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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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Stable carbon isotope signature (δ13C) of the CO2 and the newly formed methane in the microcosm headspaces (see Methods): means±1 SE; n = 3.Isolines represent different apparent fractionation factors (εapp; eq.3). “Strictly anoxic” refers only to the anoxic microcosms in the dark while “oxic/oxygenic” refers to all the rest. The arrow in the “strictly anoxic” ellipse points to the direction of temporal development (d7 and d14 Refer to day 7 and 14th resp.). 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-g004: Stable carbon isotope signature (δ13C) of the CO2 and the newly formed methane in the microcosm headspaces (see Methods): means±1 SE; n = 3.Isolines represent different apparent fractionation factors (εapp; eq.3). “Strictly anoxic” refers only to the anoxic microcosms in the dark while “oxic/oxygenic” refers to all the rest. The arrow in the “strictly anoxic” ellipse points to the direction of temporal development (d7 and d14 Refer to day 7 and 14th resp.). Treatment codes are as follows: flooded-F, wet-drained-W, light-L, dark-D, N2 headspace-N, air (21% O2) headspace-O.

Mentions: We also analyzed the stable isotope signature of the carbon in methane and CO2 (13C:12C) to decipher the proportional contribution of different methanogenic pathways [3]. Our analysis of isotopic signatures (Figure 4) revealed two distinct clusters: the strictly anoxic microcosms had δ13C-nCH4 (isotopic signature of the newly formed methane) average values of −63‰ in the first week of incubation, an average of −35‰ throughout the rest of the incubation period, and δ13C-CO2 values of −16 to −7‰. The oxic/oxygenic microcosms showed lighter isotopic signatures with average δ13C values of −75‰ and −20‰ for methane and CO2, respectively, which were stable over time. The difference between the isotopic signatures of the CO2 in the two clusters (Figure 4) can be related to the difference in the signature of the organic carbon and the carbonate reservoir in the soil, which constituted up to 34% of the soil mass [20]. The δ13C of carbonate (−4.09‰) was heavier than that of organic carbon (−20.5‰). In the oxic/oxygenic microcosms CO2 was probably produced only from organic matter. However, in the anoxic microcosms, the CO2 was probably also generated from the carbonate. The contribution of carbonate may be attributed to the release of CO2 from the reaction of the calcium carbonate in the soil with acids, which are associated with anaerobic degradation processes (Table S3).


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

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

Stable carbon isotope signature (δ13C) of the CO2 and the newly formed methane in the microcosm headspaces (see Methods): means±1 SE; n = 3.Isolines represent different apparent fractionation factors (εapp; eq.3). “Strictly anoxic” refers only to the anoxic microcosms in the dark while “oxic/oxygenic” refers to all the rest. The arrow in the “strictly anoxic” ellipse points to the direction of temporal development (d7 and d14 Refer to day 7 and 14th resp.). 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-g004: Stable carbon isotope signature (δ13C) of the CO2 and the newly formed methane in the microcosm headspaces (see Methods): means±1 SE; n = 3.Isolines represent different apparent fractionation factors (εapp; eq.3). “Strictly anoxic” refers only to the anoxic microcosms in the dark while “oxic/oxygenic” refers to all the rest. The arrow in the “strictly anoxic” ellipse points to the direction of temporal development (d7 and d14 Refer to day 7 and 14th resp.). Treatment codes are as follows: flooded-F, wet-drained-W, light-L, dark-D, N2 headspace-N, air (21% O2) headspace-O.
Mentions: We also analyzed the stable isotope signature of the carbon in methane and CO2 (13C:12C) to decipher the proportional contribution of different methanogenic pathways [3]. Our analysis of isotopic signatures (Figure 4) revealed two distinct clusters: the strictly anoxic microcosms had δ13C-nCH4 (isotopic signature of the newly formed methane) average values of −63‰ in the first week of incubation, an average of −35‰ throughout the rest of the incubation period, and δ13C-CO2 values of −16 to −7‰. The oxic/oxygenic microcosms showed lighter isotopic signatures with average δ13C values of −75‰ and −20‰ for methane and CO2, respectively, which were stable over time. The difference between the isotopic signatures of the CO2 in the two clusters (Figure 4) can be related to the difference in the signature of the organic carbon and the carbonate reservoir in the soil, which constituted up to 34% of the soil mass [20]. The δ13C of carbonate (−4.09‰) was heavier than that of organic carbon (−20.5‰). In the oxic/oxygenic microcosms CO2 was probably produced only from organic matter. However, in the anoxic microcosms, the CO2 was probably also generated from the carbonate. The contribution of carbonate may be attributed to the release of CO2 from the reaction of the calcium carbonate in the soil with acids, which are associated with anaerobic degradation processes (Table S3).

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