DOI QR코드

DOI QR Code

Methanogenesis and Methane Oxidation in Paddy Fields under Organic Fertilization

  • Kim, Chungwoo (Chungcheongbuk-do Agricultural Research ang Extension Services) ;
  • Walitang, Denver I. (College of Agriculture, Fisheries and Forestry, Romblon State University) ;
  • Sa, Tongmin (Department of Environmental and Biological Chemistry, Chungbuk National University)
  • Received : 2021.12.10
  • Accepted : 2021.12.17
  • Published : 2021.12.31

Abstract

BACKGROUND: Global warming is one of the most pressing environmental issues which concomitantly complicates global climate change. Methane emission is a balance between methanogenesis and methane consumption, both of which are driven by microbial actions in different ecosystems producing methane, one of the major greenhouse gases. Paddy fields are major sources of anthropogenic methane emissions and could be compounded by organic fertilization. METHODS AND RESULTS: Literature reviews were conducted to give an overview of the global warming conditions and to present the relationship of carbon and methane to greenhouse gas emissions, and the need to understand the underlying processes of methane emission. A more extensive review was done from studies on methane emission in paddy fields under organic fertilization with greater emphasis on long term amendments. Changes in paddy soils due to organic fertilization include alterations of the physicochemical properties and changes in biological components. There are diverse phylogenetic groups of methanogens and methane oxidizing bacteria involved in methane emission. Also, multiple factors influence methanogenesis and methane oxidation in rice paddy fields under organic fertilization and they should be greatly considered when developing mitigating steps in methane emission in paddy fields especially under long term organic fertilization. CONCLUSION(S): This review showed that organic fertilization, particularly for long term management practices, influenced both physicochemical and biological components of the paddy fields which could ultimately affect methanogenesis, methane oxidation, and methane emission. Understanding interrelated factors affecting methane emission helps create ways to mitigate their impact on global warming and climate change.

Keywords

Acknowledgement

This study was carried out with the support of "PJ015584042021", Rural Development Administration, Republic of Korea.

References

  1. Paustian K, Lehmann J, Ogle S, Reay D, Robertson GP, Smith P (2016) Climate-smart soils. Nature, 532 (7597), 49-57. https://doi.org/10.1038/nature17174.
  2. Le Mer J, Roger P (2001) Production, oxidation, emission and consumption of methane by soils: a review. European Journal of Soil Biology, 37(1), 25-50. https://doi.org/10.1016/S1164-5563(01)01067-6.
  3. Jackson RB, Abernethy S, Canadell JG, Cargnello M, Davis SJ, F?ron S, Fuss S, Heyer AJ, Hong C, Jones CD, Matthews HD, O'Connor FM, Pisciotta M, Rhoda HM, de Richter R, Solomon EI, Wilcox JL, Zickfeld K (2021) Atmospheric methane removal: a research agenda. Philosophical Transactions of the Royal Society A, 379(2210), 20200454. https://doi.org/10.1098/rsta.2020.0454.
  4. Conrad R (2007) Microbial ecology of methanogens and methanotrophs. Advances in Agronomy, 96, 1-63. https://doi.org/10.1016/S0065-2113(07)96005-8.
  5. Diacono M, Montemurro F (2011) Long-term effects of organic amendments on soil fertility. Sustainable Agriculture, 2, 761-786. https://doi.org/10.1007/978-94-007-0394-0_34.
  6. Liu L, Greaver TL (2009) A review of nitrogen enrichment effects on three biogenic GHGs: the CO2 sink may be largely offset by stimulated N2O and CH4 emission. Ecology Letters, 12(10), 1103-1117. https://doi.org/10.1111/j.1461-0248.2009.01351.x.
  7. Sun BF, Zhao H, Lu YZ, Lu F, Wang XK (2016) The effects of nitrogen fertilizer application on methane and nitrous oxide emission/uptake in Chinese croplands. Journal of Integrative Agriculture, 15(2), 440-450. https://doi.org/10.1016/S2095-3119(15)61063-2.
  8. Linquist BA, Adviento-Borbe MA, Pittelkow CM, van Kessel C, van Groenigen KJ (2012) Fertilizer management practices and greenhouse gas emissions from rice systems: a quantitative review and analysis. Field Crops Research, 135, 10-21. https://doi.org/10.1016/j.fcr.2012.06.007.
  9. Carlson KM, Gerber JS, Mueller ND, Herrero M, MacDonald GK, Brauman KA, Havlik P, O'Connell CS, Johnson JA, Saatchi S, West PC (2017) Greenhouse gas emissions intensity of global croplands. Nature Climate Change, 7(1), 63-68. https://doi.org/10.1038/nclimate3158
  10. Bhattacharyya P, Nayak AK, Mohanty S, Tripathi R, Shahid M, Kumar A, Raja R, Panda BB, Roy KS, Neogi S, Dash PK, Shukla AK, Rao KS (2013) Greenhouse gas emission in relation to labile soil C, N pools and functional microbial diversity as influenced by 39 years long term fertilizer management in tropical rice. Soil and Tillage Research, 129, 93-105. https://doi.org/10.1016/j.still.2013.01.014.
  11. Bodelier PL (2011) Interactions between nitrogenous fertilizers and methane cycling in wetland and upland soils. Current Opinion in Environmental Sustainability, 3(5), 379-388. https://doi.org/10.1016/j.cosust.2011.06.002.
  12. Hou P, Yu Y, Xue L, Petropoulos E, He S, Zhang Y, Pandey A, Xue L, Yang L, Chen D (2020) Effect of long term fertilization management strategies on methane emissions and rice yield. Science of the Total Environment, 725, 138261.https://doi.org/10.1016/j.scitotenv.2020.138261.
  13. Hakobyan A, Liesack W (2020) Unexpected metabolic versatility among type II methanotrophs in the Alphaproteobacteria. Biological Chemistry, 401(12), 1469-1477. https://doi.org/10.1515/hsz-2020-0200.
  14. Mohanty SR, Bodelier PL, Floris V, Conrad R (2006) Differential effects of nitrogenous fertilizers on methane-consuming microbes in rice field and forest soils. Applied and Environmental Microbiology, 72(2), 1346-1354. https://doi.org/10.1128/AEM.72.2.1346-1354.2006.
  15. Rajkishore SK, Vignesh NS, Doraisamy P, Maheswari M (2015) Methane emission from rice ecosystems: 100 years of research. The Ecoscan, 9(1&2), 181-193.
  16. Ahn JH, Lee SA, Kim JM, Kim MS, Song J, Weon HY (2016) Dynamics of bacterial communities in rice field soils as affected by different long-term fertilization practices. Journal of Microbiology, 54(11), 724-731. https://doi.org/10.1007/s12275-016-6463-3.
  17. Wang Z, Li X, Ji B, Struik PC, Jin K, Tang S (2021) Coupling between the responses of plants, soil, and microorganisms following grazing exclusion in an overgrazed grassland. Frontiers in Plant Science, 12, 640789. https://doi.org/10.3389/fpls.2021.640789.
  18. Vautard R, Gobiet A, Sobolowski S, Kjellstr?m E, Stegehuis A, Watkiss P, Mendlik T, Landgren O, Nikulin G, Teichmann C, Jacob D (2014) The European climate under a 2℃ global warming. Environmental Research Letters, 9(3), 034006. https://doi.org/10.1088/1748-9326/9/3/034006
  19. Zandalinas SI, Fritschi FB, Mittler R (2021) Global warming, climate change, and environmental pollution: recipe for a multifactorial stress combination disaster. Trends in Plant Science. https://doi.org/10.1016/j.tplants.2021.02.011.
  20. Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annual Review of Plant Biology, 61, 443-462. https://doi.org/10.1146/annurev-arplant-042809-112116.
  21. Awasthi R, Kaushal N, Vadez V, Turner NC, Berger J, Siddique KH, Nayyar H (2014) Individual and combined effects of transient drought and heat stress on carbon assimilation and seed filling in chickpea. Functional Plant Biology, 41(11), 1148-1167. https://doi.org/10.1071/FP13340.
  22. Zandalinas SI, Mittler R, Balfagon D, Arbona V, Gomez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiologia Plantarum, 162(1), 2-12. https://doi.org/10.1111/ppl.12540.
  23. Sehgal A, Sita K, Bhandari K, Kumar S, Kumar J, Vara Prasad PV, Nayyar H (2019) Influence of drought and heat stress, applied independently or in combination during seed development, on qualitative and quantitative aspects of seeds of lentil (Lens culinaris Medikus) genotypes, differing in drought sensitivity. Plant, Cell & Environment, 42(1), 198-211. https://doi.org/10.1111/pce.13328.
  24. Chen X, Hu Y, Xia Y, Zheng S, Ma C, Rui Y, He H, Huang D, Zhang Z, Ge T, Wu J, Guggenberger G, Kuzyakov Y, Su Y (2021) Contrasting pathways of carbon sequestration in paddy and upland soils. Global Change Biology, 27(11), 2478-2490. https://doi.org/10.1111/gcb.15595.
  25. Inagaki F, Tsunogai U, Suzuki M, Kosaka A, Machiyama H, Takai K, Nunoura T, Nealson KH, Horikoshi K (2004) Characterization of C1-metabolizing prokaryotic communities in methane seep habitats at the Kuroshima Knoll, southern Ryukyu Arc, by analyzing pmoA, mmoX, mxaF, mcrA, and 16S rRNA genes. Applied and Environmental Microbiology, 70(12), 7445-7455. https://doi.org/10.1128/AEM.70.12.7445-7455.2004.
  26. Bi L, Zhang B, Liu G, Li Z, Liu Y, Ye C, Yu X, Lai T, Zhang J, Yin J, Liang Y (2009) Long term effects of organic amendments on the rice yields for double rice cropping systems in subtropical China. Agriculture, Ecosystems & Environment, 129(4), 534-541. https://doi.org/10.1016/j.agee.2008.11.007.
  27. Singh A, Singh RS, Upadhyay SN, Joshi CG, Tripathi AK, Dubey SK (2012) Community structure of methanogenic archaea and methane production associated with compost-treated tropical rice-field soil. FEMS Microbiology Ecology, 82(1), 118-134. https://doi.org/10.1111/j.1574-6941.2012.01411.x.
  28. Shirato Y (2020) Use of models to evaluate carbon sequestration in agricultural soils. Soil Science and Plant Nutrition, 66(1), 21-27. https://doi.org/10.1080/00380768.2019.1702477.
  29. Li FR, Zhao WZ, Liu JL, Huang ZG (2009) Degraded vegetation and wind erosion influence soil carbon, nitrogen and phosphorus accumulation in sandy grasslands. Plant and Soil, 317(1), 79-92. https://doi.org/10.1007/s11104-008-9789-8.
  30. Glaser B, Lehmann J, Steiner C, Nehls T, Yousaf M, Zech W (2002) Potential of pyrolyzed organic matter in soil amelioration. In 12th ISCO conference. Beijing, 421-427.
  31. Lehmann J, Kinyangi J, Solomon D (2007) Organic matter stabilization in soil microaggregates: implications from spatial heterogeneity of organic carbon contents and carbon forms. Biogeochemistry, 85(1), 45-57. https://doi.org/10.1007/s10533-007-9105-3.
  32. Lal R, Griffin M, Apt J, Lave L, Morgan MG (2004) Managing soil carbon. Science, 304(5669), 393. https://doi.org/10.1126/science.1093079.
  33. Saunois M, Stavert AR, Poulter B, Bousquet P, Canadell JG, Jackson RB, Zhuang Q (2020) The global methane budget 2000-2017. Earth System Science Data, 12(3), 1561-1623. https://doi.org/10.5194/essd12-1561-2020.
  34. Zhou B, Wang Y, Feng Y, Lin X (2016) The application of rapidly composted manure decreases paddy CH4 emission by adversely influencing methanogenic archaeal community: a greenhouse study. Journal of Soils and Sediments, 16(7), 1889-1900. https://doi.org/10.1007/s11368-016-1377-6.
  35. Chen Y, Li S, Zhang Y, Li T, Ge H, Xia S, Gu J, Zhang H, Lu B, Wu X, Wang Z, Yang J, Zhang J, Liu L (2019) Rice root morphological and physiological traits interaction with rhizosphere soil and its effect on methane emissions in paddy fields. Soil Biology and Biochemistry, 129, 191-200. https://doi.org/10.1016/j.soilbio.2018.11.015.
  36. Pump J, Pratscher J, Conrad R (2015) Colonization of rice roots with methanogenic archaea controls photosynthesis-derived methane emission. Environmental Microbiology, 17(7), 2254-2260. https://doi.org/10.1111/1462-2920.12675.
  37. Yuan J, Yuan Y, Zhu Y, Cao L (2018) Effects of different fertilizers on methane emissions and methanogenic community structures in paddy rhizosphere soil. Science of The Total Environment, 627, 770-781. https://doi.org/10.1016/j.scitotenv.2018.01.233.
  38. Dutaur L and Verchot LV (2007) A global inventory of the soil CH4 sink. Global Biogeochemical Cycles, 21(4). https://doi.org/10.1029/2006GB002734.
  39. Stavert AR, Saunois M, Canadell JG, Poulter B, Jackson RB, Regnier P, Zhuang Q (2021) Regional trends and drivers of the global methane budget. Global Change Biology. https://doi.org/10.1111/gcb.15901.
  40. Griscom BW, Adams J, Ellis PW, Houghton RA, Lomax G, Miteva DA, Schlesinge, WH, Shoch D, Siikamaki JV, Smith P, Woodbury P (2017) Natural climate solutions. Proceedings of the National Aca demy of Sciences, 114(44), 11645-11650. https://doi.org/10.1073/pnas.1710465114.
  41. Holmes AJ, Roslev P, McDonald IR, Iversen N, Henriksen KAJ and Murrell JC (1999) Characterization of methanotrophic bacterial populations in soils showing atmospheric methane uptake. Applied and Environmental Microbiology, 65(8), 3312-3318. https://doi.org/10.1128/AEM.65.8.3312-3318.1999.
  42. Knief C, Lipski A, Dunfield PF (2003) Diversity and activity of methanotrophic bacteria in different upland soils. Applied and Environmental Microbiology, 69(11), 6703-6714. https://doi.org/10.1128/AEM.69.11.6703-6714.2003.
  43. Horz HP, Rich V, Avrahami S and Bohannan BJ (2005) Methane-oxidizing bacteria in a California upland grassland soil: diversity and response to simulated global change. Applied and Environmental Microbiology, 71(5), 2642-2652. https://doi.org/10.1128/AEM.71.5.2642-2652.2005.
  44. Nazaries L, Murrell JC, Millard P, Baggs L, Singh BK (2013) Methane, microbes and models: fundamental understanding of the soil methane cycle for future predictions. Environmental Microbiology, 15(9), 2395-2417. https://doi.org/10.1111/1462-2920.12149.
  45. Lee HJ, Kim SY, Kim PJ, Madsen E, Jeon CO (2014) Methane emission and dynamics of methanotrophic and methanogenic communities in a flooded rice field ecosystem. FEMS Microbiology Ecology, 88(1), 195-212. https://doi.org/10.1111/1574-6941.12282.
  46. Seo J, Jang I, Gebauer G, Kang H (2014) Abundance of methanogens, methanotrophic bacteria, and denitrifiers in rice paddy soils. Wetlands, 34(2), 213-223. https://doi.org/10.1007/s13157-013-0477-y
  47. Cao M, Gregson K, Marshall S (1998) Global methane emission from wetlands and its sensitivity to climate change. Atmospheric Environment, 32(19), 3293-3299. https://doi.org/10.1016/S1352-2310(98)00105-8.
  48. Whalen SC (2005) Biogeochemistry of methane exchange between natural wetlands and the atmosphere. Environmental Engineering Science, 22(1), 73-94. https://doi.org/10.1089/ees.2005.22.73.
  49. Melton JR, Wania R, Hodson EL, Poulter B, Ringeval B, Spahni R, Kaplan JO (2013) Present state of global wetland extent and wetland methane modelling: conclusions from a model inter-comparison project (WETCHIMP). Biogeosciences, 10(2), 753-788. https://doi.org/10.5194/bg-10-753-2013
  50. Fernandez-Baca CP, Truhlar AM, Omar AEH, Rahm BG, Walter MT, Richardson RE (2018) Methane and nitrous oxide cycling microbial communities in soils above septic leach fields: abundances with depth and correlations with net surface emissions. Science of the Total Environment, 640, 429-441. https://doi.org/10.1016/j.scitotenv.2018.05.303.
  51. Tiwari S, Singh C, Singh JS (2020) Wetlands: a major natural source responsible for methane emission. In Restoration of Wetland Ecosystem: A Trajectory Towards a Sustainable Environment. Springer, Singapore. 59-74. https://doi.org/10.1007/978-981-13-7665-8_5.
  52. Janzen HH (2015) Beyond carbon sequestration: soil as conduit of solar energy. European Journal of Soil Science, 66(1), 19-32. https://doi.org/10.1111/ejss.12194.
  53. Zhu L, Li J, Tao B, Hu N (2015) Effect of different fertilization modes on soil organic carbon sequestration in paddy fields in South China: a meta-analysis. Ecological indicators, 53, 144-153. https://doi.org/10.1016/j.ecolind.2015.01.038.
  54. Alam MA, Rahman MM, Biswas JC, Akhter S, Maniruzzaman M, Choudhury AK, Kalra N (2019) Nitrogen transformation and carbon sequestration in wetland paddy field of Bangladesh. Paddy and Water Environment, 17(4), 677-688. https://doi.org/10.1007/s10333-019-00693-7.
  55. Lal R (2002) Soil carbon sequestration in China through agricultural intensification, and restoration of degraded and desertified ecosystems. Land Degradation & Development, 13(6), 469-478. https://doi.org/10.1002/ldr.531.
  56. Yin S, Zhang X, Lyu J, Zhi Y, Chen F, Wang L, Liu C, Zhou S (2020) Carbon sequestration and emissions mitigation in paddy fields based on the DNDC model: A review. Artificial Intelligence in Agriculture, 4, 140-149. https://doi.org/10.1016/j.aiia.2020.07.002.
  57. Pandey A, Dou F, Morgan CL, Guo J, Deng J, Schwab P (2021) Modeling organically fertilized flooded rice systems and its long term effects on grain yield and methane emissions. Science of The Total Environment, 755, 142578. https://doi.org/10.1016/j.scitotenv.2020.142578.
  58. Zheng Y, Zhang LM, Zheng YM, Di H, He JZ (2008) Abundance and community composition of methanotrophs in a Chinese paddy soil under long term fertilization practices. Journal of Soils and Sediments, 8(6), 406-414. https://doi.org/10.1007/s11368-008-0047-8.
  59. Tang HM, Xiao XP, Wang K, Li WY, Liu J, Sun JM (2016) Methane and nitrous oxide emissions as affected by long term fertilizer management from double-cropping paddy fields in Southern China. The Journal of Agricultural Science, 154(8), 1378-1391. https://doi.org/10.1017/S0021859615001355.
  60. Zhang W, Sheng R, Zhang M, Xiong G, Hou H, Li S, Wei W (2018) Effects of continuous manure application on methanogenic and methanotrophic communities and methane production potentials in rice paddy soil. Agriculture, Ecosystems & Environment, 258, 121-128. https://doi.org/10.1016/j.agee.2018.02.018.
  61. Zhang HM, Bo-Ren WANG, Ming-Gang XU, Ting-Lu FAN (2009) Crop yield and soil responses to long term fertilization on a red soil in southern China. Pedosphere, 19(2), 199-207. https://doi.org/10.1016/S1002-0160(09)60109-0.
  62. Ma L, Lin-Zhang Y, Li-Zhong X, Ming-Xing S, ShiXue Y, Yun-Dong L (2011). Long term effects of inorganic and organic amendments on organic carbon in a paddy soil of the Taihu Lake Region, China. Pedosphere, 21(2), 186-196. https://doi.org/10.1016/S1002-0160(11)60117-3.
  63. Guo Z, Han J, Li J, Xu Y, Wang X (2019) Effects of long term fertilization on soil organic carbon mineralization and microbial community structure. PLoS One, 14(1), e0211163. https://doi.org/10.1371/journal.pone.0211163.
  64. Yuan J, Sha ZM, Hassani D, Zhao Z, Cao LK (2017) Assessing environmental impacts of organic and inorganic fertilizer on daily and seasonal greenhouse gases effluxes in rice field. Atmospheric Environment, 155, 119-128. https://doi.org/10.1016/j.atmosenv.2017.02.007.
  65. McDonald IR, Murrell JC (1997) The methanol dehydrogenase structural gene mxaF and its use as a functional gene probe for methanotrophs and methylotrophs. Applied and Environmental Microbiology, 63(8), 3218-3224. https://doi.org/10.1128/aem.63.8.3218-3224.1997.
  66. Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Applied and Environmental Microbiology, 65(11), 5066-5074. https://doi.org/10.1128/AEM.65.11.5066-5074.1999.
  67. Henckel T, Friedrich M, Conrad R (1999) Molecular analyses of the methane-oxidizing microbial community in rice field soil by targeting the genes of the 16S rRNA, particulate methane monooxygenase, and methanol dehydrogenase. Applied and Environmental Microbiology, 65(5), 1980-1990. https://doi.org/10.1128/AEM.65.5.1980-1990.1999.
  68. Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology, 148(11), 3521-3530. https://doi.org/10.1099/00221287-148-11-3521.
  69. Steinberg LM, Regan JM (2008) Phylogenetic comparison of the methanogenic communities from an acidic, oligotrophic fen and an anaerobic digester treating municipal wastewater sludge. Applied and Environmental Microbiology, 74(21), 6663-6671. https://doi.org/10.1128/AEM.00553-08.
  70. Gadagi R, Park CY, Im GJ, Lee DC, Chung JB, Singvilay O, Sa TM (2001) Enzyme and microbial activities in paddy soil amended continuously with different fertilizer systems. Korean Journal of Environmental Agriculture, 20(5), 325-329.
  71. Kim S, Samaddar S, Chatterjee P, Roy Choudhury A, Choi J, Choi J, Sa T, (2021) Structural and functional shift in soil bacterial community in response to long term compost amendment in paddy field. Applied Sciences, 11(5), 2183. https://doi.org/10.3390/app11052183.
  72. Jiang Y, Qian H, Huang S, Zhang X, Wang L, Zhang L, Shen M, Xiao X, Chen F, Zhang H, Lu C, Li C, Zhang J, Deng A, Van Groenigen KJ, Zhang W (2019) Acclimation of methane emissions from rice paddy fields to straw addition. Science Advances, 5(1), eaau9038. https://doi.org/10.1126/sciadv.aau9038.
  73. Kong D, Li S, Jin Y, Wu S, Chen J, Hu T, Wang H, Liu S, Zou J (2019) Linking methane emissions to methanogenic and methanotrophic communities under different fertilization strategies in rice paddies. Geoderma, 347, 233-243. https://doi.org/10.1016/j.geoderma.2019.04.008.
  74. Islam MR, Chauhan PS, Kim YH, Kim MS, Sa TM (2011) Community level functional diversity and enzyme activities in paddy soils under different long term fertilizer management practices. Biology and Fertility of Soils, 47(5), 599-604. https://doi.org/10.1007/s00374-010-0524-2.
  75. Zheng J, Zhang X, Li L, Zhang P, Pan G (2007) Effect of long term fertilization on C mineralization and production of CH4 and CO2 under anaerobic incubation from bulk samples and particle size fractions of a typical paddy soil. Agriculture, Ecosystems & Environment, 120(2-4), 129-138. https://doi.org/10.1016/j.agee.2006.07.008.
  76. Dziewit L, Pyzik A, Romaniuk K, Sobczak A, Szczesny P, Lipinski L, Bartosik D, Drewniak L (2015) Novel molecular markers for the detection of methanogens and phylogenetic analyses of methanogenic communities. Frontiers in Microbiology, 6, 694. https://doi.org/10.3389/fmicb.2015.00694.
  77. Strong PJ, Kalyuzhnaya M, Silverman J, Clarke WP (2016) A methanotroph-based biorefinery: potential scenarios for generating multiple products from a single fermentation. Bioresource Technology, 215, 314-323. https://doi.org/10.1016/j.biortech.2016.04.099.
  78. Bodelier PL, Roslev P, Henckel T, Frenzel P (2000) Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots. Nature, 403(6768), 421-424. https://doi.org/10.1038/35000193.
  79. Shrestha M, Shrestha PM, Frenzel P, Conrad R (2010) Effect of nitrogen fertilization on methane oxidation, abundance, community structure, and gene expression of methanotrophs in the rice rhizosphere. The ISME Journal, 4(12), 1545-1556. https://doi.org/10.1038/ismej.2010.89.
  80. Alam, MS, Jia Z (2012) Inhibition of methane oxidation by nitrogenous fertilizers in a paddy soil. Frontiers in Microbiology, 3, 246. https://doi.org/10.3389/fmicb.2012.00246.
  81. Zhang J, Olatunji OA, Pan K, Jiang X, Meng Y, Li J, Li J, Shen S, Guo D, Luo H (2020) Ammonia-and Methane-Oxidizing Bacteria: The Abundance, Niches and Compositional Differences for Diverse Soil Layers in Three Flooded Paddy Fields. Sustainability, 12(3), 953. https://doi.org/10.3390/su12030953.
  82. Conrad R (1999) Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments. FEMS microbiology Ecology, 28(3), 193-202. https://doi.org/10.1111/j.1574-6941.1999.tb00575.x.
  83. Hakobyan A, Liesack W (2020) Unexpected metabolic versatility among type II methanotrophs in the Alpha-proteobacteria. Biological Chemistry, 401(12), 1469-1477. https://doi.org/10.1515/hsz-2020-0200.
  84. Bodelier PL, Laanbroek HJ (2004) Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiology Ecology, 47(3), 265-277. https://doi.org/10.1016/S0168-6496(03)00304-0.
  85. Cai Y, Zheng Y, Bodelier PL, Conrad R, Jia Z (2016) Conventional methanotrophs are responsible for atmospheric methane oxidation in paddy soils. Nature Communications, 7(1), 1-10. https://doi.org/10.1038/ncomms11728.
  86. Conrad R, Klose M, Noll M, Kemnitz D, Bodelier PL (2008) Soil type links microbial colonization of rice roots to methane emission. Global Change Biology, 14(3), 657-669. https://doi.org/10.1111/j.1365-2486.2007.01516.x.
  87. Kim SY, Pramanik P, Gutierrez J, Hwang HY, Kim PJ (2014) Comparison of methane emission characteristics in air-dried and composted cattle manure amended paddy soil during rice cultivation. Agriculture, Ecosystems & Environment, 197, 60-67. https://doi.org/10.1016/j.agee.2014.07.013.
  88. Freitag TE, Toet S, Ineson P, Prosser JI (2010) Links between methane flux and transcriptional activities of methanogens and methane oxidizers in a blanket peat bog. FEMS Microbiology Ecology, 73(1), 157-165. https://doi.org/10.1111/j.1574-6941.2010.00871.x.
  89. Kreye C, Dittert K, Zheng X, Zhang X, Lin S, Tao H, Sattelmacher B (2007) Fluxes of methane and nitrous oxide in water-saving rice production in north China. Nutrient Cycling in Agroecosystems, 77(3), 293-304. https://doi.org/10.1007/s10705-006-9068-0.
  90. Tang H, Xiao X, Li C, Tang W, Cheng K, Pan X, Wang K, Li W (2019) Effects of different soil tillage systems on soil carbon management index under double-cropping rice field in southern China. Agronomy Journal, 111(1), 440-447. https://doi.org/10.2134/agronj2018.06.0414.