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A 'rare biosphere' microorganism contributes to sulfate reduction in a peatland.

Pester M, Bittner N, Deevong P, Wagner M, Loy A - ISME J (2010)

Bottom Line: Methane emission from peatlands contributes substantially to global warming but is significantly reduced by sulfate reduction, which is fuelled by globally increasing aerial sulfur pollution.For the identified Desulfosporosinus species a high cell-specific sulfate reduction rate of up to 341 fmol SO₄²⁻ cell⁻¹ day⁻¹ was estimated.Thus, the small Desulfosporosinus population has the potential to reduce sulfate in situ at a rate of 4.0-36.8 nmol (g soil w. wt.)⁻¹ day⁻¹, sufficient to account for a considerable part of sulfate reduction in the peat soil.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbial Ecology, University of Vienna, Wien, Austria.

ABSTRACT
Methane emission from peatlands contributes substantially to global warming but is significantly reduced by sulfate reduction, which is fuelled by globally increasing aerial sulfur pollution. However, the biology behind sulfate reduction in terrestrial ecosystems is not well understood and the key players for this process as well as their abundance remained unidentified. Comparative 16S rRNA gene stable isotope probing (SIP) in the presence and absence of sulfate indicated that a Desulfosporosinus species, which constitutes only 0.006% of the total microbial community 16S rRNA genes, is an important sulfate reducer in a long-term experimental peatland field site. Parallel SIP using dsrAB (encoding subunit A and B of the dissimilatory (bi)sulfite reductase) identified no additional sulfate reducers under the conditions tested. For the identified Desulfosporosinus species a high cell-specific sulfate reduction rate of up to 341 fmol SO₄²⁻ cell⁻¹ day⁻¹ was estimated. Thus, the small Desulfosporosinus population has the potential to reduce sulfate in situ at a rate of 4.0-36.8 nmol (g soil w. wt.)⁻¹ day⁻¹, sufficient to account for a considerable part of sulfate reduction in the peat soil. Modeling of sulfate diffusion to such highly active cells identified no limitation in sulfate supply even at bulk concentrations as low as 10 μM. Collectively, these data show that the identified Desulfosporosinus species, despite being a member of the 'rare biosphere', contributes to an important biogeochemical process that diverts the carbon flow in peatlands from methane to CO₂ and, thus, alters their contribution to global warming.

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Phylogenetic consensus tree of 16S rRNA gene clones affiliated to the genus Desulfosporosinus (marked in bold). Clones were grouped according to ≥99% sequence identity; representing T-RFs and number of clones per group are indicated. With one exception, all Desulfosporosinus clones have a 16S rRNA sequence identity of >97% to each other. Parsimony bootstrap values for branches are indicated by solid circles (>90%) and open circles (75 to 90%). GenBank accession numbers of published 16S rRNA gene sequences are indicated behind the name of the respective sequences. The bar represents 1% estimated sequence divergence as inferred from distance matrix analysis.
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Figure 3: Phylogenetic consensus tree of 16S rRNA gene clones affiliated to the genus Desulfosporosinus (marked in bold). Clones were grouped according to ≥99% sequence identity; representing T-RFs and number of clones per group are indicated. With one exception, all Desulfosporosinus clones have a 16S rRNA sequence identity of >97% to each other. Parsimony bootstrap values for branches are indicated by solid circles (>90%) and open circles (75 to 90%). GenBank accession numbers of published 16S rRNA gene sequences are indicated behind the name of the respective sequences. The bar represents 1% estimated sequence divergence as inferred from distance matrix analysis.

Mentions: Incorporation of substrate-13C into the biomass of active sulfate reducers was followed by pairwise comparison of incubations with and without sulfate using a 16S rRNA gene-based T-RFLP screening of density-resolved DNA. A clear difference in T-RFLP patterns between incubations with and without sulfate became apparent for the bacterial community after 2 months of incubation. In sulfate-amended incubations, a distinct T-RF at 140 bp dominated the ‘heaviest’ (13C-labeled) PCR-amplifiable density fractions and was almost absent in the ‘light’ (unlabeled) fractions. In the control incubation without sulfate, the 140-bp T-RF was of very minor abundance in each fraction throughout the density gradient (Fig. 2). The same was true for the 12C-control of non-incubated pristine peat soil (Fig. S3). Cloning of bacterial 16S rRNA genes from the ‘heavy’ fraction of the incubation with sulfate (Table S1, Fig. S4) revealed that the dominant 140-bp T-RF represents almost exclusively organisms within the genus Desulfosporosinus (Firmicutes) (16 out of 95 clones in the incubation with sulfate, Fig. 3) and one clone of the Acidobacteria subgroup 3. A differential T-RFLP analysis using the alternative restriction enzyme RsaI confirmed that the dominant 140-bp T-RF in the ‘heavy fraction’ represented exclusively Desulfosporosinus spp. (data not shown). Three additional Desulfosporosinus sp. clones had a T-RF at 171 bp (indicating that different Desulfosporosinus ecotypes may be present in the studied peatland) but a corresponding peak was not detected in the SIP-T-RFLP analyses. In a parallel clone library from the heavy fraction of the incubation without sulfate, no Desulfosporosinus sp. was detected (Table S1, Fig. S4). Again, one clone representing Acidobacteria subgroup 3 with a T-RF of 140 bp was retrieved, explaining the very minor T-RF at 140 bp in the incubations without sulfate (Fig. 2) and most likely also in the 12C-control of non-incubated pristine peat soil (Fig. S3).


A 'rare biosphere' microorganism contributes to sulfate reduction in a peatland.

Pester M, Bittner N, Deevong P, Wagner M, Loy A - ISME J (2010)

Phylogenetic consensus tree of 16S rRNA gene clones affiliated to the genus Desulfosporosinus (marked in bold). Clones were grouped according to ≥99% sequence identity; representing T-RFs and number of clones per group are indicated. With one exception, all Desulfosporosinus clones have a 16S rRNA sequence identity of >97% to each other. Parsimony bootstrap values for branches are indicated by solid circles (>90%) and open circles (75 to 90%). GenBank accession numbers of published 16S rRNA gene sequences are indicated behind the name of the respective sequences. The bar represents 1% estimated sequence divergence as inferred from distance matrix analysis.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4499578&req=5

Figure 3: Phylogenetic consensus tree of 16S rRNA gene clones affiliated to the genus Desulfosporosinus (marked in bold). Clones were grouped according to ≥99% sequence identity; representing T-RFs and number of clones per group are indicated. With one exception, all Desulfosporosinus clones have a 16S rRNA sequence identity of >97% to each other. Parsimony bootstrap values for branches are indicated by solid circles (>90%) and open circles (75 to 90%). GenBank accession numbers of published 16S rRNA gene sequences are indicated behind the name of the respective sequences. The bar represents 1% estimated sequence divergence as inferred from distance matrix analysis.
Mentions: Incorporation of substrate-13C into the biomass of active sulfate reducers was followed by pairwise comparison of incubations with and without sulfate using a 16S rRNA gene-based T-RFLP screening of density-resolved DNA. A clear difference in T-RFLP patterns between incubations with and without sulfate became apparent for the bacterial community after 2 months of incubation. In sulfate-amended incubations, a distinct T-RF at 140 bp dominated the ‘heaviest’ (13C-labeled) PCR-amplifiable density fractions and was almost absent in the ‘light’ (unlabeled) fractions. In the control incubation without sulfate, the 140-bp T-RF was of very minor abundance in each fraction throughout the density gradient (Fig. 2). The same was true for the 12C-control of non-incubated pristine peat soil (Fig. S3). Cloning of bacterial 16S rRNA genes from the ‘heavy’ fraction of the incubation with sulfate (Table S1, Fig. S4) revealed that the dominant 140-bp T-RF represents almost exclusively organisms within the genus Desulfosporosinus (Firmicutes) (16 out of 95 clones in the incubation with sulfate, Fig. 3) and one clone of the Acidobacteria subgroup 3. A differential T-RFLP analysis using the alternative restriction enzyme RsaI confirmed that the dominant 140-bp T-RF in the ‘heavy fraction’ represented exclusively Desulfosporosinus spp. (data not shown). Three additional Desulfosporosinus sp. clones had a T-RF at 171 bp (indicating that different Desulfosporosinus ecotypes may be present in the studied peatland) but a corresponding peak was not detected in the SIP-T-RFLP analyses. In a parallel clone library from the heavy fraction of the incubation without sulfate, no Desulfosporosinus sp. was detected (Table S1, Fig. S4). Again, one clone representing Acidobacteria subgroup 3 with a T-RF of 140 bp was retrieved, explaining the very minor T-RF at 140 bp in the incubations without sulfate (Fig. 2) and most likely also in the 12C-control of non-incubated pristine peat soil (Fig. S3).

Bottom Line: Methane emission from peatlands contributes substantially to global warming but is significantly reduced by sulfate reduction, which is fuelled by globally increasing aerial sulfur pollution.For the identified Desulfosporosinus species a high cell-specific sulfate reduction rate of up to 341 fmol SO₄²⁻ cell⁻¹ day⁻¹ was estimated.Thus, the small Desulfosporosinus population has the potential to reduce sulfate in situ at a rate of 4.0-36.8 nmol (g soil w. wt.)⁻¹ day⁻¹, sufficient to account for a considerable part of sulfate reduction in the peat soil.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbial Ecology, University of Vienna, Wien, Austria.

ABSTRACT
Methane emission from peatlands contributes substantially to global warming but is significantly reduced by sulfate reduction, which is fuelled by globally increasing aerial sulfur pollution. However, the biology behind sulfate reduction in terrestrial ecosystems is not well understood and the key players for this process as well as their abundance remained unidentified. Comparative 16S rRNA gene stable isotope probing (SIP) in the presence and absence of sulfate indicated that a Desulfosporosinus species, which constitutes only 0.006% of the total microbial community 16S rRNA genes, is an important sulfate reducer in a long-term experimental peatland field site. Parallel SIP using dsrAB (encoding subunit A and B of the dissimilatory (bi)sulfite reductase) identified no additional sulfate reducers under the conditions tested. For the identified Desulfosporosinus species a high cell-specific sulfate reduction rate of up to 341 fmol SO₄²⁻ cell⁻¹ day⁻¹ was estimated. Thus, the small Desulfosporosinus population has the potential to reduce sulfate in situ at a rate of 4.0-36.8 nmol (g soil w. wt.)⁻¹ day⁻¹, sufficient to account for a considerable part of sulfate reduction in the peat soil. Modeling of sulfate diffusion to such highly active cells identified no limitation in sulfate supply even at bulk concentrations as low as 10 μM. Collectively, these data show that the identified Desulfosporosinus species, despite being a member of the 'rare biosphere', contributes to an important biogeochemical process that diverts the carbon flow in peatlands from methane to CO₂ and, thus, alters their contribution to global warming.

Show MeSH
Related in: MedlinePlus