Biochar decreases methanogenic archaea abundance and methane emissions in a flooded paddy soil

https://doi.org/10.1016/j.scitotenv.2020.141958Get rights and content

Highlights

  • Biochar reduced CH4 emissions for two rice seasons in a flooded paddy soil.

  • Decreased CH4 emissions was linked with decreased mcrA gene abundance.

  • Community structure of the pmoA gene had large interannual variation.

  • CH4 emissions were not related to pmoA gene abundance.

Abstract

Biochar addition can reduce methane (CH4) emissions from paddy soils while the mechanisms involved are not entirely clear. Here, we studied the effect of biochar addition on CH4 emissions, and the abundance and community composition of methanogens and methanotrophs over two rice cultivation seasons. The experiment had the following five treatments: control (CK), chemical fertilizer application only (BC0), and 0.5% (w/w) (BC1), 1% (BC2), and 2% of biochar applied with chemical fertilizers (BC3). The season-wide CH4 emissions were decreased (P < 0.05) by 22.2–95.7% in biochar application compared with BC0 in the two rice seasons (2017 and 2018). In 2017, biochar application decreased methanogenic archaea (mcrA) but increased methanotrophic bacteria (pmoA) abundances, and decreased the ratio of mcrA/pmoA, as compared with BC0 (P < 0.05). In 2018, the abundance of mcrA was lower in BC2 and BC3 than in BC0 (P < 0.05) but was not different between BC0 and BC1, and the abundance of pmoA was lower in BC1, BC2 and BC3 than in BC0 (P < 0.05). The CH4 emissions were positively related to abundances of the mcrA gene (P < 0.01) but not to that of the pmoA gene in two rice seasons. Rice grain yield was increased by 62.2–94.1% in biochar addition treatments compared with BC0 in the first year (P < 0.01) and by 29.9–37.6% in BC2 and BC3 compared with BC0 in the second year (P < 0.05). Biochar application decreased CH4 emissions by reducing methanogenic archaea abundance in the studied flooded paddy soil.

Introduction

Globally, agricultural management practices are responsible for substantial emissions of greenhouse gasses (GHGs), especially methane (CH4) emissions from rice production (van Loon et al., 2019). Rice is one of the world's most important staple food crops, and the global demand for rice will increase by 24% over the next 20 years (Haque et al., 2015). China is a major rice-cultivation country, producing 28.1% of the world's rice grain (Ding et al., 2018). As a result, Chinese rice paddies are a significant source of CH4 emissions, and techniques need to be developed to reduce CH4 emissions from rice paddies. A promising technique to reduce CH4 emissions from rice paddies is applying biochar to paddy fields (Feng et al., 2012; Wang et al., 2018). Biochar is produced from the pyrolysis of biomass, which can be a waste material or a byproduct from agriculture and forestry (Hagemann et al., 2017), and its application can increase soil porosity and the soil's sorption capacity for low molecular weight substances (Gul et al., 2015), and change soil redox properties (Klüpfel et al., 2014) and nutrient transformations (Hagemann et al., 2016). The application of biochar in rice cultivation has been widely used due to its potential for increasing carbon (C) sequestration in and reducing GHG emissions from agricultural soils (Lehmann, 2007; Wu et al., 2019b).

Effects of biochar on soil CH4 emissions were dependent on the application rate (Wang et al., 2018; Zhang et al., 2010); for example, CH4 emissions were not affected when biochar was applied at 10 Mg ha−1, but were increased at 40 Mg ha−1 in a paddy soil (Zhang et al., 2010). Our previous studies found that CH4 emissions were decreased when biochar was applied at 40 Mg ha−1 but were not affected when applied at or less than 20 Mg ha−1 in a paddy soil in a pot experiment (Qi et al., 2020b). In addition, we found that CH4 emissions were higher in biochar application than in chemical fertilizer application alone in the rice season following vegetable cultivation in a 2-year field study when biochar was applied at 10 Mg ha−1 every year (Qi et al., 2020a). The effect of biochar application rate on CH4 emissions may be attributed to changes in soil bulk density (Laird et al., 2010), surface area and presence of micropores in biochar-amended soils (Mukherjee and Lal, 2013), and microbial properties (Wang et al., 2019). In our previous studies, we also found that the CH4 emissions were affected by water irrigation management practices (Qi et al., 2018), soil temperature and labile organic C (Qi et al., 2020b) and land-use change (Qi et al., 2020a) in biochar-amended soils. However, in those earlier studies, we did not investigate the effect of interannual variation in CH4 emissions and the microbial control of CH4 emissions in biochar-amended rice paddy soils.

Biochar can reduce CH4 emissions by changing the microbial community (Feng et al., 2012; Liu et al., 2011b; Qin et al., 2016). Methanogens and methanotrophs regulate CH4 emissions in paddy soils (Conrad, 2007). Feng et al. (2012) and Qin et al. (2016) found significant decreases in CH4 emissions by biochar addition and explained the result by increases in methanotrophic bacteria biodiversity and abundance. Nevertheless, biochar application effects on methanotrophic abundance change over time following a single biochar application in a paddy field, and the reduction in CH4 emissions by biochar addition can be caused by the decrease in methanogenic relative to methanotrophic gene abundances (Wang et al., 2019). In addition, Cai et al. (2018) found that CH4 emissions were closely related to changes in methanogenic archaea genes rather than methanotrophic bacteria genes in a 45-day incubation experiment. Microbial properties should be studied for more than one rice season due to interannual variability resulting from changes in soil properties, including soil temperature (Brockett et al., 2012; Liu et al., 2010), and other factors that have large temporal variations (Sato and Sugimoto, 2013; Wang et al., 2018; Wang et al., 2019). However, few people have studied the effect of interannual variation on methanogenic and methanotrophic community structures in biochar-amended rice soils (Table S1).

The objectives of this study were to (1) assess the effect of biochar application rates on CH4 emissions, and the abundance and community structure of methanogenic archaea (mcrA) and methanotrophic bacteria (pmoA) genes that are related to CH4 emissions in a pot experiment of a paddy soil in two rice seasons; (2) investigate the effect of interannual variation in CH4 emissions, and the gene abundance and community structure of methanogens and methanotrophs.

Section snippets

Experimental design

The pot experiment was conducted over two rice seasons from March 2017 to September 2018 in a greenhouse at Southwest University. Each pot had a diameter 24.4 cm on the top end, and 21.0 cm on the bottom, and a height 23.0 cm. The soil used in this pot experiment was collected from an arable soil, which had a WHC of 30–50%, from an agricultural farm of Southwest University. Vegetables (beans and chili) were planted in the farm before the soil was collected. Each pot was filled with 6 kg

Effects of biochar application rates on soil properties and CH4 emissions

Soil pH was higher in BC3 than in BC0 and BC1 in both 2017 and 2018 (Table 2). The mean redox potential across each growing season was not different among treatments in 2017 and 2018. The SOC was higher in BC2 and BC3 than in BC0 in both 2017 and 2018. The DOC was not different among BC0, BC1, BC2, and BC3 in 2017 but was lower in BC3 than in BC0, BC1, and BC2 in 2018. The MBC was lower in BC0 and BC3 than in BC1 and BC2 in 2017 but was not different among BC0, BC1, BC2, and BC3 in 2018. The NH4

Discussion

Methane emissions decreased in all treatments with biochar addition as compared with the BC0 treatment in two rice seasons; such effects were linked with decreased methanogenic mcrA archaea abundance (Fig. 3a) rather than changes in the methanotrophic pmoA bacteria abundance (Fig. 3b); this is consistent with biochar having the potential to mitigate CH4 emissions in flooded soils reported in a meta-analysis (Jeffery et al., 2016). The continuous flooding water regime for rice cultivation in the

Conclusions

Methane emissions were decreased by 22.2–95.7% in biochar addition treatments compared with BC0 in the two rice seasons, which were linked with reductions in mcrA archaea abundance, and changes in rice aboveground biomass production, MBC, NH4+-N, NO3-N, AP, and soil temperature. The abundances of methanogens were lower in higher biochar addition (9 and 18 g kg−1) treatments than in BC0 in both rice seasons. The abundance of methanotrophs was increased in the first but decreased in the second

CRediT authorship contribution statement

Conceptualization: Le Qi and Ming Gao; Formal analysis and Methodology: Le Qi and Zilong Ma; Investigation and Data curation: Le Qi, Peng Zhou, Rong Huang and Yingyan Wang; Resources and Supervision: Ming Gao, Scott X. Chang and Zifang Wang; Writing: Le Qi, Zilong Ma and Scott X. Chang. The manuscript was prepared by Le Qi with the assistance of Zilong Ma and was revised and reviewed by Scott X. Chang and Ming Gao.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We would like to acknowledge funding from the National “Five-Year” Key Research and Development Program (No. 2017YFD0800101), National Key Water Conservancy Construction Fund of the Three Gorges Follow-up Research Program (No. 5001022019CF50001), the State Cultivation Base of Eco-agriculture for Southwest Mountainous Land, the China Scholarship Council, Chongqing Graduate Student Research Innovation Program (CYB18091), and the National College Students Innovation and Entrepreneurship Training

References (55)

  • D.A. Laird et al.

    Impact of biochar amendments on the quality of a typical Midwestern agricultural soil

    Geoderma

    (2010)
  • W. Liu et al.

    Interannual variability of soil microbial biomass and respiration in responses to topography, annual burning and N addition in a semiarid temperate steppe

    Geoderma

    (2010)
  • J. Liu et al.

    Seasonal soil CO2 efflux dynamics after land use change from a natural forest to Moso bamboo plantations in subtropical China

    Forest Ecol. Manag.

    (2011)
  • X. Liu et al.

    Impact of biochar application on yield-scaled greenhouse gas intensity: a meta-analysis

    Sci. Total Environ.

    (2019)
  • P. Pokharel et al.

    Pine sawdust biochar reduces GHG emission by decreasing microbial and enzyme activities in forest and grassland soils in a laboratory experiment

    Sci. Total Environ.

    (2018)
  • L. Qi et al.

    Biochar application increased methane emission, soil carbon storage and net ecosystem carbon budget in a 2-year vegetable–rice rotation

    Agric. Ecosyst. Environ.

    (2020)
  • L. Qi et al.

    Biochar changes thermal activation of greenhouse gas emissions in a rice–lettuce rotation microcosm experiment

    J. Clean. Prod.

    (2020)
  • X. Qin et al.

    Long-term effect of biochar application on yield-scaled greenhouse gas emissions in a rice paddy cropping system: a four-year case study in south China

    Sci. Total Environ.

    (2016)
  • R.S. Quilliam et al.

    Life in the ‘charosphere’-does biochar in agricultural soil provide a significant habitat for microorganisms?

    Soil Biol. Biochem.

    (2013)
  • T.T. Tuomivirta et al.

    Quantitative PCR of pmoA using a novel reverse primer correlates with potential methane oxidation in Finnish fen

    Res. Microbiol.

    (2009)
  • N. Wang et al.

    Biochar decreases nitrogen oxide and enhances methane emissions via altering microbial community composition of anaerobic paddy soil

    Sci. Total Environ.

    (2017)
  • C. Wang et al.

    Effects of biochar amendment on net greenhouse gas emissions and soil fertility in a double rice cropping system: a 4-year field experiment

    Agric. Ecosyst. Environ.

    (2018)
  • C. Wang et al.

    Microbial mechanisms in the reduction of CH4 emission from double rice cropping system amended by biochar: a four-year study

    Soil Biol. Biochem.

    (2019)
  • Z. Wu et al.

    Biochar can mitigate methane emissions by improving methanotrophs for prolonged period in fertilized paddy soils

    Environ. Pollut.

    (2019)
  • Z. Wu et al.

    Biochar amendment reduced greenhouse gas intensities in the rice-wheat rotation system: six-year field observation and meta-analysis

    Agric. For. Meteorol.

    (2019)
  • A. Zhang et al.

    Effect of biochar amendment on yield and methane and nitrous oxide emissions from a rice paddy from Tai Lake plain, China

    Agric. Ecosyst. Environ.

    (2010)
  • A.R. Zimmerman et al.

    Positive and negative carbon mineralization priming effects among a variety of biochar-amended soils

    Soil Biol. Biochem.

    (2011)
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