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Activation of methanogenesis in arid biological soil crusts despite the presence of oxygen.

Angel R, Matthies D, Conrad R - PLoS ONE (2011)

Bottom Line: Methanogenesis is traditionally thought to occur only in highly reduced, anoxic environments.Since methanotrophs were not detectable in the BSC, all the methane produced was released into the atmosphere.Our findings point to a formerly unknown participation of desert soils in the global methane cycle.

View Article: PubMed Central - PubMed

Affiliation: Max-Planck-Institute for Terrestrial Microbiology, Marburg, Germany.

ABSTRACT
Methanogenesis is traditionally thought to occur only in highly reduced, anoxic environments. Wetland and rice field soils are well known sources for atmospheric methane, while aerated soils are considered sinks. Although methanogens have been detected in low numbers in some aerated, and even in desert soils, it remains unclear whether they are active under natural oxic conditions, such as in biological soil crusts (BSCs) of arid regions. To answer this question we carried out a factorial experiment using microcosms under simulated natural conditions. The BSC on top of an arid soil was incubated under moist conditions in all possible combinations of flooding and drainage, light and dark, air and nitrogen headspace. In the light, oxygen was produced by photosynthesis. Methane production was detected in all microcosms, but rates were much lower when oxygen was present. In addition, the δ(13)C of the methane differed between the oxic/oxygenic and anoxic microcosms. While under anoxic conditions methane was mainly produced from acetate, it was almost entirely produced from H(2)/CO(2) under oxic/oxygenic conditions. Only two genera of methanogens were identified in the BSC-Methanosarcina and Methanocella; their abundance and activity in transcribing the mcrA gene (coding for methyl-CoM reductase) was higher under anoxic than oxic/oxygenic conditions, respectively. Both methanogens also actively transcribed the oxygen detoxifying gene catalase. Since methanotrophs were not detectable in the BSC, all the methane produced was released into the atmosphere. Our findings point to a formerly unknown participation of desert soils in the global methane cycle.

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Gene and transcript copy numbers quantified using qPCR plotted against methane production rates: means±1 SE; n = 3.In situ refers to the dry BSC prior to any treatment. A. mcrA gene and transcript copy numbers. B. 16S rRNA gene copy numbers.
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pone-0020453-g003: Gene and transcript copy numbers quantified using qPCR plotted against methane production rates: means±1 SE; n = 3.In situ refers to the dry BSC prior to any treatment. A. mcrA gene and transcript copy numbers. B. 16S rRNA gene copy numbers.

Mentions: Thanks to this low-complexity methanogenic community we could individually quantify the 16S rRNA gene copies and mcrA gene and transcripts copies for the two methanogenic types as well as generally quantify the 16S rRNA gene of the archaeal community, and the total mcrA gene and transcript copies. We observed differences between individual treatment combinations, but by far the strongest effects were a smaller methanogenic community and lower transcription levels in the oxic/oxygenic compared to the anoxic microcosms (Figure 3). 16S rRNA and mcrA gene copies were in the range of 108–109 copies gdw−1 in the anoxic but only 103–107 in the oxic/oxygenic microcosms. In all treatments we observed an increase in the quantity of mcrA gene copies from 3.15×104 copies gdw−1 in the soil before incubation to at least 4.16×105 copies gdw−1 (a tenfold increase in the WLO treatment) and up to 1.15×109 copies gdw−1 in the FDN treatment (an increase of almost five orders of magnitude). Apart from a general effect of oxygen on the community size and gene expression, we noted a differential effect on Methanocella and Methanosarcina. The ratio of Methanosarcina to total 16S rRNA gene copies was significantly lower in the oxic/oxygenic than in the anoxic treatments (Table S1, Figure 3). In contrast to the effect on methane production, flooding did not have a significant effect on the ratio of Methanosarcina to total 16S rRNA gene copies. The same trend was seen for the ratio of Methanosarcina mcrA to the general mcrA gene and transcript copies, while no such effects could be seen for the ratio of Methanocella to total 16S rRNA gene and mcrA gene and transcript copies (All tests P>0.24).


Activation of methanogenesis in arid biological soil crusts despite the presence of oxygen.

Angel R, Matthies D, Conrad R - PLoS ONE (2011)

Gene and transcript copy numbers quantified using qPCR plotted against methane production rates: means±1 SE; n = 3.In situ refers to the dry BSC prior to any treatment. A. mcrA gene and transcript copy numbers. B. 16S rRNA gene copy numbers.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3105065&req=5

pone-0020453-g003: Gene and transcript copy numbers quantified using qPCR plotted against methane production rates: means±1 SE; n = 3.In situ refers to the dry BSC prior to any treatment. A. mcrA gene and transcript copy numbers. B. 16S rRNA gene copy numbers.
Mentions: Thanks to this low-complexity methanogenic community we could individually quantify the 16S rRNA gene copies and mcrA gene and transcripts copies for the two methanogenic types as well as generally quantify the 16S rRNA gene of the archaeal community, and the total mcrA gene and transcript copies. We observed differences between individual treatment combinations, but by far the strongest effects were a smaller methanogenic community and lower transcription levels in the oxic/oxygenic compared to the anoxic microcosms (Figure 3). 16S rRNA and mcrA gene copies were in the range of 108–109 copies gdw−1 in the anoxic but only 103–107 in the oxic/oxygenic microcosms. In all treatments we observed an increase in the quantity of mcrA gene copies from 3.15×104 copies gdw−1 in the soil before incubation to at least 4.16×105 copies gdw−1 (a tenfold increase in the WLO treatment) and up to 1.15×109 copies gdw−1 in the FDN treatment (an increase of almost five orders of magnitude). Apart from a general effect of oxygen on the community size and gene expression, we noted a differential effect on Methanocella and Methanosarcina. The ratio of Methanosarcina to total 16S rRNA gene copies was significantly lower in the oxic/oxygenic than in the anoxic treatments (Table S1, Figure 3). In contrast to the effect on methane production, flooding did not have a significant effect on the ratio of Methanosarcina to total 16S rRNA gene copies. The same trend was seen for the ratio of Methanosarcina mcrA to the general mcrA gene and transcript copies, while no such effects could be seen for the ratio of Methanocella to total 16S rRNA gene and mcrA gene and transcript copies (All tests P>0.24).

Bottom Line: Methanogenesis is traditionally thought to occur only in highly reduced, anoxic environments.Since methanotrophs were not detectable in the BSC, all the methane produced was released into the atmosphere.Our findings point to a formerly unknown participation of desert soils in the global methane cycle.

View Article: PubMed Central - PubMed

Affiliation: Max-Planck-Institute for Terrestrial Microbiology, Marburg, Germany.

ABSTRACT
Methanogenesis is traditionally thought to occur only in highly reduced, anoxic environments. Wetland and rice field soils are well known sources for atmospheric methane, while aerated soils are considered sinks. Although methanogens have been detected in low numbers in some aerated, and even in desert soils, it remains unclear whether they are active under natural oxic conditions, such as in biological soil crusts (BSCs) of arid regions. To answer this question we carried out a factorial experiment using microcosms under simulated natural conditions. The BSC on top of an arid soil was incubated under moist conditions in all possible combinations of flooding and drainage, light and dark, air and nitrogen headspace. In the light, oxygen was produced by photosynthesis. Methane production was detected in all microcosms, but rates were much lower when oxygen was present. In addition, the δ(13)C of the methane differed between the oxic/oxygenic and anoxic microcosms. While under anoxic conditions methane was mainly produced from acetate, it was almost entirely produced from H(2)/CO(2) under oxic/oxygenic conditions. Only two genera of methanogens were identified in the BSC-Methanosarcina and Methanocella; their abundance and activity in transcribing the mcrA gene (coding for methyl-CoM reductase) was higher under anoxic than oxic/oxygenic conditions, respectively. Both methanogens also actively transcribed the oxygen detoxifying gene catalase. Since methanotrophs were not detectable in the BSC, all the methane produced was released into the atmosphere. Our findings point to a formerly unknown participation of desert soils in the global methane cycle.

Show MeSH
Related in: MedlinePlus