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Inhibitory effect of high nitrate on N2O reduction is offset by long moist spells in heavily N loaded arable soils

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Abstract

Numerous interrelated factors (e.g., the labile C, soil NO3− concentration, and soil moisture content) are involved in controlling the microbial sources of N2O and the product stoichiometry of denitrification; however, the interactions among different factors are still poorly understood. Here, a fully robotized continuous flow soil incubation system (allowing simultaneous measurements of N2 and N2O fluxes) was employed to investigate the interactive effects of a 51-day duration of moist spell, straw amendment, and the NO3− level on the rate and product stoichiometry (N2O/(N2O + N2) ratio) of denitrification in heavily N loaded arable soils (i.e., paddy, vegetable, and orchard soils). The rewetting-induced N2O emissions mainly originated from bacterial denitrification in all soil types, with a clear shift to fungal denitrification (plus contingent nitrification) over time. The vegetable and orchard soils showed a higher share of bacterial N2O (62–70%) than that in the paddy soils (50–54%), which may be attributed to more labile-C driven bacterial activity induced by the greater manure and crop residue input therein. Interestingly, the inhibitory effect of high soil NO3− on N2O reduction in these soils was offset by a 51-day-long moist spell, regardless of the amendment of straw. To our knowledge, our study is the first to show that the inhibitory effect of high residual NO3− on N2O reduction is suppressed by a moist spell with a certain duration in heavily N loaded arable soils, suggesting that the water regime history should be considered when optimizing the N fertilizer application timing to mitigate soil N2O emissions.

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References

  • Baggs EM (2011) Soil microbial sources of nitrous oxide: recent advances in knowledge, emerging challenges and future direction. Curr Opin Environ Sustain 3:321–327

    Article  Google Scholar 

  • Buchen C, Lewicka-Szczebak D, Flessa H, Well R (2018) Estimating N2O processes during grassland renewal and grassland conversion to maize cropping using N2O isotopocules. Rapid Commun Mass Spectrom 32:1053–1067

    Article  CAS  PubMed  Google Scholar 

  • Butterbach-Bahl K, Baggs EM, Dannenmann M, Kiese R, Zechmeister-Boltenstern S (2013) Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos Trans R Soc B-Biol Sci 368:20130122

    Article  Google Scholar 

  • Cárdenas LM, Hawkins JMB, Chadwick D, Scholefield D (2003) Biogenic gas emissions from soils measured using a new automated laboratory incubation system. Soil Biol Biochem 35:867–870

    Article  Google Scholar 

  • Chee-Sanford JC, Connor L, Krichels A, Yang WH, Sanford RA (2020) Hierarchical detection of diverse Clade II (atypical) nosZ genes using new primer sets for classical- and multiplex PCR array applications. J Microbiol Methods 172:105908

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Mothapo NV, Shi W (2014) The significant contribution of fungi to soil N2O production across diverse ecosystems. Appl Soil Ecol 73:70–77

    Article  Google Scholar 

  • Ciarlo E, Conti M, Bartoloni N, Rubio G (2007) The effect of moisture on nitrous oxide emissions from soil and the N2O/(N2O+N2) ratio under laboratory conditions. Biol Fertil Soils 43:675–681

    Article  CAS  Google Scholar 

  • Decock C, Six J (2013) How reliable is the intramolecular distribution of 15N in N2O to source partition N2O emitted from soil? Soil Biol Biochem 65:114–127

    Article  CAS  Google Scholar 

  • Domeignoz-Horta L, Spor A, Bru D, Breuil m-c, Bizouard F, Leonard J, Philippot L (2015) The diversity of the N2O reducers matters for the N2O:N2 denitrification end–product ratio across an annual and a perennial cropping system. Front Microbiol 6:971

    Article  PubMed  PubMed Central  Google Scholar 

  • Firestone MK (1982) Biological Denitrification. In: Stevenson FJ (Ed) Nitrogen in agricultural soils. agronomy monographs. American Society Agronomy, Crop Science Society of America and Soil Science Society of American, Nitrogen in Agricultural Soils, Madison, WI, pp 289–326

  • Firestone MK, Tiedje JM (1979) Temporal change in nitrous oxide and dinitrogen from denitrification following onset of anaerobiosis. Appl Environ Microbiol 38:673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frame CH, Casciotti KL (2010) Biogeochemical controls and isotopic signatures of nitrous oxide production by a marine ammonia-oxidizing bacterium. Biogeosciences 7:2695–2709

    Article  CAS  Google Scholar 

  • Giles M, Morley N, Baggs E, Daniell T (2012) Soil nitrate reducing processes–drivers, mechanisms for spatial variation, and significance for nitrous oxide production. Front Microbiol 3:407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hallin S, Philippot L, Löffler FE, Sanford RA, Jones CM (2018) Genomics and ecology of novel N2O-reducing microorganisms. Trends Microbiol 26:43–55

    Article  CAS  PubMed  Google Scholar 

  • Hayatsu M, Tago K, Saito M (2008) Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci Plant Nutr 54:33–45

    Article  CAS  Google Scholar 

  • Hayden HL, Mele PM, Bougoure DS, Allan CY, Norng S, Piceno YM, Brodie EL, DeSantis TZ, Andersen GL, Williams AL, Hovenden MJ (2012) Changes in the microbial community structure of bacteria, archaea and fungi in response to elevated CO2 and warming in an Australian native grassland soil. Environ Microbiol 14:3081–3096

    Article  CAS  PubMed  Google Scholar 

  • Henriksen TM, Breland TA (2002) Carbon mineralization, fungal and bacterial growth, and enzyme activities as affected by contact between crop residues and soil. Biol Fertil Soils 35:41–48

    Article  CAS  Google Scholar 

  • Herold MB, Baggs EM, Daniell TJ (2012) Fungal and bacterial denitrification are differently affected by long-term pH amendment and cultivation of arable soil. Soil Biol Biochem 54:25–35

    Article  CAS  Google Scholar 

  • Holtan-Hartwig L, Dörsch P, Bakken LR (2000) Comparison of denitrifying communities in organic soils: kinetics of NO3− and N2O reduction. Soil Biol Biochem 32:833–843

    Article  CAS  Google Scholar 

  • Hu X, Liu J, Wei D, Zhu P, Cui X, Zhou B, Chen X, Jin J, Liu X, Wang G (2020) Chronic effects of different fertilization regimes on nirS-type denitrifier communities across the black soil region of Northeast China. Pedosphere 30:73–86

    Article  Google Scholar 

  • Kessavalou A, Mosier AR, Doran JW, Drijber RA, Lyon DJ, Heinemeyer O (1998) Fluxes of carbon dioxide, nitrous oxide, and methane in grass sod and winter wheat-fallow tillage management. J Environ Qual 27:1094–1104

    Article  CAS  Google Scholar 

  • Kim D-G, Mishurov M, Kiely G (2010) Effect of increased N use and dry periods on N2O emission from a fertilized grassland. Nutr Cycl Agroecosyst 88:397–410

    Article  CAS  Google Scholar 

  • Köster JR, Well R, Dittert K, Giesemann A, Lewicka-Szczebak D, Mühling K-H, Herrmann A, Lammel J, Senbayram M (2013) Soil denitrification potential and its influence on N2O reduction and N2O isotopomer ratios. Rapid Commun Mass Spectrom 27:2363–2373

    Article  PubMed  Google Scholar 

  • Lagomarsino A, Agnelli AE, Linquist B, Adviento-Borbe MA, Agnelli A, Gavina G, Ravaglia S, Ferrara RM (2016) Alternate wetting and drying of rice reduced CH4 emissions but triggered N2O peaks in a clayey soil of Central Italy. Pedosphere 26:533–548

    Article  CAS  Google Scholar 

  • Laughlin RJ, Stevens RJ (2002) Evidence for fungal dominance of denitrification and codenitrification in a grassland soil. Soil Sci Soc Am J 66:1540–1548

    Article  CAS  Google Scholar 

  • Lewicka-Szczebak D, Augustin J, Giesemann A, Well R (2017) Quantifying N2O reduction to N2 based on N2O isotopocules—validation with independent methods (helium incubation and 15N gas flux method). Biogeosciences 14:711–732

    Article  CAS  Google Scholar 

  • Lewicka-Szczebak D, Well R, Köster JR, Fuß R, Senbayram M, Dittert K, Flessa H (2014) Experimental determinations of isotopic fractionation factors associated with N2O production and reduction during denitrification in soils. Geochim Cosmochim Acta 134:55–73

    Article  CAS  Google Scholar 

  • Liu B, Mørkved PT, Frostegård Å, Bakken LR (2010) Denitrification gene pools, transcription and kinetics of NO, N2O and N2 production as affected by soil pH. FEMS Microbiol Ecol 72:407–417

    Article  CAS  PubMed  Google Scholar 

  • Ma S, Shan J, Yan X (2017) N2O emissions dominated by fungi in an intensively managed vegetable field converted from wheat–rice rotation. Appl Soil Ecol 116:23–29

    Article  CAS  Google Scholar 

  • Molstad L, Dörsch P, Bakken LR (2007) Robotized incubation system for monitoring gases (O2, NO, N2O N2) in denitrifying cultures. J Microbiol Methods 71:202–211

    Article  CAS  PubMed  Google Scholar 

  • Mørkved PT, Dörsch P, Bakken LR (2007) The N2O product ratio of nitrification and its dependence on long-term changes in soil pH. Soil Biol Biochem 39:2048–2057

    Article  Google Scholar 

  • Ohtonen R, Fritze H, Pennanen T, Jumpponen A, Trappe J (1999) Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 119:239–246

    Article  PubMed  Google Scholar 

  • Orellana LH, Rodriguez-R LM, Higgins S, Chee-Sanford JC, Sanford RA, Ritalahti KM, Löffler FE, Konstantinidis KT (2014) Detecting nitrous oxide reductase (nosZ) genes in soil metagenomes: method development and implications for the nitrogen cycle. mBio 5:e01193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen SO, Well R, Taghizadeh-Toosi A, Clough TJ (2020) Seasonally distinct sources of N2O in acid organic soil drained for agriculture as revealed by N2O isotopomer analysis. Biogeochemistry 147:15–33

    Article  CAS  Google Scholar 

  • Philippot L, Andert J, Jones CM, Bru D, Hallin S (2011) Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Glob Change Biol 17:1497–1504

    Article  Google Scholar 

  • Qin S, Ding K, Clough TJ, Hu C, Luo J (2017) Temporal in situ dynamics of N2O reductase activity as affected by nitrogen fertilization and implications for the N2O/(N2O+N2) product ratio and N2O mitigation. Biol Fertil Soils 53:723–727

    Article  CAS  Google Scholar 

  • Rohe L, Well R, Lewicka-Szczebak D (2017) Use of oxygen isotopes to differentiate between nitrous oxide produced by fungi or bacteria during denitrification. Rapid Commun Mass Spectrom 31:1297–1312

    Article  CAS  PubMed  Google Scholar 

  • Rousk J, Bååth E (2007) Fungal and bacterial growth in soil with plant materials of different C/N ratios. FEMS Microbiol Ecol 62:258–267

    Article  CAS  PubMed  Google Scholar 

  • Ruser R, Flessa H, Russow R, Schmidt G, Buegger F, Munch JC (2006) Emission of N2O, N2 and CO2 from soil fertilized with nitrate: effect of compaction, soil moisture and rewetting. Soil Biol Biochem 38:263–274

    Article  CAS  Google Scholar 

  • Saggar S, Jha N, Deslippe J, Bolan N, Luo J, Giltrap DL, Kim DG, Zaman M, Tillman RW (2013) Denitrification and N2O:N2 production in temperate grasslands: processes, measurements, modelling and mitigating negative impacts. Sci Total Environ Science of the Total Environment 465:173–195

    Article  CAS  Google Scholar 

  • Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH, Cruz-García C, Rodríguez G, Massol-Deyá A, Krishnani KK, Ritalahti KM, Nissen S, Konstantinidis KT, Löffler FE (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc Natl Acad Sci USA 109:19709–19714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlesinger WH (2009) On the fate of anthropogenic nitrogen. Proc Natl Acad Sci USA 106:203

    Article  CAS  PubMed  Google Scholar 

  • Senbayram M, Budai A, Bol R, Chadwick D, Marton L, Gündogan R, Wu D (2019) Soil NO3− level and O2 availability are key factors in controlling N2O reduction to N2 following long-term liming of an acidic sandy soil. Soil Biol Biochem 132:165–173

    Article  CAS  Google Scholar 

  • Senbayram M, Chen R, Budai A, Bakken L, Dittert K (2012) N2O emission and the N2O/(N2O+N2) product ratio of denitrification as controlled by available carbon substrates and nitrate concentrations. Agric Ecosyst Environ 147:4–12

    Article  CAS  Google Scholar 

  • Senbayram M, Chen R, Wienforth B, Herrmann A, Kage H, Mühling KH, Dittert K (2014) Emission of N2O from biogas crop production systems in Northern Germany. BioEnergy Res 7:1223–1236

    Article  CAS  Google Scholar 

  • Senbayram M, Well R, Bol R, Chadwick DR, Jones DL, Wu D (2018) Interaction of straw amendment and soil NO3– content controls fungal denitrification and denitrification product stoichiometry in a sandy soil. Soil Biol Biochem 126:204–212

    Article  CAS  Google Scholar 

  • Senbayram M, Well R, Shan J, Bol R, Burkart S, Jones DL, Wu D (2020) Rhizosphere processes in nitrate-rich barley soil tripled both N2O and N2 losses due to enhanced bacterial and fungal denitrification. Plant Soil 448:509–522

    Article  CAS  Google Scholar 

  • Shan J, Sanford RA, Chee-Sanford J, Ooi SK, Löffler FE, Konstantinidis KT, Yang WH (2021) Beyond denitrification: the role of microbial diversity in controlling nitrous oxide reduction and soil nitrous oxide emissions. Glob Change Biol 27:2669–2683

    Article  Google Scholar 

  • Shoun H, Kim D-H, Uchiyama H, Sugiyama J (1992) Denitrification by fungi. FEMS Microbiol Lett 94:277–281

    Article  CAS  Google Scholar 

  • Smith KA, Arah JRM (1990) Losses of nitrogen by denitrification and emissions of nitrogen oxides from soils. Proceedings-Fertiliser Society No.299 pp. 34

  • Swerts M, Merckx R, Vlassak K (1996) Influence of carbon availability on the production of NO, N2O, N2 and CO2 by soil cores during anaerobic incubation. In: Van Cleemput O, Hofman G, Vermoesen A (Eds) Progress in Nitrogen Cycling Studies: Proceedings of the 8th Nitrogen Workshop held at the University of Ghent, 5–8 September, 1994. Springer, Dordrecht, The Netherlands, pp 633–639

  • Toyoda S, Yano M, Nishimura S, Akiyama H, Hayakawa A, Koba K, Sudo S, Yagi K, Makabe A, Tobari Y, Ogawa N-O, Ohkouchi N, Yamada K, Yoshida N (2011) Characterization and production and consumption processes of N2O emitted from temperate agricultural soils determined via isotopomer ratio analysis. Glob Biogeochem Cycle 25:GB2008

  • Toyoda S, Yoshida N (1999) Determination of nitrogen isotopomers of nitrous oxide on a modified isotope ratio mass spectrometer. Anal Chem 71:4711–4718

    Article  CAS  Google Scholar 

  • Toyoda S, Yoshida N, Koba K (2017) Isotopocule analysis of biologically produced nitrous oxide in various environments. Mass Spectrom Rev 36:135–160

    Article  CAS  PubMed  Google Scholar 

  • van der Wal A, Smant W, Boschker HTS, Bloem J, Kardol P, van der Putten WH, de Boer W (2006) Fungal biomass development in a chronosequence of land abandonment. Soil Biol Biochem 38:51–60

    Article  Google Scholar 

  • Wang J, Yan X (2016) Denitrification in upland of China: magnitude and influencing factors. J Geophys Res-Biogeosci 121:2016JG003541

    Article  Google Scholar 

  • Wang R, Willibald G, Feng Q, Zheng X, Liao T, Brüggemann N, Butterbach-Bahl K (2011) Measurement of N2, N2O, NO, and CO2 emissions from soil with the gas-flow-soil-core technique. Environ Sci Technol 45:6066–6072

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Zhang J, Cai Z (2016) Effects of conversion of paddy field into vineyard on soil nitrogen transformation in the Taihu Lake Region of China. Acta Pedol Sin 53:166–176

    CAS  Google Scholar 

  • Wankel SD, Ziebis W, Buchwald C, Charoenpong C, de Beer D, Dentinger J, Xu Z, Zengler K (2017) Evidence for fungal and chemodenitrification based N2O flux from nitrogen impacted coastal sediments. Nat Commun 8:15595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei Z, Shan J, Chai Y, Well R, Yan X, Senbayram M (2020) Regulation of the product stoichiometry of denitrification in intensively managed soils. Food Energy Secur 9:e251

    Article  Google Scholar 

  • Weier KL, Doran JW, Power JF, Walters DT (1993) Denitrification and the dinitrogen nitrous-oxide ratio as affected by soil-water, available carbon, and nitrate. Soil Sci Soc Am J 57:66–72

    Article  CAS  Google Scholar 

  • Well R, Flessa H, Xing L, Xiaotang J, Römheld V (2008) Isotopologue ratios of N2O emitted from microcosms with NH4+ fertilized arable soils under conditions favoring nitrification. Soil Biol Biochem 40:2416–2426

    Article  CAS  Google Scholar 

  • Wu D, Wei Z, Well R, Shan J, Yan X, Bol R, Senbayram M (2018) Straw amendment with nitrate-N decreased N2O/(N2O+N2) ratio but increased soil N2O emission: a case study of direct soil-born N2 measurements. Soil Biol Biochem 127:301–304

    Article  CAS  Google Scholar 

  • Wu D, Well R, Cárdenas LM, Fuß R, Lewicka-Szczebak D, Köster JR, Brüggemann N, Bol R (2019) Quantifying N2O reduction to N2 during denitrification in soils via isotopic mapping approach: Model evaluation and uncertainty analysis. Environ Res 179:108806

    Article  CAS  PubMed  Google Scholar 

  • Xia L, Li X, Ma Q, Lam SK, Wolf B, Kiese R, Butterbach-Bahl K, Chen D, Li Z, Yan X (2019) Simultaneous quantification of N2, NH3 and N2O emissions from a flooded paddy field under different N fertilization regimes. Glob Change Biol 26:2292–2303

    Article  Google Scholar 

  • Yoon S, Song B, Phillips RL, Chang J, Song MJ (2019) Ecological and physiological implications of nitrogen oxide reduction pathways on greenhouse gas emissions in agroecosystems. FEMS Microbiol Ecol 95:fiz066

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Penton CR, Yu Z, Xue C, Chen Q, Chen Z, Yan C, Zhang Q, Zhao M, Quensen JF, Tiedjie JM (2021) A new primer set for Clade I nosZ that recovers genes from a broader range of taxa. Biol Fertil Soils 57:523–531

    Article  CAS  Google Scholar 

  • Zheng X, Wang M, Wang Y, Shen R, Gou J, Li J, Jin J, Li L (2000) Impacts of soil moisture on nitrous oxide emission from croplands: a case study on the rice-based agro-ecosystem in Southeast China. Chemosphere 2:207–224

    CAS  Google Scholar 

  • Zhong L, Bowatte S, Newton PCD, Hoogendoorn CJ, Luo D (2018) An increased ratio of fungi to bacteria indicates greater potential for N2O production in a grazed grassland exposed to elevated CO2. Agric Ecosyst Environ 254:111–116

    Article  CAS  Google Scholar 

  • Zhou W, Jones DL, Hu R, Clark IM, Chadwick DR (2020) Crop residue carbon-to-nitrogen ratio regulates denitrifier N2O production post flooding. Biol Fertil Soils 56:825–838

    Article  CAS  Google Scholar 

  • Zhou W, Ma Y, Well R, Wang H, Yan X (2018) Denitrification in shallow groundwater below different arable land systems in a high nitrogen-loading region. J Geophys Res-Biogeosci 123:991–1004

    Article  CAS  Google Scholar 

  • Zhu-Barker X, Doane TA, Horwath WR (2015) Role of green waste compost in the production of N2O from agricultural soils. Soil Biol Biochem 83:57–65

    Article  CAS  Google Scholar 

  • Zhu Z, Chen D (2002) Nitrogen fertilizer use in China—contributions to food production, impacts on the environment and best management strategies. Nutr Cycl Agroecosyst 63:117–127

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Martina Heuer and Jennifer Ehe for assistance in the stable isotope analysis, Ute Tambor for assistance in the mineral N analysis, Dr. Dominika Lewicka-Szczebak for assistance in the isotopomer data analysis, and Dr. Roland Fuß for the technical support.

Funding

This study was funded by the DFG project (WE 1904/12–1) and key project of the Natural Science Foundation of China (U20A20113). Dr. Jun Shan received financial support from the Scientific Instrument and Equipment Development Project of CAS (YJKYYQ20170058) and the Youth Innovation Promotion Association of CAS (2017362). Dr. Mehmet Senbayram received financial support from the TÜBITAK Project (119R042) and HUBAK Project (21141).

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  1. Mehmet Senbayram and Zhijun Wei contributed equally to this study

Authors and Affiliations

  1. Federal Research Institute for Rural Areas, Forestry and Fisheries, Thünen Institute of Climate-Smart Agriculture, Bundesallee 65, 38116, Braunschweig, Germany

    Mehmet Senbayram, Zhijun Wei & Reinhard Well

  2. Institute of Plant Nutrition and Soil Science, University of Harran, Osmanbey, 63000, Sanliurfa, Turkey

    Mehmet Senbayram

  3. State Key Laboratory of Soil and Sustainable Agriculture, Changshu National Agro-Ecosystem Observation and Research Station, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Zhijun Wei, Jun Shan & Xiaoyuan Yan

  4. University of Chinese Academy of Sciences, Beijing, 100049, China

    Zhijun Wei, Jun Shan & Xiaoyuan Yan

  5. Beijing Key Laboratory of Biodiversity and Organic Farming, College of Resources and Environmental Sciences, China Agricultural University, Beijing, 100193, China

    Di Wu

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  1. Mehmet Senbayram
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Contributions

Mehmet Senbayram: Conceptualization, Methodology, Investigation, Writing. Zhijun Wei: Investigation, Data curation, Visualization, Writing. Di Wu: Methodology and Formal analysis. Jun Shan: Conceptualization, Writing — review and editing. Xiaoyuan Yan: Writing — review and editing. Reinhard Well: Supervision, Writing — review and editing.

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Senbayram, M., Wei, Z., Wu, D. et al. Inhibitory effect of high nitrate on N2O reduction is offset by long moist spells in heavily N loaded arable soils. Biol Fertil Soils 58, 77–90 (2022). https://doi.org/10.1007/s00374-021-01612-x

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