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Influence of liming-induced pH changes on nitrous oxide emission, nirS, nirK and nosZ gene abundance from applied cattle urine in allophanic and fluvial grazed pasture soils

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Abstract

The influence of soil pH changes by liming on denitrification and denitrifier gene abundance under different biogeochemical conditions by amending two contrasting soils with water, cattle urine (600 mg N kg−1 soil) and urine + dicyandiamide (DCD) (10 mg kg−1 soil) and incubating at 10 °C and 15 °C was evaluated. Liming increased N2O emission, denitrification rate and denitrifier gene abundance in both soils. The increase in N2O and denitrification with liming was higher in fluvial soil (24% increase in N2O and 22% increase in denitrification) than in allophanic soil (16% in N2O and 19% increase in denitrification). There was more N2O coming from urine applied to limed soil than that from urine to un-limed soil. Addition of DCD with urine reduced both N2O emission and denitrification; the reduction was greater in limed soil than in un-limed soil. Results of quantitative polymerase chain reaction (qPCR) of bacterial denitrifier genes (nirS, nirK and nosZ genes) indicate that liming-induced soil pH changes increased denitrifier gene abundance and caused more complete bacterial denitrification in urine-amended soils. These results suggest that liming grazed pasture soils induces complete denitrification, which may mitigate 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

    Google Scholar 

  • Bárta J, Melichová T, Vaněk D, Picek T, Šantrůčková H (2010) Effect of pH and dissolved organic matter on the abundance of nirK and nirS denitrifiers in spruce forest soil. Biogeochemistry 101:123–132

    Google Scholar 

  • Bergaust L, Mao Y, Bakken LR, Frostegård A (2010) Denitrification response patterns during the transition to anoxic respiration and posttranscriptional effects of suboptimal pH on nitrogen oxide reductase in Paracoccus denitrificans. Appl Environ Microbiol 76:6387–6396

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blakemore LC, Searle PL, Daly BK (1987) In: Isaacs D (ed) Methods for chemical analysis of soils. NZ Soil Bureau. Department of Scientific and Industrial Research, Lower Hutt, New Zealand, pp 9–12

    Google Scholar 

  • Burger M, Matiasek M (2009) New approaches to distinguish between nitrification and denitrificationas sources of nitrous oxide. In: Sheldon AL, Barnhart EP (eds) Nitrous oxide emissions research progress. Nova Science Publishers, New York (USA), pp 167–178

    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

    Google Scholar 

  • Castellano-Hinojosa A, González-López J, Bedmar EJ (2018) Distinct effect of nitrogen fertilisation and soil depth on nitrous oxide emissions and nitrifiers and denitrifiers abundance. Biol Fertil Soils 54:829–840

    CAS  Google Scholar 

  • Clough TJ, Sherlock RR, Kelliher FM (2003) Can liming mitigate N2O fluxes from a urine-amended soil? Soil Res 41:439–457

    Google Scholar 

  • Clough TJ, Kelliher FM, Sherlock RR, Ford CD (2004) Lime and soil moisture effects on nitrous oxide emissions from a urine patch. Soil Sci Soc Am J 68:1600–1609

    CAS  Google Scholar 

  • Čuhel J, Šimek M, Laughlin RJ, Bru D, Chèneby D, Watson CJ, Philippot L (2010) Insights into the effect of soil pH on N2O and N2 emissions and denitrifier community size and activity. Appl Environ Microbiol 76:1870–1878

    PubMed  PubMed Central  Google Scholar 

  • Dandie CE, Wertz S, Leclair CL, Goyer C, Burton DL, Patten CL, Zebarth BJ, Trevours JT (2011) Abundance, diversity and functional gene expression of denitrifier communities inadjacent riparian and agricultural zones. FEMS Microbiol Ecol 77:69–82

    CAS  PubMed  Google Scholar 

  • Deslippe JR, Jamali H, Jha N, Saggar S (2014) Denitrifier community size, structure and activity along a gradient of pasture to riparian soils. Soil Biol Biochem 71:48–60

    CAS  Google Scholar 

  • Di HJ, Cameron KC (2002) The use of a nitrification inhibitor, dicyandiamide (DCD), to decrease nitrate leaching and nitrous oxide emissions in a simulated grazed and irrigated grassland. Soil Use Manag 18:395–403

    Google Scholar 

  • Di HJ, Cameron KC (2003) Mitigation of nitrous oxide emissions in spray-irrigated grazed grassland by treating the soil with dicyandiamide, a nitrification inhibitor. Soil Use Manag 19:284–290

    Google Scholar 

  • Di HJ, Cameron KC (2006a) Nitrous oxide emissions from two dairy pasture soils as affected by different rates of a fine particle suspension nitrification inhibitor, dicyandiamide. Biol Fertil Soils 42:472–480

    CAS  Google Scholar 

  • Di HJ, Cameron KC (2006b) The use of a nitrification inhibitor, dicyandiamide (DCD), to decrease nitrate leaching and nitrous oxide emissions in a simulated grazed and irrigated grassland. Soil Use Manag 18:395–403

    Google Scholar 

  • Di HJ, Cameron KC (2012) How does the application of different nitrification inhibitors affect nitrous oxide emissions and nitrate leaching from cow urine in grazed pastures? Soil Use Manag 28:54–61

    Google Scholar 

  • Di HJ, Cameron KC, Podolyan A, Robinson A (2014) Effect of soil moisture status and a nitrification inhibitor, dicyandiamide, on ammonia oxidizer and denitrifier growth and nitrous oxide emissions in a grassland soil. Soil Biol Biochem 73:59–68

    CAS  Google Scholar 

  • Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl Environ Microbiol 71:8335–8343

    CAS  PubMed  PubMed Central  Google Scholar 

  • Enwall K, Throbäck IN, Stenberg M, Söderström M, Hallin S (2010) Soil resources influence spatial patterns of denitrifying communities at scales compatible with land management. Appl Environ Microbiol 76:2243–2250

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fedorova RI, Milekhina EI, Ilyukhina NI (1973) On the possibilities of the ‘gas exchange’ method for the detection of extraterrestrial life: identification of nitrogen fixing microorganisms (Russian). Izevestiya Akademii Nauk SSSR - Seriya Biologicheskaya 6:797–806

    CAS  Google Scholar 

  • Felber R, Conen F, Flechard CR, Neftel A (2012) Theoretical and practical limitations of the acetylene inhibition technique to determine total denitrification losses. Biogeosciences 9:4125–4138

    CAS  Google Scholar 

  • Haynes RJ, Williams PH (1992) Changes in soil solution composition and pH in urine-affected areas of pasture. J Soil Sci 43:323–334

    CAS  Google Scholar 

  • Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72:5181–5189

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hewitt A (1992) Soil classification in New Zealand. DSIR Land Resources Scientific Report No 19. Deportment of Scientific and Industrial Research, pp 91–120

  • Hou Y, Miranda L, Lin S (2010) Serious overestimation in quantitative PCR by circular (supercoiled) plasmid standard: microalgal pcna as the model gene. PLoS One 5:e9545

    PubMed  PubMed Central  Google Scholar 

  • Jones CM, Graf DR, Bru D, Philippot L, Hallin S (2013) The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J 7:417–426

    CAS  PubMed  Google Scholar 

  • Kelso B, Smith RV, Laughlin RJ, Lennox SD (1997) Dissimilatory nitrate reduction in anaerobic sediments leading to river nitrite accumulation. Appl Environ Microbiol 63:4679–4685

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lambie SM, Schipper LA, Balks MR, Baisden WT (2012) Solubilisation of soil carbon following treatment with cow urine under laboratory conditions. Soil Res 50:50–57

    Google Scholar 

  • Liu B, Mørkved PT, Frostegård A, 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

    CAS  PubMed  Google Scholar 

  • McMillan AMS, Pal P, Phillips RL, Palmada T, Berben P, Jha N, Saggar S, Luo J (2016) Can pH amendments in grazed pastures help reduce N2O emissions from denitrification?—the effects of liming and urine addition on the completion of denitrification in fluvial and volcanic soils. Soil Biol Biochem 93:90–104

    CAS  Google Scholar 

  • Morales SE, Jha N, Saggar S (2015a) Biogeography and biophysicochemical traits link N2O emissions, N2O emission potential and microbial communities across New Zealand pasture soils. Soil Biol Biochem 82:87–98

    CAS  Google Scholar 

  • Morales SE, Jha N, Saggar S (2015b) Impact of urine and the application of the nitrification inhibitor DCD on microbial communities in dairy-grazed pasture soils. Soil Biol Biochem 88:344–353

    CAS  Google Scholar 

  • Mukumbuta I, Uchida Y, Hatano R (2018) Evaluating the effect of liming on N2O fluxes from denitrification in an Andosol using the acetylene inhibition and 15N isotope tracer methods. Biol Fertil Soils 54:71–81

    CAS  Google Scholar 

  • Nannipieri P, Penton CR, Purahong W, Schloter M, van Elsas JD (2019) Recommendations for soil microbiome analyses. Biol Fertil Soils 55:765–766

    Google Scholar 

  • Nannipieri P, Ascher-Jenull J, Ceccherini MT, Pietramellara G, Renella G, Schloter M (2020) Beyond microbial diversity for predicting soil functions: a mini review. Pedosphere 30:5–17

    Google Scholar 

  • Nodar R, Acea MJ, Carballas T (1992) Microbiological response to Ca(OH)2 treatments in a forest soil. FEMS Microbiol Lett 86:213–219

    CAS  Google Scholar 

  • Oenema O, Wrage N, Velthof GL, Van Groenigen JW, Dolfing J, Kuikman PJ (2005) Trends in global nitrous oxide emissions from animal production systems. Nutr Cycl Agroecosyst 72:51–65

    CAS  Google Scholar 

  • Orwin KH, Bertram JE, Clough TJ, Condron LM, Sherlock RR, O’Callaghan M, Ray J, Baird DB (2010) Impact of bovine urine deposition on soil microbial activity, biomass, and community structure. Appl Soil Ecol 44:89–100

    Google Scholar 

  • Page KL, Allen DE, Dalal RC, Slattery W (2009) Process and magnitude of CO2, CH4, and N2O fluxes from liming of Australian acidic soils: a review. Aust J Agric Res 47:747–762

    CAS  Google Scholar 

  • Pan H, Ying S, Liu H, Zeng L, Zhang Q, Liu Y, Xu J, Li Y, Di H (2018) Microbial pathways for nitrous oxide emissions from sheep urine and dung in a typical steppe grassland. Biol Fertil Soils 54:717–730

    CAS  Google Scholar 

  • Parfitt RL (2009) Allophane and imogolite: role in soil biogeochemical processes. Clay Miner 44:135–155

    CAS  Google Scholar 

  • Pfaffl MW (2004) Quantification stategies in real-time PCR. In: Bustin SA (ed) The real-time PCR encyclopedia A-Z of quantitative PCR. International University Line (IUL), La Jolla, CA, USA, pp 87–120

    Google Scholar 

  • Purves ED (1992) Optimum numerical integration methods for estimation of area-under-the-curve (AUC) and area-under-the-movement-curve (AUMC). J Pharmacokinet Biopharm 20:211–226

    CAS  PubMed  Google Scholar 

  • Qin H, Tang Y, Shen J, Wang C, Chen C, Yang J, Liu Y, Chen X, Li Y, Hou H (2018) Abundance of transcripts of functional gene reflects the inverse relationship between CH4 and N2O emissions during mid-season drainage in acidic paddy soil. Biol Fertil Soils 54:885–895

    Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Santoro AE, Boehm AB, Francis CA (2006) Denitrifier community composition along a nitrate and salinity gradient in a coastal aquifer. Appl Environ Microbiol 72:2102–2109

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schöler A, Jacquiod S, Vestergaard G, Schulz S (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Feril Soils 53:485–489

    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

    CAS  Google Scholar 

  • Silver WL, Herman DJ, Firestone MK (2001) Dissimilatory nitrate reduction to ammonium in upland tropical forest soils. Ecology 82:2410–2416

    Google Scholar 

  • Šimek M, Jisova L, Hopkins DW (2002) What is the so-called optimum pH for denitrification in soil? Soil Biol Biochem 34:1227–1234

    Google Scholar 

  • Singh J, Saggar S, Giltrap DL, Bolan NS (2008) Decomposition of dicyandiamide (DCD) in three contrasting soils and its effect on nitrous oxide emission, soil respiratory activity, and microbial biomass—an incubation study. Aust J Soil Res 46:517–525

    CAS  Google Scholar 

  • Singh J, Kunhikrishnan A, Bolan NS, Saggar S (2013) Impact of urease inhibitor on ammonia and nitrous oxide emissions from temperate pasture soil cores receiving urea fertilizer and cattle urine. Sci Total Environ 465:56–63

    CAS  PubMed  Google Scholar 

  • Singleton PL (1991) Soils of Ruakura-a window on the Waikato. DSIR Land Resources Scientific Report No 5. Deportment of Scientific and Industrial Research, p 127

  • Tiedje JM, Simkins S, Groffman PM (1989) Perspectives on measurement of denitrification in the field including recommended protocols for acetylene based methods. Plant Soil 115:261–284

    Google Scholar 

  • Uchida Y, Clough T, Kelliher F, Hunt J, Sherlock R (2011) Effects of bovine urine, plants and temperature on N2O and CO2 emissions from a sub-tropical soil. Plant Soil 345:171–186

    CAS  Google Scholar 

  • Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart—how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484

    Google Scholar 

  • Wakelin SA, Clough TJ, Gerard EM, O'Callaghan M (2013) Impact of short-interval, repeat application of dicyandiamide on soil N transformation in urine patches. Agric Ecosyst Environ 167:60–70

    CAS  Google Scholar 

  • Weiske A, Benckiser G, Herbert T, Ottow J (2001) Influence of the nitrification inhibitor 3,4-dimethylpyrazole phosphate (DMPP) in comparison to dicyandiamide (DCD) on nitrous oxide emissions, carbon dioxide fluxes and methane oxidation during 3 years of repeated application in field experiments. Biol Fertil Soils 34:109–117

    CAS  Google Scholar 

  • Welten B, Kear M, Dexter M, Judge A (2012) Efficiency of DCD extraction from soils. In: Currie LD, Christensen CL (eds) Advanced nutrient management: gains from the past—goals for the future. http://flrc.massey.ac.nz/publications.html. Occasional Report No. 25. Fertilizer and Lime Research Centre, Massey University, Palmerston North, New Zealand, pp 1–5

    Google Scholar 

  • Zaman M, Nguyen ML (2010) Effect of lime or zeolite on N2O and N2 emissions from a pastoral soil treated with urine or nitrate-N fertilizer under field conditions. Agric Ecosyst Environ 136:254–261

    CAS  Google Scholar 

  • Zaman M, Nguyen ML (2012) How application timings of urease and nitrification inhibitors affect N losses from urine patches in pastoral system. Agric Ecosyst Environ 156:37–48

    CAS  Google Scholar 

  • Zaman M, Nguyen ML, Matheson F, Blennerhassett JD, Quin BF (2007) Can soil amendments (zeolite or lime) shift the balance between nitrous oxide and dinitrogen emissions from pasture and wetland soils receiving urine or urea-N? Aust J Soil Res 45:543–553

    CAS  Google Scholar 

  • Zaman M, Nguyen ML, Blennerhassett JD, Quin BF (2008) Reducing NH3, N2O and NO3−-N losses from a pasture soil with urease or nitrification inhibitors and elemental S-amended nitrogenous fertilizers. Biol Fertil Soils 44:693–705

    CAS  Google Scholar 

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Acknowledgments

We acknowledge the funding and support for this study by New Zealand Agricultural Greenhouse Gas Research Centre and Strategic Science Investment Fund (SSIF) for Crown Research Institutes from the Ministry of Business, Innovation and Employment’s Science and Innovation Group. We also acknowledge the support from technical staff at AgResearch for collection of soil samples from Waikato, liming application and incubation for 3 months. We thank Dr. Rebecca Phillips for reviewing and Leah Kearns for editing the manuscript.

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Authors and Affiliations

  1. Massey University, Palmerston North, 4442, New Zealand

    Neha Jha

  2. Manaaki Whenua-Landcare Research, Palmerston North, 4442, New Zealand

    Neha Jha, Thilak Palmada, Peter Berben & Surinder Saggar

  3. AgResearch, Hamilton, New Zealand

    Jiafa Luo & Andrew M. S. McMillan

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  1. Neha Jha
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  2. Thilak Palmada
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  4. Surinder Saggar
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Correspondence to Neha Jha.

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Jha, N., Palmada, T., Berben, P. et al. Influence of liming-induced pH changes on nitrous oxide emission, nirS, nirK and nosZ gene abundance from applied cattle urine in allophanic and fluvial grazed pasture soils. Biol Fertil Soils 56, 811–824 (2020). https://doi.org/10.1007/s00374-020-01460-1

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