Earthworms and warming alter methane uptake and methane-cycling microbial community in meadow soil

Abstract

● Earthworms significantly reduced soil CH₄ uptake at both temperatures, and warming significantly promoted soil CH₄ uptake.

● Earthworms significantly altered methanotroph community, and warming significantly altered methanogen community, and their interaction had a significant influence on both methanogen and methanotroph communities.

● Soil properties exhibited a negative impact on CH₄ uptake, while the α-diversity of methanotrophs was associated with enhanced CH₄ uptake.

● Dissolved organic carbon (DOC) was identified as the most essential factor in forecasting soil CH₄ uptake.

The function and service of biologically driven ecosystems are undergoing significant changes due to climate warming. Earthworms play a crucial role as soil engineer by modulating the effects of climate change on soil nutrient cycle through alterations to biotic and abiotic soil conditions. However, there is currently a scarcity of information regarding the impacts of earthworms and warming on soil CH₄ uptake and their associated microbial mechanisms. This study conducted a 61-day microcosm experiment to investigate the impact of warming (temperature rise from 14.2 °C to 17.2 °C) and the presence of earthworms (Eisenia fetida and Moniligaster japonicus) on soil CH₄ uptake. We employed gas chromatography and high-throughput sequencing to investigate the fluctuations in soil CH₄ uptake and the microbial communities involved in methane cycling. Compared to low temperature conditions (14.2 °C), we observed that warming significantly increased soil CH₄ uptake in all treatments (non-earthworm: 51.85%; Eisenia fetida: 50.88%; Moniligaster japonicus: 71.78%). Both Eisenia fetida and Moniligaster japonicus significantly reduced soil CH₄ uptake at two temperatures compared to the non-earthworm treatment. Nevertheless, no significant impacts were found on soil CH₄ uptake due to the interactions between earthworms and warming. The methanotroph communities exhibited notable variations among earthworm treatments, whereas the methanogenic communities displayed significant differences among temperature treatments. The interaction between earthworm and warming also resulted in noticeable variations in both methanogenic and methanotrophic communities. The FAPROTAX analysis revealed that earthworms and warming altered relative abundance of methanogens and methanotroph associated with CH₄ cycle functions. Soil properties exhibited a negative impact on CH₄ uptake, with DOC identified as the most crucial variable in predicting soil CH₄ uptake, while the α-diversity of methanotrophs was associated with enhanced CH₄ uptake. This study emphasized the crucial role of soil fauna in adjusting soil greenhouse gas emissions under the context of global warming.

Graphical abstract

Keywords

endogeic earthworms / epigeic earthworms / greenhouse gas emissions / Illumina sequencing / network analysis

References

[1] Bastian, M., Heymann, S., Jacomy, M., 2009. Gephi: an open source software for exploring and manipulating networks. In: Proceedings of International AAAI Conference on Weblogs and Social Media. San Jose: AAAI, 361–362.

[2] Bates, S.T., Clemente, J.C., Flores, G.E., Walters, W.A., Parfrey, L.W., Knight, R., Fierer, N., 2013. Global biogeography of highly diverse protistan communities in soil. ISME Journal7, 652–659.

[3] Berry, D., Widder, S., 2014. Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Frontiers in Microbiology5, 219.

[4] Bertrand, M., Barot, S., Blouin, M., Whalen, J., De Oliveira, T., Roger-Estrade, J., 2015. Earthworm services for cropping systems. A review. Agronomy for Sustainable Development35, 553–567.

[5] Blouin, M., Lavelle, P., Laffray, D., 2007. Drought stress in rice (Oryza sativa L. ) is enhanced in the presence of the compacting earthworm Millsonia anomala. Environmental and Experimental Botany60, 352–359.

[6] Bradley, R.L., Chroňáková, A., Elhottová, D., Šimek, M., 2012. Interactions between land-use history and earthworms control gross rates of soil methane production in an overwintering pasture. Soil Biology and Biochemistry53, 64–71.

[7] Chen, C., Whalen, J.K., 2016. Earthworm interactions with denitrifying bacteria are scale-dependent: evidence from physiological to riparian ecosystem scales. Basic and Applied Ecology17, 1–10.

[8] Christiansen, J.R., Romero, A.J.B., Jørgensen, N.O.G., Glaring, M.A., Jørgensen, C.J., Berg, L.K., Elberling, B., 2015. Methane fluxes and the functional groups of methanotrophs and methanogens in a young Arctic landscape on Disko Island, West Greenland. Biogeochemistry122, 15–33.

[9] Clause, J., Barot, S., Richard, B., Decaëns, T., Forey, E., 2014. The interactions between soil type and earthworm species determine the properties of earthworm casts. Applied Soil Ecology83, 149–158.

[10] Das, S., Ganguly, D., Chakraborty, S., Mukherjee, A., De, T.K., 2018. Methane flux dynamics in relation to methanogenic and methanotrophic populations in the soil of Indian Sundarban mangroves. Marine Ecology39, e12493.

[11] Deng, Y.C., Liu, Y.Q., Dumont, M., Conrad, R., 2017. Salinity affects the composition of the aerobic methanotroph community in Alkaline Lake Sediments from the Tibetan Plateau. Microbial Ecology73, 101–110.

[12] Depkat-Jakob, P.S., Brown, G.G., Tsai, S.M., Horn, M.A., Drake, H.L., 2013. Emission of nitrous oxide and dinitrogen by diverse earthworm families from Brazil and resolution of associated denitrifying and nitrate-dissimilating taxa. FEMS Microbiology Ecology83, 375–391.

[13] Depkat-Jakob, P.S., Hunger, S., Schulz, K., Brown, G.G., Tsai, S.M., Drake, H.L., 2012. Emission of methane by Eudrilus eugeniae and other earthworms from brazil. Applied and Environmental Microbiology78, 3014–3019.

[14] Dijkstra, F.A., Morgan, J.A., Von Fischer, J.C., Follett, R.F., 2011. Elevated CO₂ and warming effects on CH₄ uptake in a semiarid grassland below optimum soil moisture. Journal of Geophysical Research: Biogeosciences116, G01007.

[15] Duc, N.T., Crill, P., Bastviken, D., 2010. Implications of temperature and sediment characteristics on methane formation and oxidation in lake sediments. Biogeochemistry100, 185–196.

[16] Eisenhauer, N., Fisichelli, N.A., Frelich, L.E., Reich, P.B., 2012. Interactive effects of global warming and 'global worming' on the initial establishment of native and exotic herbaceous plant species. Oikos121, 1121–1133.

[17] Fang, C., Ke, W.B., Campioli, M., Pei, J.Y., Yuan, Z.Q., Song, X., Ye, J.S., Li, F.M., Janssens, I.A., 2020. Unaltered soil microbial community composition, but decreased metabolic activity in a semiarid grassland after two years of passive experimental warming. Ecology and Evolution10, 12327–12340.

[18] Fox, O., Vetter, S., Ekschmitt, K., Wolters, V., 2006. Soil fauna modifies the recalcitrance-persistence relationship of soil carbon pools. Soil Biology and Biochemistry38, 1353–1363.

[19] Galbally, I.E., Kirstine, W.V., Meyer, C.P., Wang, Y.P., 2008. Soil-atmosphere trace gas exchange in semiarid and arid zones. Journal of Environmental Quality37, 599–607.

[20] Girkin, N.T., Vane, C.H., Cooper, H.V., Moss-Hayes, V., Craigon, J., Turner, B.L., Ostle, N., Sjögersten, S., 2019. Spatial variability of organic matter properties determines methane fluxes in a tropical forested peatland. Biogeochemistry142, 231–245.

[21] Gunderson, C.A., Edwards, N.T., Walker, A.V., O'Hara, K.H., Campion, C.M., Hanson, P.J., 2012. Forest phenology and a warmer climate - growing season extension in relation to climatic provenance. Global Change Biology18, 2008–2025.

[22] Gweon, H.S., Bowes, M.J., Moorhouse, H.L., Oliver, A.E., Bailey, M.J., Acreman, M.C., Read, D.S., 2021. Contrasting community assembly processes structure lotic bacteria metacommunities along the river continuum. Environmental Microbiology23, 484–498.

[23] Hallam, J., Hodson, M.E., 2020. Impact of different earthworm ecotypes on water stable aggregates and soil water holding capacity. Biology and Fertility of Soils56, 607–617.

[24] Hart, S.C., 2006. Potential impacts of climate change on nitrogen transformations and greenhouse gas fluxes in forests: a soil transfer study. Global Change Biology12, 1032–1046.

[25] Horton, D.J., Theis, K.R., Uzarski, D.G., Learman, D.R., 2019. Microbial community structure and microbial networks correspond to nutrient gradients within coastal wetlands of the laurentian great lakes. FEMS Microbiology Ecology95, fiz033.

[26] Hoyos-Santillan, J., Lomax, B.H., Large, D., Turner, B.L., Lopez, O.R., Boom, A., Sepulveda-Jauregui, A., Sjögersten, S., 2019. Evaluation of vegetation communities, water table, and peat composition as drivers of greenhouse gas emissions in lowland tropical peatlands. Science of the Total Environment688, 1193–1204.

[27] IPCC, 2014. Climate Change 2013 – The Physical Science Basis: Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press.

[28] IPCC, 2021. Climate Change Report IPCC 2021 – A Chimera of Science and Politics. Social Science Electronic Publishing.

[29] Kammann, C., Hepp, S., Lenhart, K., Müller, C., 2009. Stimulation of methane consumption by endogenous CH₄ production in aerobic grassland soil. Soil Biology and Biochemistry41, 622–629.

[30] Kaneda, S., Kaneko, N., 2011. Influence of collembola on nitrogen mineralization varies with soil moisture content. Soil Science and Plant Nutrition57, 40–49.

[31] Kernecker, M., Whalen, J.K., Bradley, R.L., 2015. Endogeic earthworms lower net methane production in saturated riparian soils. Biology and Fertility of Soils51, 271–275.

[32] Koubová, A., Goberna, M., Šimek, M., Chroňáková, A., Pižl, V., Insam, H., Elhottová, D., 2012. Effects of the earthworm Eisenia andrei on methanogens in a cattle-impacted soil: a microcosm study. European Journal of Soil Biology48, 32–40.

[33] Kumaresan, D., Héry, M., Bodrossy, L., Singer, A.C., Stralis-Pavese, N., Thompson, I.P., Murrell, J.C., 2011. Earthworm activity in a simulated landfill cover soil shifts the community composition of active methanotrophs. Research in Microbiology162, 1027–1032.

[34] Lavelle, P., Bignell, D., Lepage, M., Wolters, V., Roger, P., Ineson, P., Heal, O.W., Dhillion, S., 1997. Soil function in a changing world: the role of invertebrate ecosystem engineers. European Journal of Soil Biology33, 159–193.

[35] Li, F., Yang, G.B., Peng, Y.F., Wang, G.Q., Qin, S.Q., Song, Y.T., Fang, K., Wang, J., Yu, J.C., Liu, L., Zhang, D.Y., Chen, K.L., Zhou, G.Y., Yang, Y.H., 2020. Warming effects on methane fluxes differ between two alpine grasslands with contrasting soil water status. Agricultural and Forest Meteorology290, 107988.

[36] Lin, X.W., Wang, S.P., Hu, Y.G., Luo, C.Y., Zhang, Z.H., Niu, H.S., Xie, Z.B., 2015. Experimental warming increases seasonal methane uptake in an alpine meadow on the Tibetan Plateau. Ecosystems18, 274–286.

[37] Liu, J.G., Zhou, Y.L., Valach, A., Shortt, R., Kasak, K., Rey-Sanchez, C., Hemes, K.S., Baldocchi, D., Lai, D.Y.F., 2020. Methane emissions reduce the radiative cooling effect of a subtropical estuarine mangrove wetland by half. Global Change Biology26, 4998–5016.

[38] Liu, L.Y., Xie, G.J., Ding, J., Liu, B.F., Xing, D.F., Ren, N.Q., Wang, Q.L., 2022. Microbial methane emissions from the non-methanogenesis processes: a critical review. Science of the Total Environment806, 151362.

[39] Lofton, D.D., Whalen, S.C., Hershey, A.E., 2014. Effect of temperature on methane dynamics and evaluation of methane oxidation kinetics in shallow arctic alaskan lakes. Hydrobiologia721, 209–222.

[40] Louca, S., Parfrey, L.W., Doebeli, M., 2016. Decoupling function and taxonomy in the global ocean microbiome. Science353, 1272–1277.

[41] Lubbers, I.M., Berg, M.P., De Deyn, G.B., Van Der Putten, W.H., Van Groenigen, J.W., 2020. Soil fauna diversity increases CO₂ but suppresses N₂O emissions from soil. Global Change Biology26, 1886–1898.

[42] Luo, F., Zhong, J.X., Yang, Y.F., Scheuermann, R.H., Zhou, J.Z., 2006. Application of random matrix theory to biological networks. Physics Letters A357, 420–423.

[43] Mohanty, S.R., Bodelier, P.L.E., Conrad, R., 2007. Effect of temperature on composition of the methanotrophic community in rice field and forest soil. FEMS Microbiology Ecology62, 24–31.

[44] Montoya, J.M., Pimm, S.L., Solé, R.V., 2006. Ecological networks and their fragility. Nature442, 259–264.

[45] Noble, W.S., 2009. How does multiple testing correction work. Nature Biotechnology27, 1135–1137.

[46] Oswald, K., Milucka, J., Brand, A., Littmann, S., Wehrli, B., Kuypers, M.M.M., Schubert, C.J., 2015. Light-dependent aerobic methane oxidation reduces methane emissions from seasonally stratified lakes. PLoS One10, e0132574.

[47] Paul, B.K., Lubbers, I.M., Van Groenigen, J.W., 2012. Residue incorporation depth is a controlling factor of earthworm-induced nitrous oxide emissions. Global Change Biology18, 1141–1151.

[48] Picek, T., Čížková, H., Dušek, J., 2007. Greenhouse gas emissions from a constructed wetland - Plants as important sources of carbon. Ecological Engineering31, 98–106.

[49] Pržulj, N., Malod-Dognin, N., 2016. Network analytics in the age of big data. Science353, 123–124.

[50] Qi, Q., Zhao, J.S., Tian, R.M., Zeng, Y.F., Xie, C.Y., Gao, Q., Dai, T.J., Wang, H., He, J.S., Konstantinidis, K.T., Yang, Y.F., Zhou, J.Z., Guo, X., 2022. Microbially enhanced methane uptake under warming enlarges ecosystem carbon sink in a Tibetan alpine grassland. Global Change Biology28, 6906–6920.

[51] Raftery, A.E., Zimmer, A., Frierson, D.M.W., Startz, R., Liu, P.R., 2017. Less than 2°C warming by 2100 unlikely. Nature Climate Change7, 637–641.

[52] Sánchez-de León, Y., Wise, D.H., Lugo-Pérez, J., Norby, R.J., James, S.W., Gonzalez-Meler, M.A., 2018. Endogeic earthworm densities increase in response to higher fine-root production in a forest exposed to elevated CO₂. Soil Biology and Biochemistry122, 31–38.

[53] Sheehan, C., Kirwan, L., Connolly, J., Bolger, T., 2008. The effects of earthworm functional diversity on microbial biomass and the microbial community level physiological profile of soils. European Journal of Soil Biology44, 65–70.

[54] Shukla, P.N., Pandey, K.D., Mishra, V.K., 2013. Environmental determinants of soil methane oxidation and methanotrophs. Critical Reviews in Environmental Science and Technology43, 1945–2011.

[55] Sjögersten, S., Wookey, P.A., 2002. Spatio-temporal variability and environmental controls of methane fluxes at the forest-tundra ecotone in the Fennoscandian mountains. Global Change Biology8, 885–894.

[56] Song, C.Q., Luan, J.W., Xu, X.F., Ma, M.N., Aurela, M., Lohila, A., Mammarella, I., Alekseychik, P., Tuittila, E.S., Gong, W., Chen, X.Z., Meng, X.H., Yuan, W.P., 2020. A microbial functional group-based CH₄ model integrated into a terrestrial ecosystem model: model structure, site-level evaluation, and sensitivity analysis. Journal of Advances in Modeling Earth Systems12, e2019MS001867.

[57] Soper, F.M., Mackenzie, R.A., Sharma, S., Cole, T.G., Litton, C.M., Sparks, J.P., 2019. Non‐native mangroves support carbon storage, sediment carbon burial, and accretion of coastal ecosystems. Global Change Biology25, 4315–4326.

[58] Thakur, M.P., Geisen, S., 2019. Trophic regulations of the soil microbiome. Trends in Microbiology27, 771–780.

[59] Thébault, E., Fontaine, C., 2010. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science329, 853–856.

[60] Vanwonterghem, I., Evans, P.N., Parks, D.H., Jensen, P.D., Woodcroft, B.J., Hugenholtz, P., Tyson, G.W., 2016. Methylotrophic methanogenesis discovered in the archaeal phylum verstraetearchaeota. Nature Microbiology1, 16170.

[61] Wang, N., Wang, W.H., Jiang, Y.J., Dai, W., Li, P.F., Yao, D.D., Wang, J.L., Shi, Y., Cui, Z.L., Cao, H., Dong, Y.H., Wang, H., 2021. Variations in bacterial taxonomic profiles and potential functions in response to the gut transit of earthworms (Eisenia fetida) feeding on cow manure. Science of the Total Environment787, 147392.

[62] Watanabe, T., Kimura, M., Asakawa, S., 2007. Dynamics of methanogenic archaeal communities based on rRNA analysis and their relation to methanogenic activity in Japanese paddy field soils. Soil Biology and Biochemistry39, 2877–2887.

[63] Willaby, H.W., Costa, D.S.J., Burns, B.D., MacCann, C., Roberts, R.D., 2015. Testing complex models with small sample sizes: A historical overview and empirical demonstration of what Partial Least Squares (PLS) can offer differential psychology. Personality and Individual Differences84, 73–78.

[64] Wu, H.B., Wang, X.X., Ganjurjav, H., Hu, G.Z., Qin, X.B., Gao, Q.Z., 2020. Effects of increased precipitation combined with nitrogen addition and increased temperature on methane fluxes in alpine meadows of the Tibetan Plateau. Science of the Total Environment705, 135818.

[65] Wu, H.H., Xu, X.K., Duan, C.T., Li, T.S., Cheng, W.G., 2016. Synergistic effects of dissolved organic carbon and inorganic nitrogen on methane uptake in forest soils without and with freezing treatment. Scientific Reports6, 32555.

[66] Wu, H.T., Lu, M.Z., Lu, X.G., Guan, Q., He, X.H., 2015a. Interactions between earthworms and mesofauna has no significant effect on emissions of CO₂ and N₂O from soil. Soil Biology and Biochemistry88, 294–297.

[67] Wu, H.T., Lu, X.G., Tong, S.Z., Batzer, D.P., 2015b. Soil engineering ants increase CO₂ and N₂O emissions by affecting mound soil physicochemical characteristics from a marsh soil: a laboratory study. Applied Soil Ecology87, 19–26.

[68] Wu, H.T., Lu, X.G., Wu, D.H., Song, L.H., Yan, X.M., Liu, J., 2013. Ant mounds alter spatial and temporal patterns of CO₂, CH₄ and N₂O emissions from a marsh soil. Soil Biology and Biochemistry57, 884–891.

[69] Wu, Y.P., Shaaban, M., Zhao, J.S., Hao, R., Hu, R.G., 2015c. Effect of the earthworm gut-stimulated denitrifiers on soil nitrous oxide emissions. European Journal of Soil Biology70, 104–110.

[70] Xia, J.Y., Niu, S.L., Wan, S.Q., 2009. Response of ecosystem carbon exchange to warming and nitrogen addition during two hydrologically contrasting growing seasons in a temperate steppe. Global Change Biology15, 1544–1556.

[71] Xiong, C., He, J.Z., Singh, B.K., Zhu, Y.G., Wang, J.T., Li, P.P., Zhang, Q.B., Han, L.L., Shen, J.P., Ge, A.H., Wu, C.F., Zhang, L.M., 2021. Rare taxa maintain the stability of crop mycobiomes and ecosystem functions. Environmental Microbiology23, 1907–1924.

[72] Yang, G., Wang, M., Chen, H., Liu, L.F., Wu, N., Zhu, D., Tian, J.Q., Peng, C.H., Zhu, Q.A., He, Y.X., 2017. Responses of CO₂ emission and pore water DOC concentration to soil warming and water table drawdown in Zoige Peatlands. Atmospheric Environment152, 323–329.

[73] Ye, C., Gong, Y., Chen, M.P., Delgado-Baquerizo, M., Che, R.X., Liu, S.G., Zhang, Q.F., 2023. Revegetation promotes soil microbial network stability in a novel riparian ecosystem. Journal of Applied Ecology60, 1572–1586.

[74] Yuan, M.M., Guo, X., Wu, L.W., Zhang, Y., Xiao, N.J., Ning, D.L., Shi, Z., Zhou, X.S., Wu, L.Y., Yang, Y.F., Tiedje, J.M., Zhou, J.Z., 2021. Climate warming enhances microbial network complexity and stability. Nature Climate Change11, 343–348.

[75] Zhang, F., Zhang, K.P., Li, Y.F., Qin, R.Z., Hou, M., Li, M., Zhang, W.J., Li, F.M., 2022. A deeper look at crop residue and soil warming impact on the soil C pools. Soil and Tillage Research215, 105192.

[76] Zhang, L.H., Hou, L.Y., Guo, D.F., Li, L.H., Xu, X.F., 2017. Interactive impacts of nitrogen input and water amendment on growing season fluxes of CO₂, CH₄, and N₂O in a semiarid grassland, Northern China. Science of the Total Environment578, 523–534.

[77] Zhu, C.G., Zhang, J.Y., Tang, Y.P., Xu, Z.K., Song, R.T., 2011. Diversity of methanogenic archaea in a biogas reactor fed with swine feces as the mono-substrate by mcrA analysis. Microbiological Research166, 27–35.

[78] Zhu, Q.A., Peng, C.H., Liu, J.X., Jiang, H., Fang, X.Q., Chen, H., Niu, Z.G., Gong, P., Lin, G.H., Wang, M., Wang, H., Yang, Y. Z., Chang, J., Ge, Y., Xiang, W. H., Deng, X. W., He, J. S., 2016. Climate-driven increase of natural wetland methane emissions offset by human-induced wetland reduction in China over the past three decades. Scientific Reports6, 38020.

RIGHTS & PERMISSIONS

Higher Education Press