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J Bacteriol, June 1998, p. 2975-2982, Vol. 180, No. 11
Department of Civil Engineering,
Technological Institute, Northwestern University, Evanston,
Illinois 60208-3109,1 and
Marine
Biological Laboratory, Woods Hole, Massachusetts
02543-10152
Received 12 January 1998/Accepted 24 March 1998
Microorganisms that use sulfate as a terminal electron acceptor for
anaerobic respiration play a central role in the global sulfur cycle.
Here, we report the results of comparative sequence analysis of
dissimilatory sulfite reductase (DSR) genes from closely and distantly
related sulfate-reducing organisms to infer the evolutionary history of
DSR. A 1.9-kb DNA region encoding most of the The ability to use sulfate as
a terminal electron acceptor is characteristic of several
bacterial lineages and one thermophilic genus of Archaea. In
these prokaryotes, the enzyme dissimilatory sulfite
reductase (DSR) catalyzes the six-electron reduction of (bi)sulfite to sulfide, which is the central energy-conserving step of sulfate respiration (25). One archaeal
(Archaeoglobus fulgidus) and four bacterial DSRs have
so far been characterized by enzyme properties (8, 14, 21, 22,
36). Characterized bacterial enzymes and typical sources
include desulfoviridin (e.g., Desulfovibrio
vulgaris), desulforubidin (e.g., Desulfovibrio
desulfuricans Norway), P582 (e.g., Desulfotomaculum
ruminis), and desulfofuscidin (e.g., Thermodesulfovibrio
yellowstonii). Although they differ in absorption spectra,
electrophoretic mobilities, and redox properties, all characterized
bacterial enzymes have an Members of the redox enzyme superfamily share enzyme properties or gene
sequence motifs with the anaerobically expressed sulfite reductase from
Salmonella typhimurium (17), the inducible
sulfite reductase from Clostridium pasteurianum
(13), and the "reverse sulfite reductases"
detectable in the phototrophic sulfur bacterium Chromatium
vinosum and in the sulfur-oxidizing chemolithotroph Thiobacillus denitrificans (31, 32). Thus, all
characterized enzymes that catalyze either the oxidative or reductive
(dissimilatory or assimilatory) transformation between sulfite and
sulfide appear to be related. This study addresses the question of
archetype. Was there a common progenitor, and if so, what was its
physiological function? The recent observation of high sequence
similarity between the DSRs of A. fulgidus and
Desulfovibrio vulgaris (20), representatives of
the Archaea and Bacteria domains, respectively,
suggested either a horizontal gene transfer or a common origin of a
highly conserved reductase. To distinguish between these alternatives,
we determined the gene histories of the Isolation of nucleic acids, gene amplification procedures, and
Southern hybridization.
Genomic DNA was isolated from the
reference organisms as previously described (4). The primers
DSR1F (5'-AC[C/G]CACTGGAAGCACG-3'), DSR2F
(5'-CTGGAAGGA[C/T]GACATCAA-3', modified from reference
20), DSR3F
(5'-GAAGAA[C/G]ATG[A/T]ACGGGTT-3'), and DSR4R
(5'-GTGTAGCAGTTACCGCA-3', modified from reference
20) were dissolved to a concentration of 10 pmol/µl. For PCR amplification, 1 µl of each primer solution, 10 to
100 ng of DNA, 5 µl of 10× PCR buffer (500 mM Tris [pH 8.3], 20 mM
MgCl2, 5 to 10% Ficoll, 10 mM Tartrazine), 5 µl of 10×
bovine serum albumin (2.5 mg/ml), 5 µl of 10× deoxynucleoside
triphosphates (2 mM [each] dATP, dCTP, dGTP, and dTTP), and 2 U of
Taq DNA polymerase were combined in a final reaction volume
of 50 µl and loaded and sealed in a capillary tube. After initial
denaturation for 15 s at 94°C, amplification was carried out in
a 1650 Air Thermo-Cycler (Idaho Technology) for 30 cycles with each
cycle consisting of 15 s at 94°C, 20 s at 54°C, and
54 s at 72°C. The reaction was completed by a final extension at
72°C for 1 min. PCR products were loaded together with a 1-kb DNA
ladder molecular size marker on a 0.8% agarose gel to evaluate the
PCR. Southern transfers were performed by treating the gel with 250 mM
HCl for 10 min (DNA depurination) and blotting the DNA onto a
MagnaCharge Nylon membrane (MSI) following instructions published
by Boehringer Mannheim Corporation (3a). A 243-bp
double-stranded DNA probe labeled with digoxigenin-11-dUTP was prepared
by PCR (as described above) with the primers DSR1F and DSR5R
(5'-TGCCGAGGAGAACGATGTC-3') and Desulfovibrio
vulgaris template DNA. This probe targets a conserved region of
the analyzed DSR DSR gene cloning, sequencing, and phylogeny inference.
Untreated and EcoRI-digested PCR products were ligated
into pCRTMII plasmids and transformed into ONE SHOT
competent Escherichia coli cells following the
manufacturer's directions (TA Cloning System; Invitrogen). DNA
sequences were obtained from double-stranded insert templates with M13
forward and reverse, infrared dye-labeled primers and a 4000L automated
sequencer according to the manufacturer's instructions (LI-COR).
Deduced amino acid sequences were aligned manually by pooling the amino
acids into six groups (9) with the GDE 2.2 sequence editor
(33a). Nucleic acid sequences of the gene fragments were
then aligned according to the amino acid alignment.
Protein phylogeny.
To construct phylogenetic trees based on
the amino acid alignments, we prepared three data sets: one contained
the DSR Nucleotide phylogeny.
All nucleotide-level analyses were
based on first and second codon positions of alignments that
corresponded to the amino acid alignments described above for the
DSR sequences. Bootstrap analysis.
Bootstrap analysis for protein distance
methods utilized programs in the PHYLIP package. Bootstrap estimates
for the protein maximum-likelihood trees utilized the resampling
estimated-log likelihood method implemented in the PROTML 2.2 program.
All other bootstrapping was performed with the PAUP* program. For
protein distance, protein parsimony, nucleotide distance, and
nucleotide parsimony analyses, 500 bootstrap resamplings were analyzed.
Due to time constraints, nucleotide maximum-likelihood bootstrap
analysis was based on 250 resamplings.
Nucleotide sequence accession number.
The sequences for the
DSR We first evaluated four primers, designed on the basis of sequence
conservation between the DSR genes of A. fulgidus and
Desulfovibrio vulgaris, in different
combinations for PCR amplification of genomic DNA from a wide variety
of reference organisms (Table 1). One primer pair (DSR1F-DSR4R) amplified the expected ~1.9-kb fragment from all 22 sulfate-reducing bacteria tested. No amplification could be
observed with DNA from bacterial and archaeal species that do not
derive energy from sulfate reduction (Fig.
1), demonstrating that this primer pair
does not amplify (i) genes encoding assimilatory sulfite reductase,
(ii) genes encoding the sulfite reductase from an organism having the
capacity to respire sulfite but not sulfate (Shewanella
putrefaciens), or (iii) the genes for the reverse sulfite
reductases, which show some similarity to DSR with respect to catalytic
parameters and subunit composition (31, 32). This is also
consistent with recent sequence analysis of this enzyme (siroheme
sulfite reductase) from the sulfur-oxidizing phototrophic bacterium,
Chromatium vinosum (16). Comparative analysis
revealed that the evolutionary distance between the enzymes from
Chromatium vinosum and Desulfovibrio
vulgaris is greater than that separating the enzymes from A. fulgidus and Desulfovibrio vulgaris.
Although these data suggest a yet-earlier divergence between oxidative
and reductive modes of dissimilatory sulfur metabolism, in the absence
of additional sequences for the oxidative type of DSR, we do not
consider it further.
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Phylogeny of Dissimilatory Sulfite Reductases
Supports an Early Origin of Sulfate Respiration
ABSTRACT
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Abstract
Introduction
Materials & Methods
Results & Discussion
References
and 
subunits of
DSR could be recovered only from organisms capable of
dissimilatory sulfate reduction with a PCR primer set targeting highly
conserved regions in these genes. All DNA sequences obtained were
highly similar to one another (49 to 89% identity), and their inferred
evolutionary relationships were nearly identical to those inferred on
the basis of 16S rRNA. We conclude that the high similarity of
bacterial and archaeal DSRs reflects their common origin from a
conserved DSR. This ancestral DSR was either present before the split
between the domains Bacteria, Archaea, and
Eucarya or laterally transferred between
Bacteria and Archaea soon after domain
divergence. Thus, if the physiological role of the DSR was
constant over time, then early ancestors of Bacteria and
Archaea already possessed a key enzyme of sulfate and
sulfite respiration.
INTRODUCTION
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Abstract
Introduction
Materials & Methods
Results & Discussion
References
22 structure or an 22
2 structure
(3, 8, 27) and possess iron-sulfur clusters and siroheme
prosthetic groups. Gene sequences were previously determined for
the DSR genes of A. fulgidus and Desulfovibrio vulgaris (8, 20) and were used to assign them to a
redox enzyme superfamily characterized by a repeat structure common to
sulfite and nitrite reductases (7). This superfamily also encompasses gene sequences of assimilatory nitrite and sulfite reductases from higher plants, fungi, algae, and bacteria (used biosynthetically) and the small, monomeric sulfite reductase from Desulfovibrio vulgaris (35). The physiological
role of the monomeric reductase is unresolved, but the
Desulfovibrio vulgaris enzyme resembles spectroscopically
the low-molecular-weight sulfite reductases isolated from
Methanosarcina barkeri and Desulfuromonas
acetoxidans (24).
and subunits for
representative sulfate reducers. Both were consistent with similar
analysis of the 16S rRNA genes from these organisms, suggesting a
single ancestral progenitor.
MATERIALS AND METHODS
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Abstract
Introduction
Materials & Methods
Results & Discussion
References
subunits. The blots were hybridized with the probe
at 60°C overnight and washed at 65°C at intermediate stringency
following the Boehringer Mannheim protocol. The digoxigenin-labeled
probe and molecular weight markers were detected colorimetrically with
the nitroblue tetrazolium salt and 5-bromo-chloro-3-indolylphosphate
system (Boehringer Mannheim) according to the manufacturer's
instructions.
-subunit sequences, a second contained -subunit
sequences, and a third contained a concatenated - and -subunit
data set. For distance and parsimony analysis, gaps and missing
sequence information were coded as missing data, yielding 186, 191, and
377 positions for -subunit, -subunit, and - and -subunit
data sets, respectively. For protein maximum-likelihood methods, all
positions where two or more sequences had missing data were deleted,
while at those positions where only a single sequence was missing
information, missing data were coded as a 21st amino acid. Final data
sets consisted of 180, 184, and 363 positions for -subunit,
-subunit, and - and -subunit data sets, respectively. Protein
distances were inferred by using a maximum-likelihood method
implemented in the PROTDIST program, with the Dayhoff PAM 001 matrix as
the amino acid replacement model. Trees were inferred from the
distances by using FITCH with global rearrangements (11).
Unweighted amino acid parsimony analysis was completed with test
versions 4.0.0d59 and 4.0.0d60 of the PAUP* program written by
D. L. Swofford. Maximum-parsimony trees were determined by the
branch-and-bound algorithm. Protein maximum-likelihood trees were
calculated in two ways. Exhaustive searches were performed by using the
PROTML 2.2 (2) program with the JTT-f amino acid replacement
model to select the tree which conferred the greatest likelihood on the
data. To account for rate heterogeneity among sites, protein
maximum-likelihood trees were also estimated with the PUZZLE 3.1 program employing the JTT-f model with a mixed eight-category discrete
gamma-plus-invariant-site model with default parameter estimation
methods (34).
-Subunit, -subunit, and - and -subunit data
sets consisted of 384, 466, and 850 aligned positions, respectively. A
total of 1,041 aligned positions were utilized for the 16S rRNA data
set. In all cases, missing data or alignment gaps were treated as
missing information. The PAUP* program (and references therein) was
used to perform nucleotide parsimony, distance, and maximum-likelihood
analysis. Distance matrices were estimated by the maximum-likelihood
method with the Hasegawa-Kishino and Yano (HKY) model with a discrete gamma-invariant-site model with trees selected under the minimum evolution criterion. The transition/transversion ratio and rate heterogeneity parameters were estimated via maximum likelihood on an
HKY maximum-likelihood-distance-minimum-evolution topology. Maximum-likelihood analysis was performed with the same model. Heuristic tree-searching procedures for distance and maximum-likelihood methods involved simple stepwise addition with tree bisection reconnection rearrangements. Unweighted parsimony analysis was performed as described above.
and subunits have been deposited in GenBank (accession no.
U58114 to U58129).
RESULTS AND DISCUSSION
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Abstract
Introduction
Materials & Methods
Results & Discussion
References
TABLE 1.
PCR amplification of genomic DNA from
reference organisms
View larger version (59K):
[in a new window]
FIG. 1.
PCR specificity determinations using the DSR primer pair
DSR1F-DSR4R with genomic DNA from Desulfovibrio
vulgaris ATCC 29579 (lane 2), Desulfomicrobium
baculatus DSM 1743 (lane 3), Desulfotomaculum ruminis
ATCC 23193 (lane 4), Thermodesulfovibrio yellowstonii
(provided by R. Devereux) (lane 5), E. coli (provided by the
University of Illinois [UI]) (lane 6), Shewanella
putrefaciens ATCC 8071 (lane 7), Nitrosomonas sp.
strain C56 (provided by J. Waterbury) (lane 8), Thiobacillus
denitrificans ATCC 25259 (lane 9), Arthrobacter
globiformis ATCC 8010 (lane 10), Beggiatoa sp. strain
MS 81-1-C (provided by D. Nelson) (lane 11), Chromatium
vinosum ATCC 17899 (lane 12), and Methanosarcina
acetivorans (UI) (lane 13) Lanes 1 and 14 contain molecular weight
markers. (A). In addition, genomic DNA obtained from the following
bacteria was used for further specificity evaluation of the DSR primer
set (data not shown): Fe reducer TT4B (provided by L. Krumholtz),
Nitrospira briensis C128 (provided by Waterbury),
Nitrobacter hamburgensis 14X (provided by J. Waterbury),
Nitrosovibrio tenuis C141 (provided by J. Waterbury),
Oxalobacter formigenes ATCC 35274, Zoogloea
ramigera ATCC 19623, Fibrobacter succinogenes ATCC
19169, Bacillus subtilis ATCC 6051, a
Streptomyces sp. (UI), Streptococcus pyogenes
ATCC 12344, Pseudomonas aeruginosa (UI),
Beggiatoa sp. strain OH-75-2a (provided by D. Nelson), and
Methanobacterium thermoautotrophicum (UI). A fragment of the
expected length was exclusively obtained with DNA from the sulfate
reducers (Desulfovibrio vulgaris,
Desulfovibrio baculatus, Desulfotomaculum
ruminis, and Thermodesulfovibrio yellowstonii).
Sufficient quality of each genomic DNA for successful PCR amplification
was demonstrated in control reactions with conserved 16S rDNA-targeted
primers (data not shown). The identity of the amplified products was
confirmed by Southern hybridization with a DNA probe targeting a
conserved region in the subunit of DSR (B).
We sequenced the 1.9-kb amplification products from Desulfobotulus sapovorans, Desulfonema limicola, Desulfococcus multivorans, Desulfobacter latus, Desulfovibrio sp. strain PT-2, Desulfovibrio sp. strain PIB2, Desulfotomaculum ruminis, and Thermodesulfovibrio yellowstonii. However, the product from Thermodesulfobacterium commune was not stable in E. coli and sequence information is not yet available for this organism. We are evaluating alternative cloning strategies and hope to include this sequence in future analyses. All sequences showed high similarity to each other and to those previously determined for Desulfovibrio vulgaris and A. fulgidus (Tables 2 and 3), and much less similarity to other members of the siroheme-containing redox enzyme superfamily (7). With the exception of reverse sulfite reductase from Chromatium vinosum, no extensive alignment was possible.
|
|
Phylogenetic trees for the DSR and subunits and combined and subunits were estimated from the amino acid and nucleotide data
sets by distance, parsimony, and maximum-likelihood methods (Fig.
2). Trees were also inferred from a
16S rRNA data set containing a wider array of Bacteria and
Archaea (Fig. 3). Overall,
highly similar orderings of taxa were found between 16S rRNA and DSR trees.
|
2046.54) (A),
|
The archaeon A. fulgidus branches closest to
Thermodesulfovibrio yellowstonii and Desulfotomaculum
ruminis in -subunit, -subunit, and - and -subunit DSR
data sets (Fig. 2). However, which of these two bacteria is closest to
A. fulgidus depends on both the DSR subunit and the
phylogenetic methods. -Subunit and - and -subunit amino
acid-based analyses recover a Desulfotomaculum ruminis-A.
fulgidus clade in the majority of bootstrap replicates, whereas
nucleotide-level analyses of these data sets and both nucleotide and
amino acid analyses of the -subunit data set support a T. yellowstonii-A. fulgidus grouping. Trees inferred from the 16S
rRNA data set also show the Archaea (represented by A. fulgidus and Methanococcus jannaschii) joining the
bacterial subtree close to these two taxa with
Thermodesulfobacterium commune usually forming the deepest
bacterial branch (26). Distance and maximum-likelihood methods are congruent in finding Thermodesulfovibrio
yellowstonii the next taxon to diverge. Bootstrap support for the
clustering of Thermodesulfovibrio yellowstonii,
Thermodesulfobacterium commune, and A. fulgidus is strong only for distance methods (Fig. 3). Furthermore, the clustering of Desulfotomaculum ruminis
with these taxa is only moderately supported by parsimony and
likelihood methods. Similar results were obtained with a taxonomically
reduced 16S rRNA data set that included only those taxa used in the DSR analyses (data not shown).
For all methods with both DNA and amino acid data sets of all the DSR
data sets, the 
-subclass of the Proteobacteria
(-Proteobacteria) forms a clade that receives highly
significant bootstrap support (all bootstrap values were >97%). The
monophyly of the -Proteobacteria receives much poorer
support from 16S rRNA analysis. This is largely due to a weak tendency
for Desulfotomaculum ruminis to cluster with the
Desulfovibrio group.
Although the branching order within the -Proteobacteria
is very similar between DSR and 16S rRNA data sets, where taxa overlap, a few minor differences are apparent. First,
Desulfovibrio vulgaris and
Desulfovibrio sp. strain PT2 strongly form a
grouping to the exclusion of all other sequences in the 16S rRNA tree
(bootstrap values were 
99% for all three phylogenetic methods).
These two also form a grouping for -subunit and - and -subunit
data sets but do not form a clade in optimal protein maximum-likelihood or nucleotide maximum-likelihood trees of the -subunit data set. However, for this data set, protein distance and nucleotide distance methods do recover the Desulfovibrio
vulgaris-Desulfovibrio sp. strain PT2 grouping
with 87 and 55% bootstrap support, respectively (data not
shown). Several factors are probably responsible for the failure
of the likelihood methods to recover this relationship. First, since
the -subunit data set contains relatively few aligned positions,
inferences based on this data set will be subject to large random
error. Furthermore, the relatively short branches leading to the
Desulfovibrio vulgaris and
Desulfovibrio sp. strain PT2 sequences in the
-subunit trees compared to the -subunit tree (Fig. 2) suggest
that the subunit of these two organisms may have diverged so little
from the common ancestral sequence of the -Proteobacteria
that the branch joining them is extremely short and cannot be resolved
with the number of data available. Inclusion of more sequences in
phylogenetic analysis often increases the efficiency of the methods for
finding the correct topology (15). Consistent with this, our
preliminary analyses of larger DSR data sets containing more
-Proteobacteria with each of the phylogenetic methods
recover a relationship between Desulfovibrio vulgaris and Desulfovibrio sp. strain PT2
in trees of -subunit, -subunit, and - and -subunit amino
acid and nucleotide data sets. Furthermore, analyses of data sets
including a partial -subunit and complete -subunit DSR sequence
from Desulfovibrio gigas reveals that the
latter organism is an immediate sister to a strongly supported Desulfovibrio
vulgaris-Desulfovibrio sp. strain PT2 clade.
A second anomaly is the positioning of Desulfovibrio
oxyclinae. In 16S rRNA trees, Desulfovibrio
oxyclinae robustly groups with Desulfovibrio
africanus, with these two taxa appearing as sisters to a
Desulfovibrio vulgaris-Desulfovibrio
sp. strain PT2 clade (Fig. 3). However, all of the DSR data sets show
it as a separate branch most closely related to the Desulfobacter
latus-Desulfococcus multivorans-Desulfonema limicola-Desulfobotulus
sapovorans clade, with moderate bootstrap support. Once again,
however, inclusion of further -Proteobacteria DSR
sequences (36a) suggests that this conflict may be an
artifact of limited taxonomic representation. When
phylogenetically broader data sets are considered, the bootstrap support for the Desulfobacter latus-Desulfococcus
multivorans-Desulfonema limicola-Desulfobotulus
sapovorans-Desulfovibrio oxyclinae clade decreases, indicating that the branching order among these
groups is poorly resolved.
A final point of conflict between 16S rRNA and - and -subunit
DSR topologies is the relative branching order of
Desulfotobacter latus and Desulfotobotulus
sapovorans. In this case, the branches in question in the
DSR trees do not receive strong bootstrap support, and conflicts
between phylogenetic methods are apparent (Fig. 2), indicating once
again that the branching order among these taxa is not well resolved.
Topology aside, there are several notable differences in branch
lengths between the DSR and 16S rRNA trees. For instance, in the 16S
rRNA tree, a long branch connects the Archaea,
A. fulgidus and Methanococcus jannaschii, to the
Bacteria (Fig. 3). In contrast, archaeal and bacterial DSR
sequences are not particularly distant; for -subunit,
-subunit, and - and -subunit data sets, the branch
leading to A. fulgidus is approximately the
same length as branches leading to Desulfotomaculum ruminis
and Thermodesulfovibrio yellowstonii. In contrast, the
branch connecting the -Proteobacteria to the rest of the
tree is relatively long in the DSR data set and quite short for 16S
rRNA.
There are several explanations for these differences in branch
length. First, it is possible that both sets of genes are tracing the same evolutionary history but have suffered periodic increases and/or decreases in their rate of substitution at different times. For
instance, a periodic increase in the rate of substitution in the 16S
rRNA gene may have occurred along the branch between Archaea
and Bacteria, leading to the long branch length observed relative to that in DSR trees. Similarly, an increase in substitution rate in both subunits of DSR may have occurred on the branch connecting -Proteobacteria to all other taxa. However, it is also
possible that the disparity in branch lengths may betray different
evolutionary histories for the 16S rRNA and DSR data sets. For
instance, the high degree of similarity between A. fulgidus
DSR and homologs from Desulfotomaculum ruminis and
Thermodesulfovibrio yellowstonii could indicate that the
former organism acquired its DSR genes from one of the latter
lineages by lateral gene transfer. Lateral transfer between
gram-positive eubacteria and Archaea is not without precedent; for instance, the hsp70 and glutamine synthetase genes of
Archaea may have been acquired by lateral transfer from
gram-positive eubacteria (5, 29). Moreover, lateral transfer
would explain why sulfate respiration is not widespread among known
Archaea but is instead phylogenetically restricted to
A. fulgidus and close relatives (37). The
resolution of these alternatives will depend upon the availability of
additional DSR sequences. In this regard, we note the recent
publication of - and -subunit DSR sequences of the sulfite
reductase of the crenarchaeote Pyrobaculum islandicum
(23). Preliminary phylogenetic analyses by us show these
sequences to be highly divergent but to share a most recent common
ancestor with the Archaeoglobus sequences, suggesting that the Archaea are monophyletic in DSR trees. However, P. islandicum lacks the capacity for sulfate respiration, and its DSR
may be under different functional constraints. Molitor and associates have suggested that the protein from P. islandicum and the
sulfite reductases from sulfate reducers and from sulfur oxidizers
represent three independent lineages that originated prior to the
divergence of Archaea and Bacteria
(23).
However, in the absence of additional data, the near congruence of 16S rRNA and DSR for sulfate-reducing Bacteria and Archaea suggests that the gene histories of the DSR subunits represent the phylogeny of the organisms. Because members of the domain Archaea are considered to be more related to Eucarya than to Bacteria (10, 18, 38), one plausible implication is that DSR was already present in the progenitor of the three recognized domains of life. Although we cannot exclude the possibility that ancestral DSR evolved within either Bacteria or Archaea soon after the split of the domains and was then transferred to the other domain by an early lateral gene transfer event, the capacity for sulfate or sulfite respiration appears to have a very early origin in either case.
This conclusion is justified only if these genes are orthologous and retain their ancestral physiological role. There are at least two supporting lines of evidence that the progenitor genes coded for an enzyme similar in function to the modern DSR. First, in contrast to assimilatory sulfite and nitrite reductases, both subunits of all sequenced DSRs contain a conserved ferredoxin-like domain. The identical position of this domain in the DSRs of Bacteria and Archaea indicates that this unique feature of DSRs was present before the divergence of the two domains (8). Second, as life may have originated in hot environments (1, 19, 38), the occurrences of sulfate-reducing prokaryotes among hyperthermophilic Archaea (Archaeoglobus profundus and A. fulgidus) and deep-branching thermophilic bacteria (Thermodesulfovibrio yellowstonii and Thermodesulfobacterium commune) are consistent with an early origin. Third, isotopic data suggest that dissimilatory sulfate reduction began 2.8 to 3.1 billion years ago (28, 33) but acquired global significance only after sulfate concentrations had significantly increased in the Precambrian oceans approximately 2.35 billion years ago (6). The isotopic data are reasonably consistent with a recent estimate of the time of domain divergence, ca. 3.1 to 3.6 billion years ago, based on sequence comparisons of a large number of different proteins (12). Since our data indicate that the progenitor genes of DSR evolved before or soon after the divergence of the three domains, organisms able to reduce sulfate, or at least sulfite, may have given rise to all known forms of bacterial and archaeal life. This view is consistent with recent speculations that respiratory electron transport systems evolved prior to oxygenic photosynthesis (30).
If our inference is correct, it is difficult to understand why the capacity for this lifestyle has such restricted phylogenetic distribution among Bacteria and Archaea. Dissimilatory sulfate reduction is found in only three primary bacterial lineages and is restricted to a single archaeal genus, Archaeoglobus. One possible explanation for the apparently limited phylogenetic distribution of sulfate-reducing microorganisms is that most bacterial and archaeal lineages have lost the appropriate genes during evolution. On the other hand, we might simply have failed to isolate representatives of the natural diversity of sulfate-reducing prokaryotes. We have started to systematically evaluate the second possibility by using the PCR primers described in this study to amplify DSR genes directly from total DNA isolated from a variety of habitats (sulfidogenic aquifers, gastrointestinal sites, microbial mats, lake sediments, and biofilm reactors). Our initial phylogenetic analyses of "environmental" DSR sequences have revealed novel sequences that are distinct from described sulfate-reducing assemblages (36a). This suggests great undescribed natural diversity of sulfate-reducing prokaryotes and is also consistent with the early origin of this possibly archtypical phenotype.
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ACKNOWLEDGMENTS |
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We thank F. Widdel, M. Fukui, D. Nelson, M. J. McInerney, R. Devereux, L. Krumholtz, J. Waterbury, and Y. Cohen for providing us with bacterial strains. Valuable discussions with W. Ludwig are gratefully acknowledged. We also thank M. Ragan, K.-H. Schleifer, O. Kandler, and N. Ramsing for critical reading of the manuscript. We are grateful to Mitch Sogin for allowing phylogenetic analyses to be performed in his laboratory. We thank David Swofford for allowing us to perform analyses with the test versions 4.0.0d59 and 4.0.0d60 of the PAUP* program and to publish the results.
M.W. was supported by a postdoctoral grant from the Deutsche Forschungsgemeinschaft (Wa 1027/1-1), and D.A.S. was supported by grants from the ONR and NSF. A.J.R. was supported by the Natural Sciences and Engineering Research Council of Canada.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Civil Engineering, Technological Institute, Northwestern University, 2145 Sheridan Rd., Evanston, IL 60208-3109. Phone: (847) 491-4997. Fax: (847) 491-4011. E-mail: d-stahl{at}nwu.edu.
Present address: Technische Universität München,
Lehrstuhl für Mikrobiologie, D-80290 Munich, Germany.
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REFERENCES |
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Abstract
Introduction
Materials & Methods
Results & Discussion
References
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| 1. | Achenbach-Richter, L., R. Gupta, K. O. Stetter, and C. R. Woese. 1987. Were the original eubacteria thermophiles? Syst. Appl. Microbiol. 9:34-39[Medline]. |
| 2. | Adachi, J., and M. Hasegawa. 1996. In Computer science monographs, no. 28. MOLPHY version 2.3: programs for molecular phylogenetics based on maximum likelihood. Institute of Statistics and Mathematics, Tokyo, Japan. |
| 3. | Arendsen, A. F., M. F. J. M. Verhagen, R. B. G. Wolbert, A. J. Pierik, A. J. M. Stams, M. S. M. Jetten, and W. R. Hagen. 1993. The dissimilatory sulfite reductase from Desulfosarcina variabilis is a desulforubidin containing uncoupled metalated sirohemes and S=9/2 iron-sulfur clusters. Biochemistry 32:10323-10330[Medline]. |
| 3a. | Boehringer Mannheim Corporation. 1994. In Genius system user's guide for membrane hybridization, version 3.0. Boehringer Mannheim Corporation, Indianapolis, Ind. |
| 4. |
Boom, R.,
C. J. A. Sol,
M. M. M. Salimans,
C. L. Jansen,
P. M. E. Wertheim-van Dillen, and J. van der Noordaa.
1990.
Rapid and simple method for purification of nucleic acids.
J. Clin. Microbiol.
28:495-503 |
| 5. | Brown, J. R., and W. F. Doolittle. 1997. Archaea and the prokaryote-to-eukaryote transition. Microbiol. Mol. Biol. Rev. 61:456-502. [Abstract] |
| 6. | Cameron, E. M. 1982. Sulphate and sulphate reduction in early Precambrian oceans. Nature 296:145-148. |
| 7. |
Crane, B. R.,
L. M. Siegel, and E. D. Getzoff.
1995.
Sulfite reductase structure at 1.6 Å: evolution and catalysis for reduction of inorganic anions.
Science
270:59-67 |
| 8. |
Dahl, C.,
N. M. Kredich,
R. Deutzmann, and H. G. Trüper.
1993.
Dissimilatory sulphite reductase from Archaeoglobus fulgidus: physicochemical properties of the enzyme and cloning, sequencing and analysis of the reductase genes.
J. Gen. Microbiol.
139:1817-1828 |
| 9. | Dayhoff, M. O., R. M. Schwartz, and B. C. Orcutt. 1978. A model of evolutionary change in proteins, p. 345-352. In M. O. Dayhoff (ed.), Atlas of protein sequence and structure. National Biomedical Research Foundation, Silver Spring, Md. |
| 10. | Doolittle, R. F., D.-F. Feng, S. Tsang, G. Cho, and E. Little. 1996. Determining divergence times of the major kingdoms of living organisms with a protein clock. Science 271:470-477[Abstract]. |
| 11. | Felsenstein, J. 1993. In PHYLIP (Phylogeny Inference Package), version 3.57c. Department of Genetics, University of Washington, Seattle. |
| 12. |
Feng, D.-F.,
G. Cho, and R. F. Doolittle.
1997.
Determining divergence times with a protein clock: update and re-evaluation.
Proc. Natl. Acad. Sci. USA
94:13028-13033 |
| 13. | Harrison, G., C. Curle, and E. J. Laishley. 1984. Purification and characterization of an inducible dissimilatory type sulfite reductase from Clostridium pasteurianum. Arch. Microbiol. 138:72-78[Medline]. |
| 14. |
Hatchikian, E. C., and J. G. Zeikus.
1983.
Characterization of a new type of dissimilatory sulfite reductase present in Thermodesulfobacterium commune.
J. Bacteriol.
153:1211-1220 |
| 15. | Hillis, D. M. 1996. Inferring complex phylogenies. Nature 383:130-131[Medline]. |
| 16. |
Hipp, W. M.,
A. S. Pott,
N. Thum-Schmitz,
I. Faath,
C. Dahl, and H. G. Trüper.
1997.
Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokaryotes.
Microbiology (Reading)
143:2891-2902.
|
| 17. |
Huang, C. J., and E. L. Barrett.
1991.
Sequence analysis and expression of the Salmonella typhimurium asr operon encoding production of hydrogen sulfide from sulfite.
J. Bacteriol.
173:1544-1553 |
| 18. |
Iwabe, N.,
K. Kuma,
M. Hasegawa,
S. Osawa, and T. Miyata.
1989.
Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes.
Proc. Natl. Acad. Sci. USA
86:9355-9359 |
| 19. | Kandler, O. 1993. The early diversification of life. Nobel Symp. 84:152-160. |
| 20. | Karkhoff-Schweizer, R. R., D. P. W. Huber, and G. Voordouw. 1995. Conservation of the genes for dissimilatory sulfite reductase from Desulfovibrio vulgaris and Archaeoglobus fulgidus allows their detection by PCR. Appl. Environ. Microbiol. 61:290-296[Abstract]. |
| 21. | Lee, J.-P., and H. D. Peck, Jr. 1971. Purification of the enzyme reducing bisulfite to trithionate from Desulfovibrio gigas and its identification as desulfoviridin. Biochem. Biophys. Res. Commun. 45:583-589[Medline]. |
| 22. |
Lee, J.-P.,
C.-S. Yi,
J. LeGall, and H. D. Peck, Jr.
1973.
Isolation of a new pigment, desulforubidin, from Desulfovibrio desulfuricans (Norway strain) and its role in sulfite reduction.
J. Bacteriol.
115:453-455 |
| 23. |
Molitor, M.,
C. Dahl,
I. Faath,
U. Schaefer,
N. Speich,
R. Huber,
R. Deutzmann, and H. G. Trueper.
1998.
A dissimilatory sirohaem-sulfite-reductase-type protein from the hyperthermophilic archaeon Pyrobaculum islandicum.
Microbiology (Reading)
144:529-541.
|
| 24. | Moura, I., A. R. Lino, J. J. G. Moura, A. V. Xavier, G. Fauque, H. D. Peck, Jr., and J. LeGall. 1986. Low-spin sulfite-reductases: a new homologous group of non-heme iron-siroheme proteins in anaerobic bacteria. Biochem. Biophys. Res. Commun. 141:1032-1041[Medline]. |
| 25. | Odom, J. M., and H. D. Peck, Jr. 1984. Hydrogenase, electron transfer proteins, and energy coupling in the sulfate-reducing bacteria Desulfovibrio. Annu. Rev. Microbiol. 38:551-592[Medline]. |
| 26. |
Olsen, G. J.,
C. R. Woese, and R. Overbeek.
1994.
The winds of (evolutionary) change: breathing new life into microbiology.
J. Bacteriol.
176:1-6 |
| 27. | Pierik, A. J., M. G. Duyvis, J. M. L. M. van Helvoort, R. B. G. Wolbert, and W. R. Hagen. 1992. The third subunit of desulfoviridin-type dissimilatory sulfite reductases. Eur. J. Biochem. 205:111-115[Medline]. |
| 28. | Postgate, J. R. 1984. In The sulphate-reducing bacteria, 2nd ed. Cambridge University Press, Cambridge, United Kingdom. |
| 29. | Roger, A. J., and J. R. Brown. 1996. A chimeric origin for eukaryotes re-examined. Trends Biochem. Sci. 21:370-371[Medline]. |
| 30. | Schäfer, G., W. Purschke, and C. L. Schmidt. 1996. On the origin of respiration: electron transport proteins from archaea to man. FEMS Microbiol. Rev. 18:173-188[Medline]. |
| 31. | Schedel, M., J. LeGall, and J. Baldensperger. 1975. Sulfur metabolism in Thiobacillus denitrificans. Arch. Microbiol. 105:339-341[Medline]. |
| 32. | Schedel, M., M. Vanselow, and H. G. Trüper. 1979. Siroheme-sulfite reductase isolated from Chromatium vinosum. Purification and investigation of some of its molecular and catalytic properties. Arch. Microbiol. 121:29-36. |
| 33. | Schidlowski, M., J. M. Hayes, and I. R. Kaplan. 1983. Isotopic inferences of ancient biochemistries: carbon, sulfur, hydrogen, and nitrogen, p. 149-186. In J. W. Schopf (ed.), Earth's earliest biosphere, its origin and evolution. Princeton University Press, Princeton, N.J. |
| 33a. | Smith, S., R. Overbeek, C. R. Woese, W. Gilbert, and P. Gillevet. The genetic data environment: an expandable GUI for multiple sequence analysis. CABIOS 10:671-675. |
| 34. | Strimmer, K., and A. von Haeseler. 1996. Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13:964-969. |
| 35. | Tan, J., L. R. Helms, R. P. Swenson, and J. A. Cowan. 1991. Primary structure of the assimilatory-type sulfite reductase from Desulfovibrio vulgaris (Hildenborough): cloning and nucleotide sequence of the reductase gene. Biochemistry 30:9900-9907[Medline]. |
| 36. |
Trudinger, P. A.
1970.
Carbon monoxide-reacting pigment from Desulfotomaculum nigrificans and its possible relevance to sulfite reduction.
J. Bacteriol.
104:158-170 |
| 36a. | Wagner, M., and D. A. Stahl. Unpublished data. |
| 37. | Widdel, F., and T. A. Hansen. 1992. The dissimilatory sulfate- and sulfur-reducing bacteria, p. 583-624. In A. Balows, et al. (ed.), The prokaryotes, 2nd ed. Springer-Verlag, New York, N.Y. |
| 38. |
Woese, C. R.
1987.
Bacterial evolution.
Microbiol. Rev.
51:221-271 |
J Bacteriol, June 1998, p. 2975-2982, Vol. 180, No. 11
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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[Abstract] [Full Text] -
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67: 1494-1502
[Abstract] [Full Text] -
Thomsen, T. R., Finster, K., Ramsing, N. B.
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67: 1646-1656
[Abstract] [Full Text] -
Laue, H., Friedrich, M., Ruff, J., Cook, A. M.
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183: 1727-1733
[Abstract] [Full Text] -
Detmers, J., Brüchert, V., Habicht, K. S., Kuever, J.
(2001). Diversity of Sulfur Isotope Fractionations by Sulfate-Reducing Prokaryotes. Appl. Environ. Microbiol.
67: 888-894
[Abstract] [Full Text] -
Davey, M. E., O'toole, G. A.
(2000). Microbial Biofilms: from Ecology to Molecular Genetics. Microbiol. Mol. Biol. Rev.
64: 847-867
[Abstract] [Full Text] -
Schramm, A., Santegoeds, C. M., Nielsen, H. K., Ploug, H., Wagner, M., Pribyl, M., Wanner, J., Amann, R., de Beer, D.
(1999). On the Occurrence of Anoxic Microniches, Denitrification, and Sulfate Reduction in Aerated Activated Sludge. Appl. Environ. Microbiol.
65: 4189-4196
[Abstract] [Full Text] -
Cottrell, M. T., Cary, S. C.
(1999). Diversity of Dissimilatory Bisulfite Reductase Genes of Bacteria Associated with the Deep-Sea Hydrothermal Vent Polychaete Annelid Alvinella pompejana. Appl. Environ. Microbiol.
65: 1127-1132
[Abstract] [Full Text] -
Fritz, G., Roth, A., Schiffer, A., Buchert, T., Bourenkov, G., Bartunik, H. D., Huber, H., Stetter, K. O., Kroneck, P. M. H., Ermler, U.
(2002). Structure of adenylylsulfate reductase from the hyperthermophilic Archaeoglobus fulgidus at 1.6-A resolution. Proc. Natl. Acad. Sci. USA
99: 1836-1841
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