Skip to main content

Advertisement

Log in

Mitigation of yield-scaled greenhouse gas emissions from irrigated rice through Azolla, Blue-green algae, and plant growth–promoting bacteria

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Irrigated transplanted flooded rice is a major source of methane (CH4) emission. We carried out experiments for 2 years in irrigated flooded rice to study if interventions like methane-utilizing bacteria, Blue-green algae (BGA), and Azolla could mitigate the emission of CH4 and nitrous oxide (N2O) and lower the yield-scaled global warming potential (GWP). The experiment included nine treatments: T1 (120 kg N ha−1 urea), T2 (90 kg N ha−1 urea + 30 kg N ha−1 fresh Azolla), T3 (90 kg N ha−1 urea + 30 kg N ha−1 Blue-green algae (BGA), T4 (60 kg N ha−1 urea + 30 kg N ha−1 BGA + 30 kg N ha−1 Azolla, T5 (120 kg N ha−1 urea + Hyphomicrobium facile MaAL69), T6 (120 kg N ha−1 by urea + Burkholderia vietnamiensis AAAr40), T7 (120 kg N ha−1 by urea + Methylobacteruim oryzae MNL7), T8 (120 kg N ha−1 urea + combination of Burkholderia AAAr40, Hyphomicrobium facile MaAL69, Methylobacteruim oryzae MNL7), and T9 (no N fertilizer). Maximum decrease in cumulative CH4 emission was observed with the application of Methylobacteruim oryzae MNL7 in T7 (19.9%), followed by Azolla + BGA in T4 (13.2%) as compared to T1 control. N2O emissions were not significantly affected by the application of CH4-oxidizing bacteria. However, significantly lower (P<0.01) cumulative N2O emissions was observed in T4 (40.7%) among the fertilized treatments. Highest yields were observed in Azolla treatment T2 with 25% less urea N application. The reduction in yield-scaled GWP was at par in T4 (Azolla and BGA) and T7 (Methylobacteruim oryzae MNL7) treatments and reduced by 27.4% and 15.2% in T4 and T7, respectively, as compared to the T1 (control). K-means clustering analysis showed that the application of Methylobacteruim oryzae MNL7, Azolla, and Azolla + BGA can be an effective mitigation option to reduce the global warming potential while increasing the yield.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

All relevant data are within the manuscript and available from the corresponding author on request.

References

  • Adhya TK, Bharati K, Mohanty SR, Ramakrishnan B, Rao VR, Sethunthan N, Wassmann R (2000) Methane emission from rice fields at Cuttack, India. Nutr.Cycl.Agroecosys. 58:95–105

    Article  CAS  Google Scholar 

  • Ali MA, Farouque MG, Haque M, Kabir AU (2012) Influence of soil amendments on mitigating methane emissions and sustaining rice productivity in paddy soil ecosystems of Bangladesh. J Environ Sci Nat Resour 5:179–185

    Google Scholar 

  • Ali MA, Kim PJ, Inubushi K (2015) Mitigating yield-scaled greenhouse gas emissions through combined application of soil amendments: a comparative study between temperate and subtropical rice paddy soils. Sci Total Environ 529:140–148

    Article  CAS  Google Scholar 

  • Aliyu G, Jiafa LUO, Deyan LIU, Junji YUAN, Zengming CHEN, Tiehu HE, Weixin DING (2021) Yield-scaled nitrous oxide emissions from nitrogen-fertilized croplands in China: a meta-analysis of contrasting mitigation scenarios. Pedosphere 31(2 (2021)):231–242

    Article  Google Scholar 

  • Aulakh MS, Bodenbender J, Wassmann R, Rennenberg H (2000) Methane trasport capacity of rice plants. II. In variations among different rice cultivars and relationship with morphological characteristics. Nutr Cycl Agroecosyst 58:367–375

    Article  CAS  Google Scholar 

  • Bédard C, Knowles R (1989) Physiology, biochemistry, and specific inhibitors of CH4, NH4+, and CO oxidation by methanotrophs and nitrifiers. Microbiol Rev 53:68–84. https://doi.org/10.1128/mmbr.53.1.68-84.1989

    Article  Google Scholar 

  • Bharati K, Mohanty SR, Singh DP, Rao VR, Adhya TK (2000) Influence of incorporation or dual cropping of Azolla on methane emission from a flooded alluvial soil planted to rice in eastern India. Agric Ecosyst Environ 79:73–83

    Article  CAS  Google Scholar 

  • Bhatia A, Pathak H, Jain N, Singh PK, Singh AK (2005) Global warming potential of manure amended soils under rice–wheat system in the Indo-Gangetic plains. Atmos Environ 39:6976–6984

    Article  CAS  Google Scholar 

  • Bhatia A, Ghosh A, Kumar V, Tomer R, Singh SD, Pathak H (2011) Effect of elevated tropospheric ozone on methane and nitrous oxide emission from rice soil in north India. Agric Ecosyst Environ 144:21–28

    Article  CAS  Google Scholar 

  • Bhatia A, Pathak H, Jain N, Singh PK, Tomer R (2012) Greenhouse gas mitigation in rice–wheat system with leaf color chart-based urea application. Environ Monit Assess 184(5):3095–3107

    Article  CAS  Google Scholar 

  • Bhatia A, Kumar A, Das TK, Singh J, Jain N, Pathak H (2013) Methane and nitrous oxide emissions from soils under direct seeded rice. Int J Agric Stat Sci 9(2):729–736

    Google Scholar 

  • Bhattacharyya P, Dash PK, Swain CK, Padhy SR, Roy KS, Neogi S, Berliner J, Adak T, Pokhare SS, Baig MJ, Mohapatra T (2019) Mechanism of plant mediated methane emission in tropical lowland rice. Sci Total Environ 651:84–92

    Article  CAS  Google Scholar 

  • Bremner JM (1997) Sources of nitrous oxide in soils. Nutr Cycl Agroecosyst 49(7):16

    Google Scholar 

  • Chen GX, Huang GH, Huang B, Yu KW, Wu J, Xu H (1997) Nitrous oxide and methane emissions from soil–plant systems. Nutr Cycl Agroecosyst 49:41–45

    Article  CAS  Google Scholar 

  • Choudhaury ATMA, Kennedy IR (2005) Nitrogen fertilizer losses from rice soils and control of environmental pollution problems. Commun Soil Sci Plant Anal 36:1625–1639

    Article  CAS  Google Scholar 

  • Conrad R (2007) Microbial ecology of methanogens and methanotrophs. Adv Agron 96:1–63

    Article  CAS  Google Scholar 

  • Das S, Adhya TK (2014) Effect of combine application of organic manure and inorganic fertilizer on methane and nitrous oxide emissions from a tropical flooded soil planted to rice. Geoderma. 213:185–192

    Article  CAS  Google Scholar 

  • Datta A, Yeluripati JB, Nayak DR, Mahata KR, Santra SC, Adhya TK (2013) Seasonal variation of methane flux from coastal saline rice field with the application of different organic manures. Atmos Environ 66:114–122

    Article  CAS  Google Scholar 

  • Davamani V, Parameswari E, Arulmani S (2020) Mitigation of methane gas emissions in flooded paddy soil through the utilization of methanotrophs. Sci Total Environ 726:138570. https://doi.org/10.1016/j.scitotenv.2020.138570

    Article  CAS  Google Scholar 

  • Dedysh SN, Dunfield PF (2011) Facultative and obligate methanotrophs: how to identify and differentiate them. Methods Enzymol 495:31–44

    Article  CAS  Google Scholar 

  • Dong H, Yao Z, Zheng X, Mei B, Xie B, Wang R, Deng J, Cui F, Zhu J (2011) Effect of ammonium-based, non-sulfate fertilizers on CH4 emissions from a paddy field with a typical Chinese water management regime. Atmos Environ 45:1095–1101

    Article  CAS  Google Scholar 

  • Dubey SK (2005) Microbial ecology of methane emission in rice agroecosystem: a review. Appl Ecol Environ Res 3:1–27

    Article  Google Scholar 

  • Dubey SK, Singh JS (2001) Plant-induced spatial variations in the size of methanotrophic population in dryland and flooded rice agroecosystems. Nutr Cycl Agroecosyst 59:161–167

    Article  Google Scholar 

  • Gupta DK, Bhatia A, Kumar A, Das TK, Jain N, Tomer R, Malyan SK, Fagodiya RK, Dubey R, Pathak H (2016) Mitigation of greenhouse gas emission from rice–wheat system of the Indo-Gangetic plains: through tillage, irrigation and fertilizer management. Agric Ecosyst Environ 230:1–9

    Article  CAS  Google Scholar 

  • Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471

    Article  CAS  Google Scholar 

  • Hussain S, Peng S, Fahad S, Khaliq A, Huang J, Cui K, Nie L (2015) Rice management interventions to mitigate greenhouse gas emissions: a review. Environ Sci Pollut Res 22:3342–3360

    Article  Google Scholar 

  • Iguchi H, Yurimoto H, Sakai Y (2015) Interactions of methylotrophs with plants and other heterotrophic bacteria. Microorganisms. 3:137–151

    Article  CAS  Google Scholar 

  • Inubushi K, Naganuma H, Kitahara S (1996) Contribution of denitrification and autotrophic and heterotrophic nitrification to nitrous oxide production in andosols. Biol Fertil Soils 23:292–298

    Article  CAS  Google Scholar 

  • IPCC (2014) Climate Change 2014: Impacts, Adaptation, and Vulnerability Working Group II Contribution to the Fifth Assessment Report. Cambridge University Press, Cambridge, UK and New York, NY USA

    Google Scholar 

  • Jain N, Arora P, Tomer R, Vind S, Bhatia A, Pathak H, Chakraborty D, Kumar V, Dubey DS, Harit RC, Singh JP (2016) Greenhouse gases emission from soils under major crops in Northwest India. Sci Total Environ 542:551–561

    Article  CAS  Google Scholar 

  • Kantachote D, Nunkaew T, Kantha T, Chaiprapat S (2016) Biofertilizers from Rhodopseudomonas palustris strains to enhance rice yields and reduce methane emissions. Appl Soil Ecol 100:154–161

    Article  Google Scholar 

  • Kim Y, Talucder MSA, Kang M, Shim K-M, Kang N, Kim J (2016) Interannual variations in methane emission from an irrigated rice paddy caused by rainfalls during the aeration period. Agric Ecosyst Environ 223:67–75

  • Kimani SM, Cheng W, Kanno T, Nguyen-Sy T, Abe R, Oo AZ, Tawaraya K, Sudo S (2018) Azolla cover significantly decreased CH4 but not N2O emissions from flooding rice paddy to atmosphere. J Soil Sci Plant Nutr 64:68–76

    Article  CAS  Google Scholar 

  • Kollah B, Patra AK, Mohanty SR (2016) Aquatic microphylla Azolla: a perspective paradigm for sustainable agriculture, environment and global climate change. Environ Sci Pollut Res 23:4358–4369

    Article  CAS  Google Scholar 

  • Kumar A, Medhi K, Fagodiya KR, Subrahmanyam G, Mondal R, Raja P, Malyan SK, Gupta DK, Gupta CK, Pathak H (2020) Molecular and ecological perspectives of nitrous oxide producing microbial communities in agro-ecosystems. Rev Environ Sci Biotechnol 19(4):717–750

  • Ladha JK, Pathak H, Krupnik TJ, Six J, Kessel C (2005) Efficiency of fertilizer nitrogen in cereal production: retrospects and prospects. Adv Agron 87:85–156

    Article  CAS  Google Scholar 

  • Liessens J, Germonpre R, Kersters I, Beernaert S, Verstraete W (1993) Removing nitrate with a methylotrophic fluidized bed: microbiological water quality. J Am Water Works Assoc 85:155–161

    Article  CAS  Google Scholar 

  • Liu J, Xu H, Jiang Y, Zhang K, Hu Y, Zeng Z (2017) Methane emissions and microbial communities as influenced by dual cropping of Azolla along with early rice. Sci Rep 7:40635

    Article  CAS  Google Scholar 

  • Ma YY, Tong G, Wang WQ, Zeng CS (2012) Effect of Azolla on CH4 and N2O emissions in Fuzhou Plain paddy fields.pdf. Chin J Eco-Agric 20:723–727

    Article  CAS  Google Scholar 

  • Malla G, Bhatia A, Pathak H, Prasad S, Jain N, Singh J, Kumar V (2005) Mitigating nitrous oxide and methane emissions from soil under rice–wheat system with nitrification inhibitors. Chemosphere 58:141–147. https://doi.org/10.1016/j.chemosphere.2004.09.003

    Article  CAS  Google Scholar 

  • Malyan SK, Bhatia A, Kumar A, Gupta DK, Singh R, Kumar SS, Tomer R, Kumar O, Jain N (2016) Methane production, oxidation and mitigation: a mechanistic understanding and comprehensive evaluation of influencing factors. Sci Total Environ 572:874–896

    Article  CAS  Google Scholar 

  • Malyan SK, Bhatia A, Kumar SS, Fagodiya RK, Pugazhendhi A, Duc PA (2019) Mitigation of greenhouse gas intensity by supplementing with Azolla and moderating the dose of nitrogen fertilizer. Biocatal Agric Biotechnol 20:101266

    Article  Google Scholar 

  • McDonald IR, Doronina NV, Trotsenko YA, McAnulla C, Murrell JC (2002) Hyphomicrobium chloromethanicum sp. nov. and Methylobacterium chloromethanicum sp. nov., chloromethane-utilizing bacteria isolated from a polluted environment. Int J Syst Evol Microbiol 51(Pt 1):119–122. https://doi.org/10.1099/00207713-51-1-119

  • Moldenhauer KEWC, Slaton N (2001) Rice growth and development. Rice production handbook, pp 7–14

    Google Scholar 

  • Pathak H, Bhatia A, Prasad S, Kumar S, Jain MC, Kumar U (2002) Emission of nitrous oxide from rice–wheat systems of Indo-Gangetic Plains of India. Environ Monit Assess 77:163–178

    Article  CAS  Google Scholar 

  • Pathak H, Prasad S, Bhatia A, Singh S, Kumar S, Singh J, Jain MC (2003) Methane emission from rice–wheat cropping system in the Indo-Gangetic plain in relation to irrigation, farmyard manure and dicyandiamide application. Agric Ecosyst Environ 97(1-3):309–316

  • Prasanna R, Kumar V, Kumar S, Yadav AK, Tripathi U, Singh AK, Jain MC, Gupta P, Singh PK, Sethunathan N (2002) Methane production in rice soil is inhibited by cyanobacteria. Microbiol Res 157:1–6

    Article  Google Scholar 

  • Rani V, Bhatia A, Kaushik R (2021a) Inoculation of plant growth promoting-methane utilizing bacteria in different N-fertilizer regime influences methane emission and crop growth of flooded paddy. Sci Total Environ 145826. https://doi.org/10.1099/00221287-61-2-205

  • Rani V, Bhatia A, Nain L, Tomar GS, Kaushik R (2021b) Methane utilizing plant growth-promoting microbial diversity analysis of flooded paddy ecosystem of India. World J Microbiol Biotechnol 37(4):1–22

    Article  CAS  Google Scholar 

  • Ritchie H, Roser M (2018) CO2 and other greenhouse gas emissions. Published online at OurWorldInData.org. Retrieved from: https://ourworldindata.org/co2-and-other-greenhouse-gas-emissions. Accessed Dec 2019

  • Sass RL, Cicerone RJ (2002) Photosynthate allocations in rice plants: food production or atmospheric methane? Proc Natl Acad Sci U S A 99(19):11993–11995

    Article  CAS  Google Scholar 

  • Schimel J (2000) Rice, microbes and methane. Nature. 403:375–377

    Article  CAS  Google Scholar 

  • Shin D, Lee S, Kim TH, Lee JH, Park J, Lee J, Nam HG (2020) Natural variations at the Stay-Green gene promoter control lifespan and yield in rice cultivars. Nat Commun 11(1):1–11

    Article  CAS  Google Scholar 

  • Singh SK, Bharadwaj V, Thakur TC, Pachauri PC, Singh PP, Mishra AK (2009) Influence of crop establishment methods on methane emission from rice fields. Curr Sci 97:84–89

    CAS  Google Scholar 

  • Tan W, Yu H, Huang C, Li D, Zhang H, Jia Y, Wang G, Xi B (2018) Discrepant responses of methane emissions to additions with different organic compound classes of rice straw in paddy soil. Sci Total Environ 630:141–145

    Article  CAS  Google Scholar 

  • Tariq A, Vu QD, Jensen SL, Tourdonnet S, Sander OB, Wassmann R, Mai TV, Neergaard A (2017) Mitigating CH4 and N2O emissions from intensive rice production systems in northern Vietnam: efficiency of drainage patterns in combination with rice residue incorporation. Agric Ecosyst Environ 249:101–111

    Article  CAS  Google Scholar 

  • Theisen AR, Murrell JC (2005) GUEST COMMENTARY Facultative Methanotrophs Revisited. Society 187:4303–4305

    CAS  Google Scholar 

  • Tyler SC, Bilek RS, Sass RL, Fisher FM (1997) Methane oxidation and pathways of production in a Texas paddy field deduced from measurements of flux, delta-C-13, and delta-D of CH4. Glob Biogeochem Cycles 11:323–348

    Article  CAS  Google Scholar 

  • Van Aken B, Peres CM, Doty SL, Yoon JM, Schnoor JL (2004) Methylobacterium populi sp. nov., a novel aerobic, pink-pigmented, facultatively methylotrophic, methane-utilizing bacterium isolated from poplar trees (Populus deltoides x nigra DN34). Int J Syst Evol Microbiol 54:1191–1196

    Article  CAS  Google Scholar 

  • Wagner GM (1997) Azolla: a review of its biology and utilization. Bot Rev 63:1–26

    Article  Google Scholar 

  • Whittenbury R, Davies SL, Wilkinson JF (1970) Enrichment, isolation and some properties of methane-utilizing bacteria. J Gen Microbiol 61:205–218. https://doi.org/10.1099/00221287-61-2-205

    Article  CAS  Google Scholar 

  • Xie B, Zheng X, Zhou Z, Gu J, Zhu B, Chen X (2010) Effects of nitrogen fertilizer on CH4 emission from rice fields: multi-site field observations. Plant Soil 326:393–401

    Article  CAS  Google Scholar 

  • Xu H, Zhu B, Liu J, Li D, Yang Y, Zhang K, Jiang Y, Hu Y, Zeng Z (2017) Azolla planting reduces methane emission and nitrogen fertilizer application in double rice cropping system in southern China. Agron Sustain Dev 37. https://doi.org/10.1007/s13593-017-0440-z

  • Yao Z, Zheng X, Wang R, Liu C, Lin S, Butterbach-Bahl K (2019) Benefits of integrated nutrient management on N2O and NO mitigations in water-saving ground cover rice production systems. Sci Total Environ 646:1155–1163

    Article  CAS  Google Scholar 

  • Ying Z, Boeckx P, Chen GX, Cleemput OV (2000) Influence of Azolla on CH4 emission from rice fields. Nutr.Cycl.Agroecosyst. 58:321–326

    Article  CAS  Google Scholar 

  • Yu, K., Wang, Z., Vermoesen, A., Patrick Jr, W. and Van Cleemput, O., 2001. Nitrous oxide and methane emissions from different soil suspensions: effects of soil redox status.

    Google Scholar 

  • Zhao X, Pu C, Ma ST, Liu SL, Xue JF, Wang X, Wang YQ, Li SS, Lal R, Chen F, Zhang HL (2019) Management-induced greenhouse gases emission mitigation in global rice production. Sci Total Environ 649:1299–1306

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Director, Dean, and PG School of Indian Agricultural Research Institute, New Delhi for providing all facilities required in this study. We are also thankful to Head, Dr. G. Abraham and Dr. Sunil Pabbi, Division of Microbiology, IARI, for providing Azolla and BGA for experimentation. Financial support to S.K.M. during Ph.D. as UGC-JRF/SRF provided by University Grant Commission (UGC) is gratefully acknowledged. This study has been supported by the grant of National Innovations in Climate Resilient Agriculture (NICRA, IARI/112-15) project.

Author information

Authors and Affiliations

Authors

Contributions

S.K.M.: investigation, writing—original draft. A.B.: conceptualization, supervision, writing—review and editing. R.T.: sample analysis. R.C.H.: field management. A.B.: statistical analysis. N.J.: writing—initial draft. R.K.: conceptualization, supervision.

Corresponding author

Correspondence to Arti Bhatia.

Ethics declarations

Ethical approval

Not applicable.

Consent for participate

The authors have agreed with the content and all have given consent to publish.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Malyan, S.K., Bhatia, A., Tomer, R. et al. Mitigation of yield-scaled greenhouse gas emissions from irrigated rice through Azolla, Blue-green algae, and plant growth–promoting bacteria. Environ Sci Pollut Res 28, 51425–51439 (2021). https://doi.org/10.1007/s11356-021-14210-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-14210-z

Keywords

Navigation