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Journal of Bacteriology, October 2001, p. 6028-6035, Vol. 183, No. 20
Lehrstuhl für Mikrobiologie, Technische
Universität München, D-85350
Freising,1 and Department of
Biogeochemistry, Max Planck Institute for Terrestrial Microbiology,
D-35043-Marburg,2 Germany; Department of
Biochemistry and Molecular Biology, Dalhousie University, Halifax,
Nova Scotia B3H 4H7, Canada3; Advanced
Wastewater Management Centre, Department of Microbiology and
Parasitology, The University of Queensland, Brisbane 4072, Queensland, Australia4; Department of
Civil Engineering, Northwestern University, Evanston, Illinois
60208-31095; and Department of Civil and
Environmental Engineering, University of Washington, Seattle,
Washington 98195-27006
Received 26 February 2001/Accepted 3 July 2001
A large fragment of the dissimilatory sulfite reductase genes
(dsrAB) was PCR amplified and fully sequenced from 30 reference strains representing all recognized lineages of
sulfate-reducing bacteria. In addition, the sequence of the
dsrAB gene homologs of the sulfite reducer
Desulfitobacterium dehalogenans was determined. In
contrast to previous reports, comparative analysis of all available DsrAB sequences produced a tree topology partially inconsistent with
the corresponding 16S rRNA phylogeny. For example, the DsrAB sequences
of several Desulfotomaculum species (low G+C
gram-positive division) and two members of the genus
Thermodesulfobacterium (a separate bacterial
division) were monophyletic with Siroheme dissimilatory sulfite
reductases (EC 1.8.99.3) catalyze the reduction of sulfite to sulfide,
an essential step in the anaerobic sulfate-respiration pathway.
Consequently, this enzyme has been found in all dissimilatory
sulfate-reducing prokaryotes (SRPs) investigated so far. Furthermore,
siroheme dissimilatory sulfite reductase-like enzymes have been
detected in the hyperthermophilic archaeon Pyrobaculum
islandicum capable of using sulfite as terminal electron acceptor
(23), the phototrophic bacterium Allochromatium vinosum (10, 12), and the obligate chemolithotrophic
species Thiobacillus denitrificans (32). In the
latter two organisms the dissimilatory sulfite reductase has a proposed
function in sulfide oxidation.
Siroheme sulfite reductases consist of at least two different
polypeptides in an In the present study we investigated this question further by
phylogenetic analysis of the dsrAB genes from a wide range
of cultivated SRPs. We found a clear case for multiple lateral transfer events of the dsrAB genes between major lineages of
Bacteria and likely between the domains Bacteria
and Archaea, suggesting that genes involved in primary
metabolic functions, such as sulfate respiration, may be more prone to
lateral transfer than previously thought.
Bacterial strains.
The investigated reference
strains of sulfate- and sulfite-reducing bacteria are listed in Table
1. If necessary, strains were cultured as
recommended by the DSMZ type culture collection (Braunschweig,
Germany).
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.20.6028-6035.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Multiple Lateral Transfers of Dissimilatory Sulfite Reductase
Genes between Major Lineages of Sulfate-Reducing Prokaryotes
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
-proteobacterial DsrAB sequences.
The most parsimonious interpretation of these data is that
dsrAB genes from ancestors of as-yet-unrecognized sulfate reducers within the -Proteobacteria were
laterally transferred across divisions. A number of insertions and
deletions in the DsrAB alignment independently support these inferred
lateral acquisitions of dsrAB genes. Evidence for a
dsrAB lateral gene transfer event also was found within
the -Proteobacteria, affecting Desulfobacula toluolica. The root of the dsr tree was inferred
to be within the Thermodesulfovibrio lineage by
paralogous rooting of the alpha and beta subunits. This rooting
suggests that the dsrAB genes in
Archaeoglobus species also are the result of an ancient
lateral transfer from a bacterial donor. Although these findings
complicate the use of dsrAB genes to infer phylogenetic
relationships among sulfate reducers in molecular diversity studies,
they establish a framework to resolve the origins and diversification
of this ancient respiratory lifestyle among organisms mediating a key step in the biogeochemical cycling of sulfur.
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
2
2
structure. The genes encoding the two subunits are found adjacent to
each other in the respective genomes (see, for example, references
3, 15, 17, 18, and 35) and probably arose
from duplication of an ancestral gene (3). Comparative
amino acid sequence analysis of the dissimilatory sulfite reductase
genes (dsrAB) has recently been used to investigate the
evolutionary history of anaerobic sulfate (sulfite) respiration (10, 17, 18, 35). The presence of dsrAB
homologs in at least five highly divergent prokaryotic lineages and
overall phylogenetic congruence of the dsrAB tree with the
16S rRNA gene tree suggested that the dissimilatory sulfite reductases
of extant SRPs evolved vertically from common ancestral protogenotic
genes (35). The remarkable degree of conservation of the
dsrAB genes also provided a basis for culture-independent
molecular diversity studies of natural sulfate-reducing assemblages
with the use of PCR primers broadly specific for a large fragment of
all known dsrAB genes (1, 22). However, one
contradiction between the dsrAB and 16S rRNA phylogenies was
recently recognized in that the dsrAB sequences of
Desulfotomaculum thermocisternum (17) and
Desulfotomaculum ruminis are not monophyletic
(18). This finding could indicate that, in addition to
vertical transmission, lateral gene transfer is involved in the
evolution of SRPs.
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
TABLE 1.
Physiological and biochemical properties of the sulfite-
and sulfate-reducing prokaryotes investigated in this study
DNA isolation and PCR amplification. Genomic DNA of the reference organisms investigated was obtained from logarithmically growing or lyophilized cells by either using the FastPrep FP120 bead beater and the FastDNA Kit MH (Bio-101, Inc., La Jolla, Calif.) or another direct lysis technique (24) modified as described previously (9). An approximately 1.9-kb dsrAB segment was PCR amplified as described previously (35). Since amplification of the dsrAB gene fragment was not possible for all investigated reference strains, additional degeneracies were introduced in the previously published primers DSR1F and DSR4R (DSR1Fdeg, 5'-ACSCAYTGGAARCACG-3'; DSR4Rdeg, 5'-GTGTARCAGTTDCCRCA-3'), making them fully complementary to the respective target sites of recently published dsrAB sequences (17, 18). However, it should be noted that many "non-dsrAB" amplificates of ca. 1.9 kb were obtained using the degenerated primers.
Cloning and sequencing of dsrAB gene fragments. If not mentioned otherwise dsrAB PCR products of the sulfite- and sulfate-reducing reference strains were ligated into pCR2.1-TOPO or pCR-XL-TOPO vectors (Invitrogen). Clones with approximate 1.9-kb inserts were recovered with the QIAprep spin kit (Qiagen, Hilden, Germany) and sequenced with a 4200L automated Li-Cor Long Reader DNA Sequencer (MWG, Ebersberg, Germany). dsrAB PCR products of the Desulfotomaculum species D. aeronauticum, D. putei, D. geothermicum, D. kuznetsovii, and D. thermobenzoicum were directly sequenced. In addition, dsr sequences of Desulforhabdus amnigena, Desulfobulbus sp., and Desulfitobacterium dehalogenans were determined by direct sequencing as well as sequencing of the cloned PCR product. Previously published (35) partial dsrAB sequences of Desulfotomaculum ruminis, Thermodesulfovibrio yellowstonii, Desulfobacter latus sp., Desulfobotulus sapovorans, Desulfococcus multivorans, and Desulfovibrio sp. strain PT-2 were completed by resequencing of the original clones.
16S rRNA of Thermodesulfobacterium mobile. The 16S rRNA gene sequence of Thermodesulfobacterium mobile (=T. thermophilum) was obtained as described previously (14).
Phylogeny inference. Phylogenetic analyses were performed on alignments of the 16S ribosomal DNA (rDNA) nucleotide and the inferred amino acid sequences of the dsrAB genes. Regions of ambiguous positional homology were removed from the 16S rDNA data set using the Lane mask (16) and a DsrAB amino acid alignment mask prepared in ARB (http://www.arb-home.de). A total of 1,335 nucleotides and 543 amino acid positions (alpha subunit, 327; beta subunit, 216) were used in 16S rDNA and DsrAB analyses, respectively. For paralogous rooting DsrA sequences were aligned against DsrB and trees were calculated based on 173 amino acid positions, including positions with insertions and deletions. Phylogenetic analyses were performed with PAUP* version 4.0b2a (D. L. Swofford, Sinauer Associates, Sunderland, Mass.), ARB, or PHYLIP version 3.57c (J. Felsenstein, University of Washington, Seattle). Evolutionary distance (ED) analyses were conducted on the 16S rDNA data set using the Kimura 2 parameter and general time-reversible substitution model corrections with and without rate correction. Rate heterogeneities were corrected using a gamma distribution model (the shape parameter, alpha, was estimated to be 0.52 using a parsimony-based approximation in PAUP*). ED analysis of the DsrAB data set was performed by using a Dayhoff PAM correction and neighbor joining. Maximum parsimony (MP) trees were constructed for both data sets using the default settings in PAUP*. Maximum likelihood (ML) analysis of the 16S rDNA data set was performed in the ARB package using the fastDNAml program (28). Bootstrap resampling of the ED and MP trees was performed for all analyses to provide confidence estimates for the inferred topologies. A total of 1,000 or 2,000 replicates was used in all cases, with the exception of the ED analysis of the DsrAB data set, wherein 100 replicates were calculated.
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RESULTS |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Dissimilatory sulfite reductase phylogeny.
A DNA fragment ca.
1.9 kb in size, encompassing most of the alpha and beta subunit genes
of the dissimilatory sulfite reductase, was amplified from 30 sulfite-
and sulfate-reducing bacteria (Table 1). Complete sequences of the PCR
products were obtained. Compiled sequences were entered into the
dsrAB database, translated into amino acids, and manually
aligned. Previously published partial length dsr sequences
of Desulfovibrio oxyclinae (U58116/7 [35]), Desulfovibrio simplex (U78738 [10]),
Desulfovibrio gigas (U80961), Desulfonema
limicola (U58128/9 [35]), and
Desulfobacterium autotrophicum (Y15478) were not included to
avoid resolution loss in phylogenetic analyses. Comparative sequence
analyses were performed based on each subunit and both subunits
combined. No major differences were noted between the individual and
combined subunit tree topologies regardless of the inference method
used, indicating a shared evolutionary history for the alpha and beta subunits. Consistent with these findings, the G+C contents of dsrA and dsrB were almost identical for each
organism (data not shown). Consequently, detailed phylogenetic analyses
were performed on a combined (DsrAB) data set in order to include the
maximum number of 543 comparable amino acid positions. For comparison, trees were calculated from the 16S rRNA genes of the identical set of
organisms to avoid sampling artifacts (Fig.
1).
Since the 16S rDNA sequence of Thermodesulfobacterium
mobile was not available, it was determined in this study (1,520 nucleotides). In Fig. 1, the Archaeoglobus sequences were
used as the outgroup for the 16S rRNA tree since they are the only
representatives of the archaeal domain in an otherwise bacterial tree.
In contrast, the Thermodesulfovibrio sequences (bacterial
Nitrospira division) were used as the outgroup in the DsrAB
analyses since paralogous outgrouping of the alpha and beta subunits
suggests that the root of the Dsr tree is along the
Thermodesulfovibrio line of descent (Fig.
2). Therefore, it appears likely that the
dissimilatory sulfite reductases of the Archaeoglobales have
a bacterial origin (see Discussion).
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-proteobacterium
Desulfobacula toluolica (color coded; Fig. 1). In contrast
to relationships inferred using the rRNA, the genus
Desulfotomaculum, a member of the low G+C gram-positive division (33), is not monophyletic in the DsrAB tree.
Desulfotomaculum aeronauticum, D. ruminis, and
D. putei form a clearly separated grouping, together with
Desulfosporosinus orientis, based on their DsrAB sequences,
while the other seven Desulfotomaculum species cluster
together with Desulfobacula toluolica within the
-proteobacterial radiation. Similarly, Thermodesulfobacterium
commune and T. mobile comprise a division level lineage
by rRNA analysis but branch within the -Proteobacteria
according to their DsrAB sequences. A final discrepancy recognized is
the inconsistent branching point of Desulfobacula toluolica.
By 16S rRNA comparison, this species is closely related to
Desulfobacter latus and Desulfobacter
vibrioformis, while its DsrAB sequence is robustly associated with
the Desulfotomaculum group in the
-Proteobacteria (Fig. 1). The most parsimonious interpretation is that these significant topological conflicts reflect
lateral transfer of the DsrAB genes (see Discussion). Points of
inferred lateral gene transfer (LGT) are indicated in Fig. 1 by circled
letters on the 16S rRNA tree.
Additional evidence for lateral transfer of dissimilatory sulfite
reductase.
Insertions and deletions within the DsrAB amino acid
sequences (excluded in the phylogenetic analyses) were investigated as additional signposts of the deduced evolutionary relationships, particularly with respect to inferred LGT events. In total, three insertions were unique to the -Proteobacteria: one in the
alpha subunit and two in the beta subunit (Fig.
3). These insertions were also found in
the -proteobacterium-like DsrAB sequences of the seven
Desulfotomaculum species, and two
Thermodesulfobacterium species, thus independently
supporting the suggested LGT events.
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Dissimilatory sulfite reductase homolog of Desulfitobacterium dehalogenans The conserved dsrAB primers also amplified a fragment of the expected length from Desulfitobacterium dehalogenans, a bacterium capable of sulfite reduction but not of sulfate reduction (34). Comparative sequence analysis of the amplicon demonstrated a specific relationship to the dissimilatory sulfite reductase of Desulfosporosinus orientis, a finding consistent with their 16S rRNA-based relationship (Fig. 1). Furthermore, the recently completed genome sequence of Desulfitobacterium hafniense (http://www.jgi.doe.gov) contains a dsrAB sequence highly similar to the one of Desulfitobacterium dehalogenans (97.0% amino acid identity). As expected from the close relationship of both species by 16S rDNA comparison (96.7% similarity), their DsrAB sequences group together independent of the treeing methods applied.
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DISCUSSION |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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In this study we investigated the phylogeny of the dissimilatory sulfite reductase from a study set of reference species encompassing all described lineages of SRPs in order to clarify whether dsr genes, in addition to undergoing vertical transmission, have also been laterally transferred. Using degenerated PCR primers, DNA fragments with strong sequence similarities over their entire length to previously published dsrAB sequences were obtained from all investigated SRPs and from the sulfite reducer Desulfitobacterium dehalogenans.
DSR sequence motifs.
The newly determined
dsrAB-like sequences contain the essential cluster-binding
residues typical for dissimilatory sulfite reductases. In particular,
all alpha-subunit sequences contain the complete
(Cys-X5-Cys)-Xn-(Cys-X3-Cys)
motif required for coupling of the
[Fe4S4]-siroheme cofactor
(2). As for other dissimilatory sulfite reductases
(10), this Cys motif is truncated in the beta subunit of
the newly determined DsrAB sequences. In contrast to the prediction of
Dahl et al. (3) the DsrB subunit of
Thermodesulfobacterium mobile and
Thermodesulfobacterium commune (4, 8) does not
contain a complete
siroheme-[Fe4S4] binding site that could explain the measured binding of four sirohemes per
22 molecule (versus
two sirohemes for typical sulfite reductases). Furthermore, all DsrA
sequences possess the Cys-Pro and
Cys-X2-Cys-X2-Cys motif
required for linking
[Fe4S4] clusters
(3). Since the reverse PCR primers used for amplification
target part of the [Fe4S4] cluster binding
motif of DsrB only the Cys-Pro signature is present in all deduced DsrB
sequences. The absolute conservation of functionally important protein
sequences and the absence of frameshift or nonsense mutations suggests
that the characterized genes are transcribed and translated and
function as dissimilatory sulfite reductases. The sequenced
dissimilatory sulfite reductase genes of
Thermodesulfobacterium mobile are most likely
functionally expressed since the highly variable N-terminal sequence of
the beta-subunit is identical to the one determined by Edman
degradation (4). Comparison of the 10 N-terminal amino
acids of the beta-subunit determined by Edman degradation of the
dissimilatory sulfite reductase of Thermodesulfobacterium
commune (8) to the sequence deduced in our study
revealed a single amino acid difference at position 1 (Thr/Ser
predicted by Edman and Gly [GGA codon] found in our study). This
inconsistency is either caused by an experimental artifact (mistake in
the Edman degradation determination or at least two
Taq-induced mutations in the dsrAB clone of
Thermodesulfobacterium commune) or by the presence of more
than one type of dsrAB genes in this organism. Differences
between the deduced N-terminal sequence and that determined by
N-terminal polypeptide sequencing were also reported for the DsrB
protein of Desulfovibrio desulfuricans (25).
DSR homologs. Additional homologs to the investigated dsrAB genes may exist in some of the analyzed strains. This is not the case for Desulfitobacterium hafniense and Archaeoglobus fulgidus, since no additional dsrAB homologs are present in their complete genome sequences. Under the assumption that the PCR primers applied would amplify all putative dsr copies, we have indirect evidence that the Desulfotomaculum species, D. aeronauticum, D. putei, D. geothermicum, D. kuznetsovii, and D. thermobenzoicum do not contain multiple dsrAB copies which differ in sequence since the respective dsrAB PCR amplificates could be sequenced directly. For the other analyzed SRPs, knowledge of the copy number of dsrAB-like genes must await an extensive Southern hybridization or complete genome sequence analysis which was beyond the scope of this study.
DSR phylogeny and lateral transfer.
The core of our study was
a direct comparison between 16S rRNA and DsrAB trees of the respective
SRPs (Fig. 1). In this analysis it is an explicit assumption that the
16S rRNA phylogeny reflects the organismal phylogeny (36),
that is, that these highly conserved genes have undergone no lateral
transfer in the organisms studied. Based on this supposition, seven
Desulfotomaculum species, two Thermodesulfobacterium species, and Desulfobacula
toluolica possess nonorthologous dsrAB genes as
demonstrated by major inconsistencies between the DsrAB and 16S rRNA
trees. These inconsistencies most likely reflect lateral transfer of
dsrAB genes rather than the occurrence of dsrAB
paralogs which diverged after an initial dsr operon
duplication since all nonorthologous dsrAB genes are
phylogenetically affiliated with the (presumably orthologous)
dsrAB genes of the -Proteobacteria (Fig. 1).
Furthermore, organisms distantly related by 16S rRNA sequence
relationship, such as Desulfobacula toluolica and several
Desulfotomaculum species, contain similar nonorthologous dsrAB genes. This close relatedness of dsrAB
genes between species belonging to different bacterial divisions is
unlikely to be the product of convergent evolution and can more
reasonably be explained by multiple lateral acquisitions from
a common donor lineage within the -Proteobacteria.
Consistent with this inference, all putative xenologous
dsrAB sequences have insertions typical for the
-Proteobacteria (Fig. 3).
-Proteobacteria these
limitations apply to Desulfoarculus baarsii and
Desulfomonile tiedjei. Furthermore, the characterized DsrAB
sequences of Archaeoglobus and
Thermodesulfovibrio species and the "authentic"
Desulfotomaculum and Desulfitobacterium species
possibly could originate from a progenitor of the
-Proteobacteria or from other as-yet-unidentified SRPs.
In fact, it seems likely that the genus Archaeoglobus
inherited dsrAB genes from a bacterial donor (i) because the
evolutionary distance between Archaeoglobus species and the
bacterial sulfate reducers is much shorter in the DsrAB tree than in
the 16S rRNA tree and (ii) because the sulfate-reducing phenotype is
currently restricted to the genus Archaeoglobus within the
archaeal domain. Further support for a lateral transfer of the
dsrAB genes to the Archaeoglobales was obtained
by a phylogenetic analysis on an alignment of the alpha- against the
beta-subunit amino acid sequences. Such analysis can be used to root
the Dsr subunit trees (6, 13) (Fig. 2), since the subunits
are paralogs arising from an ancestral dsr gene duplication (3). Independent of the treeing method used, the root was
consistently indicated between the DsrAB of the
Thermodesulfovibrio species and the DsrABs of all other
analyzed SRPs, including the Archaeoglobales. This is
inconsistent with the 16S rRNA phylogeny and points to a bacterial
origin of the Archaeoglobales dsrAB genes
(
in the DsrAB tree; Fig.
1). However, the results from the paralogous rooting should not be
overemphasized since the alignment of the Dsr subunits against each
other (i) is relatively short (173 amino acid positions) and (ii)
contains several regions which cannot unambiguously be aligned (caused
by the relatively low sequence similarities of the subunits to each
other). Furthermore, no evidence for lateral transfer of the
Archaeoglobus fulgidus dsrAB genes was indicated by atypical
sequence characteristic analysis (27; J. Lawrence,
unpublished data), suggesting that, if the genes are xenologs, they
have completely ameliorated toward their host genome and were the
result of an ancient LGT event.
DSR donor lineages.
The dsrAB gene donors were
members of at least two distinct evolutionary lineages within the
-Proteobacteria
(
to
and b
in the DsrAB tree; Fig. 1). Donor lineage a
contributed dsrAB genes to two phylogenetically remote
groups of bacteria, Desulfobacula toluolica
(-Proteobacteria) and several Desulfotomaculum
species (low G+C gram positives)
( to
in the 16S rDNA
tree; Fig. 1), suggesting that this lineage is particularly adept at
donating dsrAB and possibly other genes. The specific
identities of the donor lineages is unknown based on the current data,
since no orthologous dsrAB genes were identified within the
putative xenolog groups. It is however striking that
Desulfobacula toluolica and all but two
Desulfotomaculum species which received the xenologous dsrAB are oxidizing their characteristic substrates
completely to CO2 while the "authentic"
Desulfotomaculum and Desulfitobacterium species
are exclusively incomplete oxidizers. One possible explanation for this
feature is that the dsrAB donor was a complete oxidizer which bestowed this metabolic capability to the
Desulfotomaculum and Desulfobacula species, which
subsequently was lost in Desulfotomaculum thermosapovorans
and Desulfotomaculum thermocisternum (Table 1). Furthermore,
most of the recipients of xenologous dsrAB are thermophilic (Table 1) which could indicate a thermophilic lifestyle of the donor species.
DSR recipient lineages.
Desulfobacula toluolica is
the recipient of the most recent putative LGT event thus far identified
(; Fig. 1) since
its close relatives, Desulfobacter latus and
Desulfobacter vibrioformis, contain orthologous
dsrAB genes. This is also supported by no identifiable
amelioration of the third codon position G+C content of the xenologous
dsr genes toward the mean G+C content of the host D. toluolica genome (Table 1). The evolution of the genus Desulfotomaculum was also affected by LGT events of
dsrAB genes. The number of LGT events within this genus is
difficult to predict since the subclustering of its members is not
always well supported in the 16S rDNA tree (Fig. 1). On the basis of
the presented 16S rDNA tree, it is most parsimonious to postulate at
least three LGT events within this genus
(
to
in the 16S rDNA
tree of Fig. 1). Alternatively, one could hypothesize that a single
lateral dsrAB gene transfer event occurred to the common
ancestor of the genera Desulfotomaculum, Desulfosporosinus,
and Desulfitobacterium (which did not displace the
orthologous dsr genes), followed by a subsequent xenolog
gene loss on at least two independent occasions from the ancestors of
the "authentic" Desulfotomaculum and
Desulfosporosinus-Desulfitobacterium species, respectively.
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ACKNOWLEDGMENTS |
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M.K. and H.A. were supported by a grant from the Deutsche
Forschungsgemeinschaft to M.W. in the framework of the
project "Degradation of marine pollutants by cyanobacterial mats
an
interdisciplinary approach." M.F. was supported by the
Max-Planck-Gesellschaft. A.J.R. was funded by NSERC grant 2277085-00.
D.A.S. and S.F. were supported by NSF grant DEB-9714303. P.H. is funded
by the Cooperative Research Centre for Waste Management and Pollution
Control, Ltd., a center established and supported under the Australian
Government's Cooperative Research Centres Program.
We thank Bianca Wagner (Marburg, Germany) for excellent technical assistance. We also thank Kathrin Riedel for helpful discussions.
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FOOTNOTES |
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* Corresponding author. Mailing address: Lehrstuhl für Mikrobiologie, Technische Universität München, Am Hochanger 4, D-85350 Freising, Germany. Phone: 49-816-171-5444. Fax: 49-816-171-5475. E-mail: wagner{at}mikro.biologie.tu-muenchen.de.
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Journal of Bacteriology, October 2001, p. 6028-6035, Vol. 183, No. 20
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.20.6028-6035.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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