur
substrate in an oxidative reaction (equation 9 [see below]), or (iii)
fuse SoxY and SoxZ in acrobic lithotrophs, thus acting as a heme
enzyme. The catalytic properties of the Sox proteins of P. pantotrophus and the cysteine motif of SoxY suggest a mechanism
for sulfur oxidation. The cysteine residue of SoxY is exposed at the C
terminus (Fig. 4). Thus, its sulfur atom is located at the tip of the
protein and is able to swing to either SoxXA, SoxCD, or SoxB.
Proposed reactions and intermediates.
The N-terminal amino
acid sequence of SoxZ is highly homologous to that of enzyme A of
P. versutus (20), suggesting that the function
of SoxYZ is identical to the function of enzyme A. Enzyme A of P. versutus binds thiosulfate and sulfite. It has been suggested that
binding of sulfite occurs at a protein disulfide group
(40). By analogy, complexes of the two substrates may be
similarly formed by SoxYZ of P. pantotrophus. Each subunit contains a single cysteine whose thiols are able to form a disulfide bond. SoxZ molecules of phototrophic bacteria lack a cysteine residue,
and SoxXA may initiate oxidation of thiosulfate to form SoxY-thiocysteine-S-sulfate (equation 9). SoxB would hydrolyze sulfate
from the thiocysteine-S-sulfate residue to give S-thiocysteine (equation 10). SoxCD could then oxidize the outer sulfur atom to SoxY-cysteine-S-sulfate (equations 11 to 13). Finally, sulfate may
again be hydrolyzed and removed by SoxB to regenerate the cysteine
residue of SoxY (equation 14). The sequence of reactions is summarized
in Fig. 5.
Sulfite oxidation does not require SoxCD. Sulfite may also be added to
SoxY to form SoxY-cysteine-S-sulfate (equation
15),
which would be
subsequently hydrolyzed by SoxB, yielding sulfate
(equation
14).
Hydrogen sulfide may be initially oxidized by SoxXA
to form an
S-thiocysteine residue of SoxY (equation
16) with further
oxidation
(equations
11 to 13) and hydrolysis (equation
14), and
sulfur may be
initially oxidized similarly, as proposed for hydrogen
sulfide.
|
(9)
|
|
(10)
|
|
(11)
|
|
(12)
|
|
(13)
|
|
(14)
|
|
(15)
|
|
(16)
|
Tetrathionate is hydrolyzed by tetrathionate hydrolase to sulfate
and thioperoxymonosulfate ([O
3S-S-S]
2). Its
spontaneous decomposition to sulfur and thiosulfate (
59)
enables the same Sox system to oxidize both products. SoxYZAB
proteins
appear to be crucial for sulfur oxidation and are present
in all
sulfur-oxidizing bacteria, as deduced from the available
data (Fig.
2).
In the hyperthermophile
A. aeolicus a SoxC homologue
has not
been detected, while SorA appears to be present. Also,
ShxVW homologues
are missing from the genome of
A. aeolicus. In
this
hyperthermophile initiation of sulfur oxidation may occur
as it does in
other bacteria but may proceed differently, as proposed
here.
| |
CONCLUSION |
The sulfur-oxidizing enzyme system of P. pantotrophus
is able to oxidize different reduced inorganic sulfur compounds. It is
proposed that the sulfur atom oxidized binds covalently to the cysteine
residue of the SoxY protein to form S-thiocysteine. The outer sulfur
atom is oxidized by the sulfur dehydrogenase SoxCD, and sulfate is
hydrolyzed by the sulfatase SoxB. From available genome sequence data
for sulfur-oxidizing bacteria evidence has emerged that similar
proteins are present in anaerobic phototrophic and aerobic lithotrophic
bacteria but not in the archaeon S. solfataricus. Thus,
oxidation of sulfur to sulfate may be mediated by very similar systems
in bacteria. However, differences may involve the mechanism of linkage
of the sulfur atom to be oxidized with SoxY during aerobic and
anaerobic sulfur metabolism in lithotrophic and phototrophic bacteria.
Also, the systems may differ with respect to the specificities of the
actual sulfur substrates.
| |
ACKNOWLEDGMENTS |
We thank Christiane Dahl for making available the nucleotide
sequence-predicting sox genes of A. vinosum prior
to publication, John van der Oost for performing the BLAST search of
the S. solfataricus genome for Sox protein homologues of
P. pantotrophus, and Erko Stackebrandt for providing the 16S
ribosomal DNA sequence of P. salicylatoxidans KCT001 prior
to publication.
This study was supported by grant Fr318/6-3 from the Deutsche
Forschungsgemeinschaft and the Ministerium für Wissenschaft und
Forschung des Landes Nordrhein-Westfalen.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Lehrstuhl
für Technische Mikrobiologie, Fachbereich Chemietechnik,
Universität Dortmund, Emil-Figge-Strasse 66, D-44221 Dortmund,
Germany. Phone: 49-231 755 5115. Fax: 49-231 755 5118. E-mail:
friedric{at}ct.uni-dortmund.de.
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Applied and Environmental Microbiology, July 2001, p. 2873-2882, Vol. 67, No. 7
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.7.2873-2882.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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