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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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Methane production in the microcosms throughout the incubation.A. Accumulation of CH4 in the microcosm headspaces B. mean production rate per day: means±1 SE; n = 3. Treatment codes are as follows: flooded-F, wet-drained-W, light-L, dark-d, N2 headspace-N, air (21% O2) headspace-O.
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pone-0020453-g001: Methane production in the microcosms throughout the incubation.A. Accumulation of CH4 in the microcosm headspaces B. mean production rate per day: means±1 SE; n = 3. Treatment codes are as follows: flooded-F, wet-drained-W, light-L, dark-d, N2 headspace-N, air (21% O2) headspace-O.

Mentions: Methane was detectable in the headspace of all microcosms seven days after the start of the experiment and it continuously accumulated throughout the incubation, regardless of treatment (Figure 1A). The lag in the methane detection can be due to the time it takes for oxygen, and potentially other alternative electron acceptors, to be depleted and/or to the recovery and growth of the methanogenic population. A strong, two orders of magnitude, difference in the methanogenic activity was seen between the oxic and the anoxic microcosms incubated in the dark. These anoxic treatments-FDN and WDN-accumulated methane at a rate of 3800±400 and 1500±400 nmol gdw−1 d−1, respectively, while the parallel oxic treatments-FDO and WDO-accumulated methane at a rate of 41.6±12.4 and 9.2±4.3 nmol gdw−1 d−1, respectively (Figure 1B, Table S1). The microcosms incubated in the light showed similar methane production rates to the dark oxic microcosms (21.7±3.7 nmol gdw−1 d−1 on average), and indeed methane production rates between these treatments were not significantly different, indicating no apparent effect of initial oxygen levels (P = 0.66 in a t-test).


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

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

Methane production in the microcosms throughout the incubation.A. Accumulation of CH4 in the microcosm headspaces B. mean production rate per day: means±1 SE; n = 3. Treatment codes are as follows: flooded-F, wet-drained-W, light-L, dark-d, N2 headspace-N, air (21% O2) headspace-O.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0020453-g001: Methane production in the microcosms throughout the incubation.A. Accumulation of CH4 in the microcosm headspaces B. mean production rate per day: means±1 SE; n = 3. Treatment codes are as follows: flooded-F, wet-drained-W, light-L, dark-d, N2 headspace-N, air (21% O2) headspace-O.
Mentions: Methane was detectable in the headspace of all microcosms seven days after the start of the experiment and it continuously accumulated throughout the incubation, regardless of treatment (Figure 1A). The lag in the methane detection can be due to the time it takes for oxygen, and potentially other alternative electron acceptors, to be depleted and/or to the recovery and growth of the methanogenic population. A strong, two orders of magnitude, difference in the methanogenic activity was seen between the oxic and the anoxic microcosms incubated in the dark. These anoxic treatments-FDN and WDN-accumulated methane at a rate of 3800±400 and 1500±400 nmol gdw−1 d−1, respectively, while the parallel oxic treatments-FDO and WDO-accumulated methane at a rate of 41.6±12.4 and 9.2±4.3 nmol gdw−1 d−1, respectively (Figure 1B, Table S1). The microcosms incubated in the light showed similar methane production rates to the dark oxic microcosms (21.7±3.7 nmol gdw−1 d−1 on average), and indeed methane production rates between these treatments were not significantly different, indicating no apparent effect of initial oxygen levels (P = 0.66 in a t-test).

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