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Coupled steel slag and biochar amendment correlated with higher methanotrophic abundance and lower CH4 emission in subtropical paddies

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Abstract

Aerobic methanotrophs in paddies serve as methane (CH4) filters and thereby reduce CH4 emissions. Amending soil with waste products can mitigate CH4 emissions in crops, but little is known about the impacts of amendments with steel slag and biochar on the populations and activities of aerobic methanotrophs in rice cropland. We used real-time quantitative PCR detecting system and high-throughput sequencing to determine the effects of slag and biochar amendments on CH4 emission, abundance, and community structure of methanotrophs, and the relationships between soil properties and the abundance and community composition of methanotrophs during the rice growing season in both early and late paddies. Soil salinity and pH were significantly higher for an amendment with both slag and biochar than the control in both the early and late paddies, and pH was significantly higher for a slag amendment in the late paddy. Cumulative CH4 emission was lower for the slag and slag + biochar amendments than the control in early paddy by—34.1%. Methanotrophic abundance was three- and sixfold higher for the slag + biochar amendment than the control in the early and late paddies (p < 0.05), respectively. The abundance of different groups of methanotrophs varied among the treatments. The relative abundance of Methylosarcina was higher for the slag amendment than the control, and the relative abundance of Methylomonas was lower for biochar, and slag + biochar amendments than the control. The relative abundance of Methylocystis was higher for the slag and slag + biochar amendments than the control in the early paddy, and the relative abundance of Methylocystis was higher for the slag, biochar, and slag + biochar amendments in the late paddy. Univariate and multivariate analyses indicated that the higher abundance of methanotrophic bacteria for the slag and slag + biochar amendments was correlated with soil pH, salinity, soil organic carbon, and C/N ratio, and the relative abundances of Methylocystis, Methylomonas, and Methylosarcina were associated with the effective mitigation of CH4 emission in the paddies. A discriminant general analysis indicated that the total population of methanotrophs was larger for the slag + biochar amendment than the control, and that this effect was only weakly correlated with changes in the soil properties, demonstrating that this effect on the size and species composition of methanotrophic soil populations was mostly associated with a direct effect of the slag + biochar amendment.

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References

  • Ali, M. A., Lee, C. H., & Kim, P. J. (2008a). Effect of silicate fertilizer on reducing methane emission during rice cultivation. Biology and Fertility Soils,44, 597–604.

    CAS  Google Scholar 

  • Ali, M. A., Lee, C. H., Sang, Y. K., & Kim, P. J. (2009). Effect of industrial by-products containing electron acceptors on mitigating methane emission during rice cultivation. Waste Management,29, 2759–2764.

    CAS  Google Scholar 

  • Ali, M. A., Oh, J. H., & Kim, P. J. (2008b). Evaluation of silicate iron slag amendment on reducing methane emission from flood water rice farming. Agriculture Ecosystem and Environment,128, 21–26.

    CAS  Google Scholar 

  • Barton, L., Murphy, D. V., & Butterbach-Bahl, K. (2013). Influence of crop rotation and liming on greenhouse gas emissions from a semi-arid soil. Agriculture, Ecosystems & Environment,167(2), 23–32.

    CAS  Google Scholar 

  • Bridgham, S. D., Cadillo-Quiroz, H., Keller, J. K., & Zhuang, Q. (2013). Methane emissions from wetlands: Biogeochemical, microbial, and modeling perspectives from local to global scales. Global Change Biology,19, 1325–1346.

    Google Scholar 

  • Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods,7, 335–336.

    CAS  Google Scholar 

  • Castaldi, S., Riondino, M., Baronti, S., Esposito, F. R., Marzaioli, R., Rutigliano, F. A., et al. (2011). Impact of biochar application to a Mediterranean wheat crop on soil microbial activity and greenhouse gas fluxes. Chemosphere,85, 1464–1471.

    CAS  Google Scholar 

  • Chan, O. C., Yang, X. D., Fu, Y., Feng, Z. L., Sha, L. Q., Casper, P., et al. (2006). 16S rRNA gene analyses of bacterial community structures in the soils of evergreen broad-leaved forests in south-west China. FEMS Microbiology Ecology,58, 247–259.

    CAS  Google Scholar 

  • Chang, H. L., Sang, Y. K., Villamil, M. B., Pramanik, P., Chang, O. H., & Kim, P. J. (2012). Different response of silicate fertilizer having electron acceptors on methane emission in rice paddy soil under green manuring. Biology and Fertility of Soils,48, 435–442.

    Google Scholar 

  • Cole, J. R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R. J., et al. (2009). The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Research,37, D141–D145.

    CAS  Google Scholar 

  • Datta, A., Yeluripati, J. B., Nayak, D. R., Mahata, K. R., Santra, S. C., & Adhya, T. K. (2013). Seasonal variation of methane flux from coastal saline rice field with the application of different organic manures. Atmospheric Environment,66, 114–122.

    CAS  Google Scholar 

  • Dong, D., Yang, M., Wang, C., Wang, H. L., Li, Y., Luo, J. F., et al. (2013). Responses of methane emissions and rice yield to applications of biochar and straw in a paddy field. Journal of Soils and Sediments,13, 1450–1460.

    CAS  Google Scholar 

  • Esson, K. C., Lin, X., Kumaresan, D., Chanton, J. P., Murrell, J. C., & Kostka, J. E. (2016). Alpha and gammaproteobacterial methanotrophs co-dominate the active methane oxidizing communities in an acidic boreal peat bog. Applied and Environmental Microbiology,82, 2363–2371.

    CAS  Google Scholar 

  • Feng, Y., Xu, Y., Yu, Y., Xie, Z., & Lin, X. (2012). Mechanisms of biochar decreasing methane emission from Chinese paddy soils. Soil Biology & Biochemistry,46, 80–88.

    CAS  Google Scholar 

  • Guallar, V., Gherman, B. F., Lippard, S. J., & Friesner, R. A. (2002). Quantum chemical studies of methane monooxygenase: Comparision with P450. Current Opinion in Chemical Biology,6, 236–242.

    CAS  Google Scholar 

  • Han, X. G., Xue, S., Cheng, W., Wu, W. X., Dong, D., Zhong, T., et al. (2016). Mitigating methane emission from paddy soil with rice-straw biochar amendment under projected climate change. Scientific Reports,6, 24731.

    CAS  Google Scholar 

  • Ho, A., Kerckhof, F. M., Luke, C., Reim, A., Krause, S., Boon, N., et al. (2013). Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies. Environmental Microbiology Reports,5, 335–345.

    CAS  Google Scholar 

  • IPCC. (2014). Climate change 2014: Impacts, adaptation, and vulnerability working group II contribution to the fifth assessment report. Cambridge: Cambridge University Press.

    Google Scholar 

  • Jackel, U., & Schnell, S. (2000). Suppression of methane emission from rice paddies by ferric iron fertilization. Soil Biology Biochemistry,32, 1811–1814.

    CAS  Google Scholar 

  • Kim, J., Yoo, G., Kim, D., Ding, W., & Kang, H. (2017). Combined application of biochar and slow-release fertilizer reduces methane emission but enhances rice yield by different mechanisms. Applied Soil Ecology,117–118, 57–62.

    Google Scholar 

  • Knoblauch, C., Marifaat, A. A., & Haefele, M. S. (2008). Biochar in rice based system: Impact on carbonmineralization and trace gas emissions. http://www.biochar-international.org/2008/conference/posters.

  • Kögel-Knabner, I., Amelung, W., Cao, Z. H., Fiedler, S., Frenzel, P., Jahn, R., et al. (2010). Biogeochemistry of paddy soils. Geoderma,157, 1–14.

    Google Scholar 

  • Köppen, W. (1936). The geographic system of climates. In W. Köppen & G. Rudofl (Eds.), Handbuch der Klimatologie 1. Berlin: Borntraeger.

    Google Scholar 

  • Lau, E., Fisher, M. C., Steudler, P. A., & Cavanaugh, C. M. (2013). The methanol dehydrogenase gene, mxaf, as a functional and phylogenetic marker for proteobacterial methanotrophs in natural environments. PLoS ONE,8, e56993.

    CAS  Google Scholar 

  • Lee, H. J., Kim, S. Y., Kim, P. J., Madsen, E. L., & Che, O. J. (2014). Methane emission and dynamics of methanotrophic and methanogenic communities in a flooded rice field ecosystem. FEMS Microbiology Ecology,88, 195–212.

    CAS  Google Scholar 

  • Lee, C. H., Kim, S. Y., Villamil, M. B., Pramanik, P., Hong, C. O., & Kim, P. J. (2012). Different response of silicate fertilizer having electron acceptors on methane emission in rice paddy soil under green manuring. Biology and Fertility of Soils,48, 435–442.

    CAS  Google Scholar 

  • Lehmann, J., RilligM, C., Thies, J., Masiello, C. A., Hockaday, W. C., & Crowley, D. (2011). Biochar effects on soil biota—A review. Soil Biology & Biochemistry,43, 1812–1836.

    CAS  Google Scholar 

  • Lima, A. B., Muniz, A. W., & Dumont, M. G. (2014). Activity and abundance of methane-oxidizing bacteria in secondary forest and manioc plantations of amazonian dark earth and their adjacent soils. Frontiers in Microbiology,5, 550.

    Google Scholar 

  • Liu, Y., Yang, M., Wu, Y., Wang, H., Chen, Y., & Wu, W. (2011). Reducing CH4 and CO2 emissions from waterlogged paddy soil with biochar. Journal Soils and Sediments,11, 930–939.

    CAS  Google Scholar 

  • Lu, Q. Y. (2016). The microbial community structure in Liaohe Delta wetlands and its environmental significances. China University of Geosciences, 37–38.

  • Lüke, C., Frenze, P., Ho, A., Fiantis, D., Schad, P., Schneider, B., et al. (2014). Macroecology of methane-oxidizing bacteria: The β-diversity of pmoA genotypes in tropical and subtropical rice paddies. Environmental Microbiology,16, 72–83.

    Google Scholar 

  • Ma, K., Qiu, Q., & Lu, Y. (2010). Microbial mechanism for rice variety control on methane emission from rice field soil. Global Change Biology,16, 3085–3095.

    Google Scholar 

  • May, T., Polag, D., Keppler, F., Greule, M., Müller, L., & König, H. (2018). Methane oxidation in industrial biogas plants–insights in a novel methanotrophic environment evidenced by pmoa gene analyses and stable isotope labelling studies. Journal of Biotechnology,270, 77–84.

    CAS  Google Scholar 

  • Mohanty, S. R., Kollah, B., Sharma, V. K., Singh, A. B., Singh, M., & Rao, A. S. (2014). Methane oxidation and methane driven redox process during sequential reduction of a flooded soil ecosystem. Annals of Microbiology,64, 65–74.

    CAS  Google Scholar 

  • Nguyen, S. G., Guevarra, R. B., Kim, J., Ho, C. T., Trinh, M. V., & Unno, T. (2015). Impacts of initial fertilizers and irrigation systems on paddy methanogens and methane emission. Water, Air, and Soil pollution,226, 309–419.

    Google Scholar 

  • Pandey, A., Mai, V. T., Vu, D. Q., Bui, T. P. L., Mai, T. L. A., Jensen, L. S., et al. (2014). Organic matter and water management strategies to reduce methane and nitrous oxide emissions from rice paddies in Vietnam. Agriculture, Ecosystems & Environment,196, 137–146.

    CAS  Google Scholar 

  • Piatak, N. M., Parsons, M. B., & Seal, R. (2015). Characteristics and environmental aspects of slag: A review. Applied Geochemistry,57, 236–266.

    CAS  Google Scholar 

  • Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research,41, D590–D596.

    CAS  Google Scholar 

  • Raamsdonk, L. M., Teusink, B., Broadhurst, D., Zhang, N. S., Hayes, A., Walsh, M. C., et al. (2001). A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations. Nature Biotechnology,19, 45–50.

    CAS  Google Scholar 

  • Reim, A., Luke, C., Krause, S., Pratscher, J., & Frenzel, P. (2012). One millimetre makes the difference: high-resolution analysis of methane-oxidizing bacteria and their specific activity at the oxic-anoxic interface in a flooded paddy soil. ISME Journal,6, 2128–2139.

    CAS  Google Scholar 

  • Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., et al. (2009). Introducing mothur: Open-source, platform-independent, community supported software for describing and comparing microbial communities. Applied and Environmental Microbiology,75, 7537–7541.

    CAS  Google Scholar 

  • Sharp, C. E., Martínez-Lorenzo, A., Brady, A. L., Grasby, S. E., & Dunfield, P. F. (2014). Methanotrophic bacteria in warm geothermal spring sediments identified using stable-isotope probing. FEMS Microbiology Ecology,90, 92–102.

    CAS  Google Scholar 

  • Singla, A., & Inubushi, K. (2015). Effect of slag-type fertilizers on N2O flux from komatsuna vegetated soil and CH4 flux from paddy vegetated soil. Paddy and Water Environment,13, 43–50.

    Google Scholar 

  • Susilawati, H. L., Setyanto, P., Makarim, A. K., Ariani, M., Ito, K., & Inubushi, K. (2015). Effects of steel slag applications on CH4, N2O and the yields of Indonesian rice fields: A case study during two consecutive rice-growing seasons at two sites. Soil Science and Plant Nutrition,61, 704–718.

    CAS  Google Scholar 

  • Wang, N., Chang, Z. Z., Xue, X. M., Yu, J. G., Shi, X. X., Ma, L. Q., et al. (2017). Biochar decreases nitrogen oxide and enhances methane emissions via altering microbial community composition of anaerobic paddy soil. Science of the Total Environment,581–582, 689–696.

    Google Scholar 

  • Wang, W., Lai, D. Y. F., Li, S., Kim, P. J., Zeng, C., Li, P., et al. (2014). Steel slag amendment reduces methane emission and increases rice productivity in subtropical paddy fields in China. Wetlands Ecology and Management,22, 683–691.

    CAS  Google Scholar 

  • Wang, J., Pan, X., Liu, Y., Zhang, X., & Xiong, Z. (2012). Effects of biochar amendment in two soils on greenhouse gas emissions and crop production. Plant and Soil,360, 287–298.

    CAS  Google Scholar 

  • Wang, W., Sardans, J., Lai, D. Y. F., Wang, C., Zeng, C., Tong, C., et al. (2015). Effects of steel slag application on greenhouse gas emissions and crop yield over multiple growing seasons in a subtropical paddy field in China. Field Crops Research,171, 146–156.

    Google Scholar 

  • Wang, M. Y., Xu, X. P., Wang, W. Q., Wang, G. L., & Su, C. J. (2018). Effects of slag and biochar amendments on methanogenic community structures in paddy fields. Acta Ecologica Sinica,38(8), 2816–2828.

    Google Scholar 

  • Wise, M. G., Mcarthur, J. V., & Shimkets, L. J. (2001). Methylosarcina fibrata gen. nov. sp. nov. and Methylosarcina quisquiliarum sp.nov. novel type I methanotrophs. International Journal of Systematic and Evolutionary Microbiology,51, 611–621.

    CAS  Google Scholar 

  • Woese, C. R., Kandler, O., & Wheelis, M. L. (1990). Towards to a natural system of organisms. Proposal for the domains Archaea, Bacteria and Eucarya. Proceedings of the National Academy of Sciences of the United States of America,87, 44576–44579.

    Google Scholar 

  • Zhang, A. F., Bian, R. J., Hussain, Q., Li, L. Q., Pan, G. X., Zheng, J. W., et al. (2013). Change in net global warming potential of a rice–wheat cropping system with biochar soil amendment in a rice paddy from china. Agriculture, Ecosystems & Environment,173, 37–45.

    Google Scholar 

  • Zhang, A. F., Cui, L. Q., Pan, G. X., Li, L. Q., Hussain, Q., Zhang, X. H., et al. (2010). Effect of biochar amendment on yield and methane and nitrous oxide emissions from a rice paddy from Tai Lake plain, China. Agriculture, Ecosystems & Environment,139, 469–475.

    CAS  Google Scholar 

  • Zhang, A. F., Liu, Y. M., Pan, G. X., Hussain, Q., Li, L. Q., Zheng, J. W., et al. (2012). Effect of biochar amendment on maize yield and greenhouse gas emissions from a soil organic carbon poor calcareous loamy soil from Central China Plain. Plant and Soil,351, 263–275.

    CAS  Google Scholar 

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Acknowledgements

The authors would like to thank Wanli An and Guixiang Chen for their assistance with field sampling. Funding was provided by the National Science Foundation of China (41571287, 31000209), Research Project of Public Institute of Fujian Province (2018R1034-1), Outstanding Young Research Talents in Higher Education of Fujian Province (2017), European Research Council Synergy grant ERC-SyG-2013-610028 IMBALANCE-P, Spanish Government Grant CGL2016-79835-P, and Catalan Government Grant SGR 2017-1005.

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  1. Miaoying Wang and Chun Wang have contributed equally to this work.

Authors and Affiliations

  1. College of Life Science, Fujian Normal University, Fuzhou, 350108, China

    Miaoying Wang, Xingfu Lan & Xuping Xu

  2. Key Laboratory of Humid Sub-tropical Eco-geographical Process of Ministry of Education, Fujian Normal University, Fuzhou, 350007, China

    Chun Wang & Weiqi Wang

  3. Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Key Laboratory of Environment Remediation and Ecological Health, Ministry of Education, Zhejiang University, Hangzhou, 310058, People’s Republic of China

    Abbas Ali Abid

  4. Regional Centre of Organic Farming, Ministry of Agriculture and Farmers Welfare, Bhubaneswar, Odisha, 751-021, India

    Ankit Singla

  5. Global Ecology Unit, CREAF-CSIC-UAB, CSIC, 08193, Bellaterra, Catalonia, Spain

    Jordi Sardans, Joan Llusià & Josep Peñuelas

  6. CREAF, 08193, Cerdanyola del Vallès, Catalonia, Spain

    Jordi Sardans, Joan Llusià & Josep Peñuelas

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  1. Miaoying Wang
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Wang, M., Wang, C., Lan, X. et al. Coupled steel slag and biochar amendment correlated with higher methanotrophic abundance and lower CH4 emission in subtropical paddies. Environ Geochem Health 42, 483–497 (2020). https://doi.org/10.1007/s10653-019-00378-4

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