Temperature sensitivity of anaerobic methane oxidation versus methanogenesis in paddy soil: Implications for the CH₄ balance under global warming

Abstract

The global methane (CH 4 ) budget is based on a sensitive balance between methanogenesis and CH 4 oxidation (aerobic and anaerobic). The response of these processes to climate warming, however, is not quantified. This largely reflects our lack of knowledge about the temperature sensitivity (Q 10 ) of the anaerobic oxidation of CH 4 (AOM)-a ubiquitous process in soils. Based on a 13 CH 4 labeling experiment, we determined the rate, Q 10 and activation energy of AOM and of methanogenesis in a paddy soil at three temperatures (5, 20, 35°C). The rates of AOM and of methanogenesis increased exponentially with temperature, whereby the AOM rate was significantly lower than methanogenesis. Both the activation energy and Q 10 of AOM dropped significantly from 5-20 to 20-35°C, indicating that AOM is a highly temperaturedependent microbial process. Nonetheless, the Q 10 of AOM and of methanogenesis were similar at 5-35°C, implying a comparable temperature dependence of AOM and methanogenesis in paddy soil. The continuous increase of AOM Q 10 over the 28-day experiment reflects the successive utilization of electron acceptors according to their thermodynamic efficiency. The basic constant for Q 10 of AOM was calculated to be 0.1 units for each 3.2 kJ mol −1 increase of activation energy. We estimate the AOM in paddy soils to consume 2.2~5.5 Tg CH 4 per year on a global scale. Considering these results in conjunction with literature data, the terrestrial AOM in total consumes ~30% of overall CH 4 production. Our data corroborate a similar Q 10 of AOM and methanogenesis. As the rate of AOM in paddy soils is lower than methanogenesis, however, it will not fully compensate for an increased methane production under climate warming.

Significance of anaerobic oxidation of methane (AOM) in mitigating methane emission from major natural and anthropogenic sources: a review of AOM rates in recent publications

“…It must be noted that the estimated 75% percentiles based on rates measured under ideal conditions may not be reached during rice cultivation due to the limitation caused by methanogenesis (oen not a limiting factor in lab-scale incubations). The lower end of the currently estimated methane oxidation via AOM is close to the estimated values from a recent publication, 97 55 DAMO was found to be a major AOM pathway in freshwater ecosystems. 106,107 AOM driven by other electron acceptors has also been reported.…”

“…It must be noted that the estimated 75% percentiles based on rates measured under ideal conditions may not be reached during rice cultivation due to the limitation caused by methanogenesis (often not a limiting factor in lab-scale incubations). The lower end of the currently estimated methane oxidation via AOM is close to the estimated values from a recent publication, 97 2.2–5.5 Tg CH 4 per year. Regarding methane emission, the recently estimated efflux from paddy fields in the 2008–2017 decade is 30 [min–max: 25–38] Tg CH 4 per year 1 or 29.9 [Q1–Q3, 24.9–32.1] Tg CH 4 per year, 55 which are comparable.…”

“…4,31,83 The AOM rate reects the activities of local microbiota, which are under the control of multiple environmental factors. In addition to the availability of methane and a suitable electron acceptor, other environmental factors, such as temperature, 97,216 pressure, 171,181,216,240 accessibility of essential metal ions, 241 the turnover rate of electron acceptors, 200 organic content, 172,175 etc., have all been documented to affect the AOM rate. It seems that no straightforward model can explain all the observations across different environments due to the different concentrations/levels of these above factors.…”

“…85,89 For example, in rice paddy soil from the Yangtze River Plain, China, a high abundance of DAMO bacteria (8.5 Â 10 7 to 1.0 Â 10 8 copies per g dry soil) was detected in 60-140 cm soil core sections in the summertime and all soil core sections from 40 cm down to 200 cm in wintertime. 90 The reported AOM rates in paddy soils are from 0.2 to 79.9 nmol CO 2 g À1 d À1 (median ¼ 1.9 nmol CO 2 g À1 d À1 and Q1-Q3: 0.6-9.4 nmol CH 4 g À1 d À1 ; rates from bioreactors using paddy soils as inocula were excluded) 85,86,93,94,[96][97][98] (Fig. 5).…”

Opposing seasonal temperature dependencies of CO2 and CH4 emissions from wetlands

“…Different temperature dependencies of CO 2 and CH 4 emissions within a 1‐year cycle might be expected. The temperature dependence of CO 2 emissions usually decreases with temperature increase (Davidson & Janssens, 2006; Li, Pei, et al, 2020); an opposite pattern might be expected for the temperature dependence of CH 4 emissions because the temperature dependence of CH 4 production is usually higher than that of CH 4 oxidation (Chang et al, 2019) with the temperature dependence of CH 4 oxidation being observed to decline significantly with increasing temperatures but not for that of methanogenesis (Fan et al, 2022) and because the capacity of below‐ground stored CH 4 decreases with increasing temperatures (Sieczko et al, 2020). Additionally, changes in soil hydrology have been reported having no significant effect on the temperature dependence of CO 2 emissions but temperature dependence of CH 4 emissions increased with increasing water table depths (WTDs) (Chen et al, 2021).…”