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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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Quantification of Desulfosporosinus 16S rRNA gene numbers by quantitative PCR over a peatland depth profile of 0–30 cm and quantification of potential Desulfosporosinus sulfate reduction rates (SRR). 16S rRNA gene numbers were determined in triplicate cores over the years 2004, 2006, and 2007, with the exception of the 20–30-cm depth, where samples were only available for the year 2007. The distribution of gene numbers is represented in boxplots showing the interquartile range and the median. Whiskers (maximum 1.5-fold interquartile range) represent the data distribution outside the interquartile range; outliers are depicted as black circles. Potential SRR of the Desulfosporosinus population were determined using the estimated cell-specific SRR of the identified peatland Desulfosporosinus sp., the interquartile range of Desulfosporosinus 16S rRNA genes per depth, and an average of 4.4 16S rRNA gene copies per cell (for details see text).
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Figure 5: Quantification of Desulfosporosinus 16S rRNA gene numbers by quantitative PCR over a peatland depth profile of 0–30 cm and quantification of potential Desulfosporosinus sulfate reduction rates (SRR). 16S rRNA gene numbers were determined in triplicate cores over the years 2004, 2006, and 2007, with the exception of the 20–30-cm depth, where samples were only available for the year 2007. The distribution of gene numbers is represented in boxplots showing the interquartile range and the median. Whiskers (maximum 1.5-fold interquartile range) represent the data distribution outside the interquartile range; outliers are depicted as black circles. Potential SRR of the Desulfosporosinus population were determined using the estimated cell-specific SRR of the identified peatland Desulfosporosinus sp., the interquartile range of Desulfosporosinus 16S rRNA genes per depth, and an average of 4.4 16S rRNA gene copies per cell (for details see text).

Mentions: Desulfosporosinus sp. with its low natural abundance of 0.006% of the total bacterial and archaeal community is a member of the ‘rare biosphere’, which is defined as the sum of those taxa with an abundance of less than 0.1–1% (Fuhrman, 2009; Pedros-Alio, 2006; Sogin et al., 2006). Based on its absolute abundance in the peatland over a depth profile of 0–30 cm (Fig. 5), the potential SRR of the natural Desulfosporosinus population was calculated using its estimated cs-SRR. The potential SRRs of the natural Desulfosporosinus population were 4.0–36.8 nmol (g soil w. wt.)−1 day−1 between 0–30 cm soil depth (Fig. 5). In comparison, radiotracer-measured gross SRRs of the studied peatland ranged from 0 to ca. 340 nmol (g soil w. wt.)−1 day−1 over a depth profile of 0–30 cm and a 300 days period, with sulfate reduction proceeding at >10 nmol (g soil w. wt.)−1 day−1 in at least one of the analyzed depth fractions at each sampling day (5–10 cm depth fractions) (Knorr and Blodau, 2009; Knorr et al., 2009). Even if cs-SRR of Desulfosporosinus sp. were overestimated by one order of magnitude and would therefore resemble average cs-SRR of cultured sulfate reducers (Detmers et al., 2001) or if a subpopulation would have occurred as inactive spores, the natural Desulfosporosinus population would still have the potential to drive a considerable part of sulfate reduction compared to its abundance. The presence of mostly physiologically active Desulfosporosinus cells in water-saturated, anoxic soil pockets above the water-table and in the anoxic peat below the water-table is expected as sulfate reduction in peatlands is not only fuelled by allochthonous sulfate but also by an oxic (Deppe et al., 2009; Knorr and Blodau, 2009; Knorr et al., 2009; Reiche et al., 2009) and anoxic sulfur cycle (Blodau et al., 2007; Jørgensen, 1990b; Nielsen et al., 2010) and constitutes an ongoing process in the studied peatland as evident from δ34S measurements (e.g., Alewell and Novak, 2001; Alewell et al., 2008) and the radiotracer studies described above. In addition, Desulfosporosinus spp. are known to switch under sulfate limitation to the fermentation of lactate and pyruvate (Spring and Rosenzweig, 2006), to reductive acetogenesis from formate, methanol, or methyl groups of aromatic compounds (Rabus et al., 2006), or to dissimlatory iron(III) reduction (Ramamoorthy et al., 2006). At the same time, Desulfosporosinus spp. are well adapted to persist throughout extended periods of droughts and subsequent complete oxygenation of the peat soil (Reiche et al., 2009) by their ability to form endospores (Lee et al., 2009a; Ramamoorthy et al., 2006; Spring and Rosenzweig, 2006; Vatsurina et al., 2008). In summary, Desulfosporosinus spp. appear well-adapted to the highly fluctuating conditions in low-sulfate peatlands.


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

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

Quantification of Desulfosporosinus 16S rRNA gene numbers by quantitative PCR over a peatland depth profile of 0–30 cm and quantification of potential Desulfosporosinus sulfate reduction rates (SRR). 16S rRNA gene numbers were determined in triplicate cores over the years 2004, 2006, and 2007, with the exception of the 20–30-cm depth, where samples were only available for the year 2007. The distribution of gene numbers is represented in boxplots showing the interquartile range and the median. Whiskers (maximum 1.5-fold interquartile range) represent the data distribution outside the interquartile range; outliers are depicted as black circles. Potential SRR of the Desulfosporosinus population were determined using the estimated cell-specific SRR of the identified peatland Desulfosporosinus sp., the interquartile range of Desulfosporosinus 16S rRNA genes per depth, and an average of 4.4 16S rRNA gene copies per cell (for details see text).
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Related In: Results  -  Collection

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Figure 5: Quantification of Desulfosporosinus 16S rRNA gene numbers by quantitative PCR over a peatland depth profile of 0–30 cm and quantification of potential Desulfosporosinus sulfate reduction rates (SRR). 16S rRNA gene numbers were determined in triplicate cores over the years 2004, 2006, and 2007, with the exception of the 20–30-cm depth, where samples were only available for the year 2007. The distribution of gene numbers is represented in boxplots showing the interquartile range and the median. Whiskers (maximum 1.5-fold interquartile range) represent the data distribution outside the interquartile range; outliers are depicted as black circles. Potential SRR of the Desulfosporosinus population were determined using the estimated cell-specific SRR of the identified peatland Desulfosporosinus sp., the interquartile range of Desulfosporosinus 16S rRNA genes per depth, and an average of 4.4 16S rRNA gene copies per cell (for details see text).
Mentions: Desulfosporosinus sp. with its low natural abundance of 0.006% of the total bacterial and archaeal community is a member of the ‘rare biosphere’, which is defined as the sum of those taxa with an abundance of less than 0.1–1% (Fuhrman, 2009; Pedros-Alio, 2006; Sogin et al., 2006). Based on its absolute abundance in the peatland over a depth profile of 0–30 cm (Fig. 5), the potential SRR of the natural Desulfosporosinus population was calculated using its estimated cs-SRR. The potential SRRs of the natural Desulfosporosinus population were 4.0–36.8 nmol (g soil w. wt.)−1 day−1 between 0–30 cm soil depth (Fig. 5). In comparison, radiotracer-measured gross SRRs of the studied peatland ranged from 0 to ca. 340 nmol (g soil w. wt.)−1 day−1 over a depth profile of 0–30 cm and a 300 days period, with sulfate reduction proceeding at >10 nmol (g soil w. wt.)−1 day−1 in at least one of the analyzed depth fractions at each sampling day (5–10 cm depth fractions) (Knorr and Blodau, 2009; Knorr et al., 2009). Even if cs-SRR of Desulfosporosinus sp. were overestimated by one order of magnitude and would therefore resemble average cs-SRR of cultured sulfate reducers (Detmers et al., 2001) or if a subpopulation would have occurred as inactive spores, the natural Desulfosporosinus population would still have the potential to drive a considerable part of sulfate reduction compared to its abundance. The presence of mostly physiologically active Desulfosporosinus cells in water-saturated, anoxic soil pockets above the water-table and in the anoxic peat below the water-table is expected as sulfate reduction in peatlands is not only fuelled by allochthonous sulfate but also by an oxic (Deppe et al., 2009; Knorr and Blodau, 2009; Knorr et al., 2009; Reiche et al., 2009) and anoxic sulfur cycle (Blodau et al., 2007; Jørgensen, 1990b; Nielsen et al., 2010) and constitutes an ongoing process in the studied peatland as evident from δ34S measurements (e.g., Alewell and Novak, 2001; Alewell et al., 2008) and the radiotracer studies described above. In addition, Desulfosporosinus spp. are known to switch under sulfate limitation to the fermentation of lactate and pyruvate (Spring and Rosenzweig, 2006), to reductive acetogenesis from formate, methanol, or methyl groups of aromatic compounds (Rabus et al., 2006), or to dissimlatory iron(III) reduction (Ramamoorthy et al., 2006). At the same time, Desulfosporosinus spp. are well adapted to persist throughout extended periods of droughts and subsequent complete oxygenation of the peat soil (Reiche et al., 2009) by their ability to form endospores (Lee et al., 2009a; Ramamoorthy et al., 2006; Spring and Rosenzweig, 2006; Vatsurina et al., 2008). In summary, Desulfosporosinus spp. appear well-adapted to the highly fluctuating conditions in low-sulfate peatlands.

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