Impact of conversion of coastal wetlands into paddy fields on the process of nitrite-dependent anaerobic methane oxidation

Highlights

	● n-damo activity increased by 43.6%−165.8% after conversion in mangrove wetland.
	● n-damo activity showed no significant change after conversion in P. australis wetland.
	● Community altered more significantly after conversion in mangrove wetland.
	● Bulk density, salinity, and organic carbon were main factors affecting n-damo activity.

Abstract

Nitrite-dependent anaerobic methane oxidation (n-damo), performed by the bacteria associated with Candidatus Methylomirabilis oxyfera, acts as a novel methane sink in coastal wetlands. Conversion of coastal wetlands into paddy fields is a common land-use change that has profound effects on methane emissions, but its impact on n-damo process is nearly unknown. Our study adopted a space-for-time substitution method to compare n-damo activity and community of Methylomirabilis-like bacteria between natural vegetation covered by Phragmites australis, Kandelia candek, or Bruguiera sexangula and adjacent converted paddy fields in six China’s coastal wetlands. Generalized linear mixed model indicated that the activity of n-damo significantly increased by 43.6% and 165.8% after conversion of K. candek and B. sexangula wetlands into rice paddies, respectively, while the activity exhibited no significant change after conversion of P. australis wetlands. Furthermore, the abundance of Methylomirabilis-like bacteria significantly increased by 90.2%, 210.0%, and 110.1% following the conversion in wetlands covered by K. candek, B. sexangula, and P. australis, respectively. Principal co-ordinates analysis revealed significant changes in community structure of Methylomirabilis-like bacteria among vegetation types, with K. candek and B. sexangula showing a greater divergence than P. australis when compared to respective paddy fields. Path analysis indicated that land conversion resulted in changes in soil moisture content, organic carbon content, bulk density, and salinity and further affected the abundance of Methylomirabilis-like bacteria and ultimately n-damo activity. Overall, this is the first study to reveal the impact of conversion of coastal wetlands into paddy fields on n-damo activity and Methylomirabilis-like bacteria, and the impact was closely associated with the original native plant types. The results can enhance our understanding of the microbial-driven mechanisms of the impact of land conversion on methane emissions.

Graphical abstract

Keywords

conversion / coastal wetlands / paddy fields / nitrite-dependent anaerobic methane oxidation

References

[1] An, S.Q., Li, H., Guan, B.H., Zhou, C.F., Wang, Z.S., Deng, Z.F., Zhi, Y.B., Liu, Y.H., Xu, C., Fang, S.B., Jiang, J.H., Li, H.L., 2007. China's natural wetlands: past problems, current status, and future challenges. AMBIO: A Journal of the Human Environment36, 335–342.

[2] Avrahami, S., 2002. Effects of temperature, soil ammonium concentration and fertilizer on activity and community structure of ammonia oxidizers. Ph.D. Dissertation. Philipps-Universität Marburg, Marburg, Germany.

[3] Blois, J.L., Williams, J.W., Fitzpatrick, M.C., Jackson, S.T., Ferrier, S., 2013. Space can substitute for time in predicting climate-change effects on biodiversity. Proceedings of the National Academy of Sciences of the United States of America110, 9374–9379.

[4] Bridgham, S.D., Cadillo-Quiroz, H., Keller, J.K., Zhuang, Q.L., 2013. Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales. Global Change Biology19, 1325–1346.

[5] Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods7, 335–336.

[6] Chen, F.Y., Zheng, Y.L., Hou, L.J., Niu, Y.H., Gao, D.Z., An, Z.R., Zhou, J., Yin, G.Y., Dong, H.P., Han, P., Liang, X., Liu, M., 2021. Microbial abundance and activity of nitrite/nitrate-dependent anaerobic methane oxidizers in estuarine and intertidal wetlands: heterogeneity and driving factors. Water Research190, 116737.

[7] Chen, J., Zhou, Z.C., Gu, J.D., 2015. Complex community of nitrite-dependent anaerobic methane oxidation bacteria in coastal sediments of the Mai Po wetland by PCR amplification of both 16S rRNA and pmoA genes. Applied Microbiology and Biotechnology99, 1463–1473.

[8] Cui, J., Liu, C., Li, Z.L., Wang, L., Chen, X.F., Ye, Z.Z., Fang, C.M., 2012. Long-term changes in topsoil chemical properties under centuries of cultivation after reclamation of coastal wetlands in the Yangtze Estuary, China. Soil and Tillage Research123, 50–60.

[9] Deutzmann, J.S., Schink, B., 2011. Anaerobic oxidation of methane in sediments of lake constance, an oligotrophic freshwater lake. Applied and Environmental Microbiology77, 4429–4436.

[10] Ettwig, K.F., Butler, M.K., Le Paslier, D., Pelletier, E., Mangenot, S., Kuypers, M.M.M., Schreiber, F., Dutilh, B.E., Zedelius, J., de Beer, D., Gloerich, J., Wessels, H.J.C.T., van Alen, T., Luesken, F., Wu, M.L., van de Pas-Schoonen, K.T., Op den Camp, H.J.M., Janssen-Megens, E.M., Francoijs, K.J., Stunnenberg, H., Weissenbach, J., Jetten, M.S.M., Strous, M., 2010. Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature464, 543–548.

[11] Ettwig, K.F., van Alen, T., van de Pas-Schoonen, K.T., Jetten, M.S.M., Strous, M., 2009. Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum. Applied and Environmental Microbiology75, 3656–3662.

[12] Geng, C.Y., Shen, L.D., Ren, B.J., Huang, H.C., Jin, J.H., Yang, W.T., Agathokleous, E., Liu, J.Q., Yang, Y.L., Bai, Y.N., Song, Y.Z., 2024. Vertical and temporal variations in activity, abundance, and composition of nitrite-driven anaerobic methanotrophs in a paddy field. Applied Soil Ecology197, 105342.

[13] He, Y., Zhang, M.X., 2001. Study on wetland loss and its reasons in China. Chinese Geographical Science11, 241–245.

[14] He, Z.F., Wang, J.Q., Hu, J.J., Yu, H.Q., Jetten, M.S.M., Liu, H., Cai, C.Y., Liu, Y., Ren, H.X., Zhang, X., Hua, M.L., Xu, X.H., Zheng, P., Hu, B.L., 2019. Regulation of coastal methane sinks by a structured gradient of microbial methane oxidizers. Environmental Pollution244, 228–237.

[15] He, Z.F., Wang, J.Q., Hu, J.J., Zhang, H., Cai, C.Y., Shen, J.X., Xu, X.H., Zheng, P., Hu, B.L., 2016. Improved PCR primers to amplify 16S rRNA genes from NC10 bacteria. Applied Microbiology and Biotechnology100, 5099–5108.

[16] He, Z.F., Zhang, Q.Y., Feng, Y.D., Luo, H.W., Pan, X.L., Gadd, G.M., 2018. Microbiological and environmental significance of metal-dependent anaerobic oxidation of methane. Science of the Total Environment610–611, 759–768.

[17] Hu, M.J., Sardans, J., Yang, X.Y., Peñuelas, J., Tong, C., 2020. Patterns and environmental drivers of greenhouse gas fluxes in the coastal wetlands of China: a systematic review and synthesis. Environmental Research186, 109576.

[18] IPCC, 2021. Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press.

[19] Juretschko, S., Timmermann, G., Schmid, M., Schleifer, K.H., Pommerening-Röser, A., Koops, H.P., Wagner, M., 1998. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Applied and Environmental Microbiology64, 3042–3051.

[20] Li, X., Gao, D., Hou, L., Liu, M., 2019. Salinity stress changed the biogeochemical controls on CH₄ and N₂O emissions of estuarine and intertidal sediments. Science of the Total Environment652, 593–601.

[21] Liu, J.Q., Wang, W.Q., Shen, L.D., Bai, Y.N., Yang, W.T., Yang, Y.L., Xu, J.B., Tian, M.H., Liu, X., Jin, J.H., Song, Y.Z., 2024. Variations of activity and community structure of nitrite-driven anaerobic methanotrophs in soils between native and invasive species in China's coastal wetlands. European Journal of Soil Biology120, 103592.

[22] Liu, X., Shen, L.D., Yang, W.T., Tian, M.H., Jin, J.H., Yang, Y.L., Liu, J.Q., Hu, Z.H., Wu, H.S., 2022. Effect of elevated atmospheric CO₂ concentration on the activity, abundance and community composition of aerobic methanotrophs in paddy soils. Applied Soil Ecology170, 104301.

[23] Long, Y., Jiang, X.J., Guo, Q.W., Li, B.X., Xie, S.G., 2017. Sediment nitrite-dependent methane-oxidizing microorganisms temporally and spatially shift in the Dongjiang River. Applied Microbiology and Biotechnology101, 401–410.

[24] Luesken, F.A., Sánchez, J., van Alen, T.A., Sanabria, J., Op den Camp, H.J.M., Jetten, M.S.M., Kartal, B., 2011. Simultaneous nitrite-dependent anaerobic methane and ammonium oxidation processes. Applied and Environmental Microbiology77, 6802–6807.

[25] Luesken, F.A., Wu, M.L., den Camp, H.J.M.O., Keltjens, J.T., Stunnenberg, H., Francoijs, K.J., Strous, M., Jetten, M.S.M., 2012. Effect of oxygen on the anaerobic methanotroph ‘Candidatus Methylomirabilis oxyfera’: kinetic and transcriptional analysis. Environmental Microbiology14, 1024–1034.

[26] Marchand, C., David, F., Jacotot, A., Leopold, A., Ouyang, X.G., 2022. CO₂ and CH₄ emissions from coastal wetland soils. In: Ouyang, X.G., Lee, S.Y., Lai, D.Y.F., Marchand, C., eds. Carbon Mineralization in Coastal Wetlands. Amsterdam: Elsevier, 55–91.

[27] McDaniel, M.D., Saha, D., Dumont, M.G., Hernández, M., Adams, M.A., 2019. The effect of land-use change on soil CH₄ and N₂O fluxes: a global meta-analysis. Ecosystems22, 1424–1443.

[28] Niu, Y.H., Zheng, Y.L., Hou, L.J., Gao, D.Z., Chen, F.Y., Pei, C.Y., Dong, H.P., Liang, X., Liu, M., 2022. Microbial dynamics and activity of denitrifying anaerobic methane oxidizers in China's estuarine and coastal wetlands. Science of the Total Environment806, 150425.

[29] Robinson, D.A., Thomas, A., Reinsch, S., Lebron, I., Feeney, C.J., Maskell, L.C., Wood, C.M., Seaton, F.M., Emmett, B.A., Cosby, B.J., 2022. Analytical modelling of soil porosity and bulk density across the soil organic matter and land-use continuum. Scientific Reports12, 7085.

[30] Sasmito, S.D., Taillardat, P., Clendenning, J.N., Cameron, C., Friess, D.A., Murdiyarso, D., Hutley, L.B., 2019. Effect of land-use and land-cover change on mangrove blue carbon: a systematic review. Global Change Biology25, 4291–4302.

[31] Shen, L.D., Hu, B.L., Liu, S., Chai, X.P., He, Z.F., Ren, H.X., Liu, Y., Geng, S., Wang, W., Tang, J.L., Wang, Y.M., Lou, L.P., Xu, X.Y., Zheng, P., 2016a. Anaerobic methane oxidation coupled to nitrite reduction can be a potential methane sink in coastal environments. Applied Microbiology and Biotechnology100, 7171–7180.

[32] Shen, L.D., Huang, Q., He, Z.F., Lian, X., Liu, S., He, Y.F., Lou, L.P., Xu, X.Y., Zheng, P., Hu, B.L., 2015. Vertical distribution of nitrite-dependent anaerobic methane-oxidising bacteria in natural freshwater wetland soils. Applied Microbiology and Biotechnology99, 349–357.

[33] Shen, L.D., Ouyang, L., Zhu, Y.Z., Trimmer, M., 2019. Spatial separation of anaerobic ammonium oxidation and nitrite-dependent anaerobic methane oxidation in permeable riverbeds. Environmental Microbiology21, 1185–1195.

[34] Shen, L.D., Tian, M.H., Cheng, H.X., Liu, X., Yang, Y.L., Liu, J.Q., Xu, J.B., Kong, Y., Li, J.H., Liu, Y., 2020. Different responses of nitrite- and nitrate-dependent anaerobic methanotrophs to increasing nitrogen loading in a freshwater reservoir. Environmental Pollution263, 114623.

[35] Shen, L.D., Wu, H.S., Gao, Z.Q., Liu, X., Li, J., 2016b. Comparison of community structures of Candidatus methylomirabilis oxyfera-like bacteria of NC10 phylum in different freshwater habitats. Scientific Reports6, 25647.

[36] Shen, L.D., Yang, W.T., Yang, Y.L., Liu, X., Tian, M.H., Jin, J.H., Liu, J.Q., Ren, B.J., Pan, Y.Y., Han, M.J., 2021. Spatial and temporal variations of the community structure and abundance of Candidatus methanoperedens nitroreducens-like archaea in paddy soils. European Journal of Soil Biology106, 103345.

[37] Shen, L.D., Zhu, Q., Liu, S., Du, P., Zeng, J.N., Cheng, D.Q., Xu, X.Y., Zheng, P., Hu, B.L., 2014. Molecular evidence for nitrite-dependent anaerobic methane-oxidising bacteria in the Jiaojiang Estuary of the East Sea (China). Applied Microbiology and Biotechnology98, 5029–5038.

[38] Shi, L.D., Guo, T., Lv, P.L., Niu, Z.F., Zhou, Y.J., Tang, X.J., Zheng, P., Zhu, L.Z., Zhu, Y.G., Kappler, A., Zhao, H.P., 2020. Coupled anaerobic methane oxidation and reductive arsenic mobilization in wetland soils. Nature Geoscience13, 799–805.

[39] Shi, Y., Zhang, X.Y., Wang, Z.C., Xu, Z.W., He, C.G., Sheng, L.X., Liu, H.Y., Wang, Z.Q., 2021. Shift in nitrogen transformation in peatland soil by nitrogen inputs. Science of the Total Environment764, 142924.

[40] Tian, M.H., Shen, L.D., Liu, X., Bai, Y.N., Hu, Z.H., Jin, J.H., Feng, Y.F., Liu, Y., Yang, W.T., Yang, Y.L., Liu, J.Q., 2021. Response of nitrite-dependent anaerobic methanotrophs to elevated atmospheric CO₂ concentration in paddy fields. Science of the Total Environment801, 149785.

[41] Wang, W.Q., Wang, C., Sardans, J., Fang, Y.Y., Singh, B.P., Wang, H.r., Huang, X.T., Zeng, C.S., Tong, C., Peñuelas, J., 2020. Multiple trade-offs between maximizing yield and minimizing greenhouse gas production in Chinese rice croplands. Land Degradation & Development31, 1287–1299.

[42] Wang, Z.H., Li, J.Y., Xu, X.Y., Li, K., Chen, Q.F., 2022. Denitrifying anaerobic methane oxidation and mechanisms influencing it in Yellow River Delta coastal wetland soil, China. Chemosphere298, 134345.

[43] Xi, D., Bai, R., Zhang, L.M., Fang, Y.T., 2016. Contribution of anammox to nitrogen removal in two temperate forest soils. Applied and Environmental Microbiology82, 4602–4612.

[44] Yang, W.T., Wang, W.Q., Shen, L.D., Bai, Y.N., Liu, X., Tian, M.H., Wang, C., Feng, Y.F., Liu, Y., Yang, Y.L., Liu, J.Q., Geng, C.Y., 2022a. Potential role of nitrite-dependent anaerobic methane oxidation in methane consumption and nitrogen removal in Chinese paddy fields. Science of the Total Environment838, 156534.

[45] Yang, Y.L., Shen, L.D., Zhao, X., Agathokleous, E., Wang, S.W., Ren, B.J., Yang, W.T., Liu, J.Q., Jin, J.H., Huang, H.C., Wu, H.S., 2023. Long-term fertilization enhances the activity of anaerobic oxidation of methane coupled to nitrate reduction and associated microbial abundance in paddy soils. Soil Biology and Biochemistry185, 109130.

[46] Yang, Y.L., Shen, L.D., Zhao, X., Shan, J., Wang, S.W., Zhou, W., Liu, J.Q., Liu, X., Tian, M.H., Yang, W.T., Jin, J.H., Wu, H.S., 2022b. Long-term incorporation of wheat straw changes the methane oxidation potential, abundance and community composition of methanotrophs in a paddy ecosystem. Applied Soil Ecology173, 104384.

[47] Yao, X.C., Wang, W.Q., Yang, Y.L., Yang, W.T., Hu, Q.N., Jin, J.H., Liu, J.Q., Wang, Y.C., Shen, L.D., 2024. Stimulation of methane production potential and alteration in community composition of methanogens following conversion of China’s coastal marshes to paddy fields. CATENA246, 108428.

[48] Zhang, M., Huang, W., Zhang, L., Feng, Z., Zuo, Y., Xie Z., Xing, W., 2024. Nitrite-dependent anaerobic methane oxidation (N-DAMO) in global aquatic environments: A review. Science of the Total Environment921, 171081.

[49] Zhang, M.P., Luo, Y., Lin, L.A., Lin, X.L., Hetharua, B., Zhao, W.J., Zhou, M.K., Zhan, Q., Xu, H., Zheng, T.L., Tian, Y., 2018. Molecular and stable isotopic evidence for the occurrence of nitrite-dependent anaerobic methane-oxidizing bacteria in the mangrove sediment of Zhangjiang Estuary, China. Applied Microbiology and Biotechnology102, 2441–2454.

Acknowledgments

This study was supported by the National Natural Science Foundation of China (Grant Nos. 41977037, 42377116, and 42077086), the 333 High-level Talents Training Project of Jiangsu Province (Grant No. BRA2022023), and Fujian Natural Science Foundation (Grant No. 2021J06019).

Conflict of interest

The authors declare that they have no conflicts of interest.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-024-0288-5 and is accessible for authorized users.

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