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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 deduced DsrAB amino acid sequences longer than 500 amino acids, showing the affiliation of OTUs retrieved from the ‘heavy’ SIP fractions (indicated by a triangle) in comparison to known sulfate reducers and peat soil OTUs retrieved in a previous study from the same and a neighboring peatland (Loy et al., 2004. An OTU comprises all sequences having ≥90% amino acid sequence identity. Deduced DsrAB sequences shorter than 500 amino acids (indicated by dashed branches) were individually added to the distance matrix tree without changing the overall tree topology by using the ARB Parsimony_interactive tool. Parsimony bootstrap values for branches are indicated by solid circles (>90%) and open circles (75 to 90%). The Desulfosporosinus-related dsrA clone (shown in red) was retrieved from the 2-month incubation with sulfate using Desulfosporosinus/Desulfitobacterium-selective primers. GenBank accession numbers of published DsrAB sequences are indicated behind the name of the respective sequences. The bar represents 10% estimated sequence divergence as inferred from distance matrix analysis.
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Figure 6: Phylogenetic consensus tree of deduced DsrAB amino acid sequences longer than 500 amino acids, showing the affiliation of OTUs retrieved from the ‘heavy’ SIP fractions (indicated by a triangle) in comparison to known sulfate reducers and peat soil OTUs retrieved in a previous study from the same and a neighboring peatland (Loy et al., 2004. An OTU comprises all sequences having ≥90% amino acid sequence identity. Deduced DsrAB sequences shorter than 500 amino acids (indicated by dashed branches) were individually added to the distance matrix tree without changing the overall tree topology by using the ARB Parsimony_interactive tool. Parsimony bootstrap values for branches are indicated by solid circles (>90%) and open circles (75 to 90%). The Desulfosporosinus-related dsrA clone (shown in red) was retrieved from the 2-month incubation with sulfate using Desulfosporosinus/Desulfitobacterium-selective primers. GenBank accession numbers of published DsrAB sequences are indicated behind the name of the respective sequences. The bar represents 10% estimated sequence divergence as inferred from distance matrix analysis.

Mentions: As evident from gross SRRs (Knorr and Blodau, 2009; Knorr et al., 2009) and previous diversity studies, several other sulfate reducers are present in this peatland, e.g., Desulfomonile spp. and Syntrophobacter spp. (Loy et al., 2004). In addition, the presence of potentially new taxa is indicated by the detection of novel deep-branching lineages of the functional marker genes dsrAB [encoding subunit A and B of the dissimilatory (bi)sulfite reductase] (Loy et al., 2004; Schmalenberger et al., 2007). Currently, it is not known whether microorganisms harboring these novel dsrAB are capable of dissimilatory sulfate/sulfite (Wagner et al., 2005) or organosulfonate reduction (Laue et al., 1997; Laue et al., 2001), switch between a syntrophic and sulfate reducing lifestyle upon the availability of sulfate (Wallrabenstein et al., 1994; Wallrabenstein et al., 1995), or are purely syntrophic microorganisms (Imachi et al., 2006). Comparison of dsrAB clone libraries from the ‘heavy’ fractions of the SIP incubations with and without sulfate (Fig. 6, Table 2) and dsrAB T-RFLP analyses for both incubations (Fig. S7) indicated that known sulfate reducers other than Desulfosporosinus or microorganisms harboring novel deep-branching dsrAB made no quantitatively important contribution (if any) to sulfate reduction (detailed in SI Text). However, it is very likely that additional sulfate reducers in the studied peatland use other substrates for energy metabolism or are adapted to other conditions than those provided in our SIP incubations and, thus, were not identified as active populations.


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 deduced DsrAB amino acid sequences longer than 500 amino acids, showing the affiliation of OTUs retrieved from the ‘heavy’ SIP fractions (indicated by a triangle) in comparison to known sulfate reducers and peat soil OTUs retrieved in a previous study from the same and a neighboring peatland (Loy et al., 2004. An OTU comprises all sequences having ≥90% amino acid sequence identity. Deduced DsrAB sequences shorter than 500 amino acids (indicated by dashed branches) were individually added to the distance matrix tree without changing the overall tree topology by using the ARB Parsimony_interactive tool. Parsimony bootstrap values for branches are indicated by solid circles (>90%) and open circles (75 to 90%). The Desulfosporosinus-related dsrA clone (shown in red) was retrieved from the 2-month incubation with sulfate using Desulfosporosinus/Desulfitobacterium-selective primers. GenBank accession numbers of published DsrAB sequences are indicated behind the name of the respective sequences. The bar represents 10% estimated sequence divergence as inferred from distance matrix analysis.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4499578&req=5

Figure 6: Phylogenetic consensus tree of deduced DsrAB amino acid sequences longer than 500 amino acids, showing the affiliation of OTUs retrieved from the ‘heavy’ SIP fractions (indicated by a triangle) in comparison to known sulfate reducers and peat soil OTUs retrieved in a previous study from the same and a neighboring peatland (Loy et al., 2004. An OTU comprises all sequences having ≥90% amino acid sequence identity. Deduced DsrAB sequences shorter than 500 amino acids (indicated by dashed branches) were individually added to the distance matrix tree without changing the overall tree topology by using the ARB Parsimony_interactive tool. Parsimony bootstrap values for branches are indicated by solid circles (>90%) and open circles (75 to 90%). The Desulfosporosinus-related dsrA clone (shown in red) was retrieved from the 2-month incubation with sulfate using Desulfosporosinus/Desulfitobacterium-selective primers. GenBank accession numbers of published DsrAB sequences are indicated behind the name of the respective sequences. The bar represents 10% estimated sequence divergence as inferred from distance matrix analysis.
Mentions: As evident from gross SRRs (Knorr and Blodau, 2009; Knorr et al., 2009) and previous diversity studies, several other sulfate reducers are present in this peatland, e.g., Desulfomonile spp. and Syntrophobacter spp. (Loy et al., 2004). In addition, the presence of potentially new taxa is indicated by the detection of novel deep-branching lineages of the functional marker genes dsrAB [encoding subunit A and B of the dissimilatory (bi)sulfite reductase] (Loy et al., 2004; Schmalenberger et al., 2007). Currently, it is not known whether microorganisms harboring these novel dsrAB are capable of dissimilatory sulfate/sulfite (Wagner et al., 2005) or organosulfonate reduction (Laue et al., 1997; Laue et al., 2001), switch between a syntrophic and sulfate reducing lifestyle upon the availability of sulfate (Wallrabenstein et al., 1994; Wallrabenstein et al., 1995), or are purely syntrophic microorganisms (Imachi et al., 2006). Comparison of dsrAB clone libraries from the ‘heavy’ fractions of the SIP incubations with and without sulfate (Fig. 6, Table 2) and dsrAB T-RFLP analyses for both incubations (Fig. S7) indicated that known sulfate reducers other than Desulfosporosinus or microorganisms harboring novel deep-branching dsrAB made no quantitatively important contribution (if any) to sulfate reduction (detailed in SI Text). However, it is very likely that additional sulfate reducers in the studied peatland use other substrates for energy metabolism or are adapted to other conditions than those provided in our SIP incubations and, thus, were not identified as active populations.

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