Removal of atmospheric methane by soil ecosystems and its controlling variables from microbial to global scales

Methane(CH4),a potent greenhouse gas,plays a pivotal role in the dynamics of climate change.While CH4emissions have been widely investigated,biological removal of CH4by upland soils has been less explored.Understanding the mechanisms and factors affecting CH4oxidation in soils is of paramount importance for devising successful mitigation strategies.This perspective paper discusses different types of aerobic methanotrophs and their activities under varying environmental conditions,highlighting the significant contribution of soil ecosystems to global CH4sinks.We emphasize the need for in-depth research on variables controlling CH4sinks on different spatiotemporal scales and the exploration of previously unidentified CH4sinks,such as deserts and areas of glacier retreat.

Methane(CH4),as the second most abundant anthropogenic greenhouse gas,exhibits radiative strength approximately 30 times greater than carbon dioxide (CO2) on a molar basis (IPCC,2021).Its substantial greenhouse effect,shorter half-life,and relatively easier controllability have spurred extensive efforts to comprehend its dynamics and develop effective mitigation strategies(Neubauer and Megonigal,2015;Balcombeet al.,2018).While natural sources of CH4emissions from soil ecosystems have been well studied,soil CH4sinks,particularly those mediated by methanotrophic bacteria,remain relatively less explored.This perspective paper aims to provide an overview of the current understanding of atmospheric CH4oxidation in soils,with a focus on the role of aerobic methanotrophs and the factors influencing their activity.

While natural sources of CH4from soil ecosystems have been widely addressed,soil CH4sinks have been less explored(Kirschkeet al.,2013;Murguia-Floreset al.,2018).Approximately 5%-10%of global CH4sinks are attributed to soil uptake mediated by aerobic methanotrophs(Le Mer and Roger,2001;Kirschkeet al.,2013).Methanotrophs,autotrophic bacteria capable of oxidizing CH4,are classified into three types,type I,type II,and type X,based on their morphology,membrane structure,carbon assimilation pathways,and 16S rRNA sequences(Hanson and Hanson,1996).Type I and Type II methanotrophs display distinct affinities for CH4concentration:Type II methanotrophs are proficient in oxidizing low-concentration CH4,while Type I methanotrophs are prevalent in high-concentration CH4environments,such as wetlands and water-flooded ecosystems (Grahamet al.,1993;Mohantyet al.,2006).The upland soil cluster methanotrophs are a specific group of methanotrophs that are particularly prevalent in upland nonwaterlogged soils and are responsible for soil CH4sinks(Kniefet al.,2003).Methanotrophs are categorized into high-and low-affinity types as well.High-affinity methanotrophs are adapted to oxidizing CH4at low concentrations,while low-affinity methanotrophs are suited for higher CH4concentrations(Reay and Nedwell,2004;Singhet al.,2010).Typically,soils display oxidation characteristics of both high and low affinities,with a transition from high-affinity to lowaffinity CH4oxidation occurring between 100 and 1 000 mL L-1CH4(Bender and Conrad,1992).

The amount of CH4oxidized and removed from the atmosphere is estimated to be between 11 and 49 Tg year-1on a global scale (Saunoiset al.,2020).Among various ecosystems,forests account for about 60%of the terrestrial removal,followed by grasslands (Kirschkeet al.,2013;Zhuanget al.,2013).However,previous models estimated the global forest CH4sink to range from 9 to 24 Tg CH4year-1with significant uncertainties (Curry,2007;Dutaur and Verchot,2007;Murguia-Floreset al.,2018),This uncertainty is likely attributed to our limited understanding of the primary variables controlling soil CH4sinks and their underlying mechanisms,with only a few modeling attempts having been made (Sabrekovet al.,2016;Murguia-Floreset al.,2021).This large uncertainty highlights the need for further investigations to understand the role of unidentified CH4sinks in the global CH4budget.

Accurate estimation of atmospheric CH4oxidation rates in ecosystems is vital,and several key controlling variables have been identified for CH4oxidation in soils,including CH4concentration,soil temperature,and soil moisture(Janget al.,2011;Zhenget al.,2018).Temperature and water concentration directly influence CH4oxidation rates by affecting microbial activity and gas diffusivity,respectively(Janget al.,2011;Zhenget al.,2018).Additionally,spatiotemporal variations in CH4oxidation rates are influenced by factors such as precipitation amount and intensity,winter snowpack depth,and soil texture and porosity (Castroet al.,1995;Fanget al.,2010;Festet al.,2017).For instance,tropical forest soils take up less CH4than temperate forest soils,likely due to higher soil moisture resulting from increased precipitation(Gaticaet al.,2020).A meta-analysis revealed that forests exhibit a CH4uptake rate three times higher than grasslands,a phenomenon attributed to differences in soil physical structure and methanotrophic communities(Yuet al.,2017).Furthermore,natural ecosystems,such as forests and grasslands,take up more CH4than agricultural soils (Malghaniet al.,2016).Land use intensity can significantly reduce potential methanotrophic activity by approximately 40%,with fertilizers inhibiting methanotrophic activity(Täumeret al.,2021).Temporal variation in CH4sinks within terrestrial ecosystems are influenced by temperature (Janget al.,2011).Yet,methanotrophic activity exhibits lesser temperature sensitivity compared to methanogenesis,suggesting that factors such as soil moisture might predominantly dictate the temporal or seasonal variations of CH4sinks,rather than solely soil temperature(Fanet al.,2022).The effects of inorganic nutrients,particularly nitrogen (e.g.,and),have drawn attention as potential controlling variables for CH4oxidation in soils,although conflicting influences have been noted(Kanget al.,2022).For example,excessive nitrogen was noted to inhibit CH4oxidation in Arctic soils(Leeet al.,2023b),suggesting the previously unidentified effect of inorganic nitrogen on CH4dynamics.Recent studies have underscored the role of soil organic matter in determining CH4oxidation rates in forest ecosystems at both ecosystem and global levels(Leeet al.,2023a),highlighting the significance of a stable carbon supply from primary producers to maximize CH4oxidation in forest soils by promoting interaction between heterotrophic microorganisms and methanotrophs.

This perspective paper identifies critical knowledge gaps and research directions to enhance our understanding of CH4oxidation in soils.Urgent attention is needed for investigating CH4oxidation in arid and semiarid regions,which account for nearly 40%of the land surface,but have generally been overlooked in the context of the global carbon cycle.The lack of information in these regions is attributed to low primary productivity and perceived minor microbial activities compared to other ecosystems.Furthermore,logistic diffi-culties and distance from the main scientific institutes hinder the acquisition of data from these areas.However,recent controversies surrounding CO2uptake rates in arid regions emphasize the necessity to revisit current global models,which assume negligible CH4uptake in arid regions(Evanset al.,2014).Potential methanotrophic activity has been observed in the soil of the Atacama Desert,a hyperarid region often called a Mars-like environment(Hallet al.,2012).The discovery ofMethylobacteriumsp.in the Atacama Desert further provides evidence of CH4sink capacity of extremely arid regions (Warren-Rhodeset al.,2019).Moreover,the presence of methanotrophs and their activities in areas with soil biological crusts warrant extensive surveying(Ghiloufiet al.,2019),as these regions could potentially function as significant hotspots for CH4oxidation.

Secondly,the impact of rapid warming in Arctic and polar ecosystems on CH4oxidation,particularly in regions experiencing glacier retreat,requires in-depth assessment.Melting surface glaciers can expose new land surfaces,harboring various microbes,including methanotrophs,capable of expanding CH4sinks.While some studies have touched upon this phenomenon(Yunet al.,2023),a comprehensive and accurate assessment of the effect of glacier retreat on CH4oxidation remains to be conducted,considering the rapid rise in Arctic temperature.

Thirdly,urban green spaces,which host more than 50%of the human population,have garnered significant attention for their ecological potential(Derkzenet al.,2015;Veerkampet al.,2021).However,the effects of urban green spaces on CH4oxidation in soils have not been extensively explored.With urban forests displaying substantial carbon storage,there is significant potential for CH4oxidation in such areas.

Finally,refining methodology for CH4oxidation rates deserves further attention from soil scientists.Existing methods,such as the static chamber method coupled with gas chromatography equipped with FID detector and molecular biology-based approaches targetingpmoAgenes,have their respective merits and limitations.In particular,while lowaffinity methanotrophs have been investigated to some extent,significant progress is still needed in the identification and quantitative analysis of high-affinity methanotrophs-also referred to as upland clusters-to fully understand their community in soils(Guerrero-Cruzet al.,2021).Incorporating multiple approaches and conducting comparative studies will enrich scientific understanding of CH4oxidation processes.

This paper highlights the intricate processes of CH4oxidation in soils,emphasizing the pivotal role of methanotrophs and the significance of controlling variables in harnessing CH4sinks.Addressing knowledge gaps in poorly explored regions,particularly arid and semiarid areas,polar ecosystems,and urban green spaces,is essential for a holistic understanding of CH4sinks on a global scale.Additionally,methodological advancements will contribute to accurate estimation of CH4oxidation rates,ultimately aiding in the development of effective strategies to mitigate CH4emissions.

ACKNOWLEDGEMENT

We acknowledge the support from the Ministry of Environment of Korea(Nos.2022003640002 and RS-2023-00232066).