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      Methane emission induced by short-chain organic acids in lowland soil

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          Abstract

          ABSTRACT Methane (CH4) is the second major greenhouse gas after CO2, exerting a significant influence on the climate and the chemistry of the atmosphere. In lowland soil, acetate and H2/CO2 are the most important precursors of CH4 and formed from organic matter fermentation in an anaerobic environment, giving rise to short-chain organic acids (ethanoic, propanoic, and butanoic), depending on the type of crop residue and the soil management system. Ethanoic acid can be directly converted to CH4 by methanogenic microorganisms, but propanoic and butanoic acids must be converted to acetate before being converted to CH4. This study aimed to quantify, in isolation, the dynamics and CH4 emission potential of the three short-chain organic acids found in flooded lowland soils with rice crops. The study was carried out in a controlled environment using four standard carbon doses (0, 90, 180, and 270 mg kg−1) of ethanoic, propanoic, and butanoic acids. The dynamics and the potential emission of CH4 from soil were investigated when the acids were applied to flooded soil previously incubated for 20 days. The CH4 emission dynamics were altered with the application of the three short-chain organic acids to the soil, even using an equal amount of carbon. The faster and more intense emission was achieved with the ethanoic acid application in relation to the other two acids application, while butanoic acid presents slower, delayed, and prolonged dynamics of CH4 emission. Propanoic acid resulted in the lowest CH4 emission due to its own stoichiometry and the temperature condition in which the experiment was conducted, which were unfavorable to the hydrogenotrophic bacteria. The addition of short-chain organic acids promoted a priming effect in the soil with conversion values of C to CH4 above the calculated theoretical values.

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          Methane fluxes show consistent temperature dependence across microbial to ecosystem scales.

          Methane (CH4) is an important greenhouse gas because it has 25 times the global warming potential of carbon dioxide (CO2) by mass over a century. Recent calculations suggest that atmospheric CH4 emissions have been responsible for approximately 20% of Earth's warming since pre-industrial times. Understanding how CH4 emissions from ecosystems will respond to expected increases in global temperature is therefore fundamental to predicting whether the carbon cycle will mitigate or accelerate climate change. Methanogenesis is the terminal step in the remineralization of organic matter and is carried out by strictly anaerobic Archaea. Like most other forms of metabolism, methanogenesis is temperature-dependent. However, it is not yet known how this physiological response combines with other biotic processes (for example, methanotrophy, substrate supply, microbial community composition) and abiotic processes (for example, water-table depth) to determine the temperature dependence of ecosystem-level CH4 emissions. It is also not known whether CH4 emissions at the ecosystem level have a fundamentally different temperature dependence than other key fluxes in the carbon cycle, such as photosynthesis and respiration. Here we use meta-analyses to show that seasonal variations in CH4 emissions from a wide range of ecosystems exhibit an average temperature dependence similar to that of CH4 production derived from pure cultures of methanogens and anaerobic microbial communities. This average temperature dependence (0.96 electron volts (eV)), which corresponds to a 57-fold increase between 0 and 30°C, is considerably higher than previously observed for respiration (approximately 0.65 eV) and photosynthesis (approximately 0.3 eV). As a result, we show that both the emission of CH4 and the ratio of CH4 to CO2 emissions increase markedly with seasonal increases in temperature. Our findings suggest that global warming may have a large impact on the relative contributions of CO2 and CH4 to total greenhouse gas emissions from aquatic ecosystems, terrestrial wetlands and rice paddies.
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            Effects of volatile fatty acid concentrations on methane yield and methanogenic bacteria

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              Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils.

              The possibility that Methanothrix (formerly Methanosaeta) and Geobacter species cooperate via direct interspecies electron transfer (DIET) in terrestrial methanogenic environments was investigated in rice paddy soils. Genes with high sequence similarity to the gene for the PilA pilin monomer of the electrically conductive pili (e-pili) of Geobacter sulfurreducens accounted for over half of the PilA gene sequences in metagenomic libraries and 42% of the mRNA transcripts in RNA sequencing (RNA-seq) libraries. This abundance of e-pilin genes and transcripts is significant because e-pili can serve as conduits for DIET. Most of the e-pilin genes and transcripts were affiliated with Geobacter species, but sequences most closely related to putative e-pilin genes from genera such as Desulfobacterium, Deferribacter, Geoalkalibacter, and Desulfobacula, were also detected. Approximately 17% of all metagenomic and metatranscriptomic bacterial sequences clustered with Geobacter species, and the finding that Geobacter spp. were actively transcribing growth-related genes indicated that they were metabolically active in the soils. Genes coding for e-pilin were among the most highly transcribed Geobacter genes. In addition, homologs of genes encoding OmcS, a c-type cytochrome associated with the e-pili of G. sulfurreducens and required for DIET, were also highly expressed in the soils. Methanothrix species in the soils highly expressed genes for enzymes involved in the reduction of carbon dioxide to methane. DIET is the only electron donor known to support CO2 reduction in Methanothrix Thus, these results are consistent with a model in which Geobacter species were providing electrons to Methanothrix species for methane production through electrical connections of e-pili.IMPORTANCEMethanothrix species are some of the most important microbial contributors to global methane production, but surprisingly little is known about their physiology and ecology. The possibility that DIET is a source of electrons for Methanothrix in methanogenic rice paddy soils is important because it demonstrates that the contribution that Methanothrix makes to methane production in terrestrial environments may extend beyond the conversion of acetate to methane. Furthermore, defined coculture studies have suggested that when Methanothrix species receive some of their energy from DIET, they grow faster than when acetate is their sole energy source. Thus, Methanothrix growth and metabolism in methanogenic soils may be faster and more robust than generally considered. The results also suggest that the reason that Geobacter species are repeatedly found to be among the most metabolically active microorganisms in methanogenic soils is that they grow syntrophically in cooperation with Methanothrix spp., and possibly other methanogens, via DIET.
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                Author and article information

                Contributors
                Role: ND
                Role: ND
                Role: ND
                Role: ND
                Role: ND
                Role: ND
                Role: ND
                Journal
                rbcs
                Revista Brasileira de Ciência do Solo
                Rev. Bras. Ciênc. Solo
                Sociedade Brasileira de Ciência do Solo (Viçosa, MG, Brazil )
                1806-9657
                2019
                : 43
                : e0180252
                Affiliations
                [1] Santa Maria Rio Grande do Sul orgnameUniversidade Federal de Santa Maria orgdiv1Departamento de Solos orgdiv2Programa de Pós-Graduação em Ciência do Solo Brazil
                [2] Santa Maria Rio Grande do Sul orgnameUniversidade Federal de Santa Maria orgdiv1Departamento de Solos Brazil
                [3] Santa Maria Rio Grande do Sul orgnameUniversidade Federal de Santa Maria Brazil
                Article
                S0100-06832019000100412
                10.1590/18069657rbcs20180252
                5c0d3f4d-7e3e-4fc9-a6cb-58fe371df400

                This work is licensed under a Creative Commons Attribution 4.0 International License.

                History
                : 27 August 2019
                : 03 December 2018
                Page count
                Figures: 0, Tables: 0, Equations: 0, References: 48, Pages: 0
                Product

                SciELO Brazil

                Categories
                Division - Soil Processes and Properties

                methanogenesis,irrigated rice,ethanoic acid,butanoic acid,propanoic acid

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