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Dissimilatory nitrate reduction to ammonium increased with rising temperature

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Abstract

Although recent studies have explored dissimilatory nitrate reduction to ammonium (DNRA), little is known about the dependence of this process on temperature. A laboratory experiment was conducted to investigate if temperature regulates nitrate (NO3ˉ) reduction by DNRA and denitrification. Soil samples were incubated at 10 to 40 °C for 28 days, and 15N tracer methods were applied to estimate the reduction of 15NO3ˉ to 15NH4+ by DNRA organisms and to 15N2O or 15N2 by denitrifiers. Raising the temperature from 10 to 40 °C increased DNRA, which contributed to enrichment of the NH4+ pool, particularly at 40 °C. The percentage of 15NO3ˉ reduced by DNRA was from 4 to 30% of that reduced by denitrification, and decreased with increasing temperature. DNRA and denitrification were positively correlated with the abundance of nrfA and nosZ genes, respectively. The accumulation of 15NH4+ slowed in the final 12 h of sampling times, which may be due to a re-conversion of 15NH4+ to 15NO3ˉ by nitrification. High temperatures (30 to 40 °C) enhanced 15N2 production, which suggests that temperature plays an important role in regulating complete denitrification from NO3ˉ to N2.

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References

  • Bolan NS, Kemp P (2003) A review of factors affecting and prevention of pasture-induced nitrate toxicity in grazing animals. Proc N Z Gras Assoc 65:71–78

    Google Scholar 

  • Buresh R, Patrick W (1978) Nitrate reduction to ammonium in anaerobic soil 1. Soil Sci Soc Am J 42:913–918

    Article  CAS  Google Scholar 

  • Chen Z, Ding W, Xu Y, Müller C, Rütting T, Yu H, Fan J, Zhang J, Zhu T (2015) Importance of heterotrophic nitrification and dissimilatory nitrate reduction to ammonium in a cropland soil: evidences from a 15N tracing study to literature synthesis. Soil Biol Biochem 91:65–75

    Article  CAS  Google Scholar 

  • Cole J (1990) Physiology, biochemistry and genetics of nitrate dissimilation to ammonia. In: Revsbech N (ed) Denitrification in soil and sediment. Springer. Plenum Press, New York, pp 57–76

    Chapter  Google Scholar 

  • Cole J, Brown C (1980) Nitrite reduction to ammonia by fermentative bacteria: a short circuit in the biological nitrogen cycle. FEMS Microbiol Lett 7:65–72

    Article  CAS  Google Scholar 

  • Corrêa EF, Germon J (1991) Dissimilative nitrate reduction to ammonium in different soils in waterlogged conditions. Devel Geoche 6:295–308

    Article  Google Scholar 

  • Davidson E, Hart S, Shanks C, Firestone M (1991) Measuring gross nitrogen mineralization, and nitrification by 15N isotopic pool dilution in intact soil cores. J Soil Sci 42:335–349

    Article  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jha N, Palmada T, Berben P, Saggar S, Luo J, McMillan A (2020) 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

    Article  CAS  Google Scholar 

  • Ji Y, Conrad R, Xu H (2020) Responses of archaeal, bacterial, and functional microbial communities to growth season and nitrogen fertilization in rice fields. Biol Fertil Soils 56:81–95

    Article  CAS  Google Scholar 

  • Kamphake L, Hannah S, Cohen J (1967) Automated analysis for nitrate by hydrazine reduction. Water Res 1:205–216

    Article  CAS  Google Scholar 

  • Kaplan A (1965) Standard methods of clinical chemistry. Academic Press, New York

    Google Scholar 

  • Lai TV, Denton MD (2018) N2O and N2 emissions from denitrification respond differently to temperature and nitrogen supply. J Soils Sediments 18:1548–1557

    Article  CAS  Google Scholar 

  • Lai TV, Farquharson R, Denton MD (2019) High soil temperatures alter the rates of nitrification, denitrification and associated N2O emissions. J Soils Sediments 19:2176–2189

    Article  CAS  Google Scholar 

  • Maag M, Vinther FP (1996) Nitrous oxide emission by nitrification and denitrification in different soil types and at different soil moisture contents and temperatures. Appl Soil Ecol 4:5–14

    Article  Google Scholar 

  • Malhi S, McGill W, Nyborg M (1990) Nitrate losses in soils: effect of temperature, moisture and substrate concentration. Soil Biol Biochem 22:733–737

    Article  CAS  Google Scholar 

  • Miller KS, Geisseler D (2018) Temperature sensitivity of nitrogen mineralization in agricultural soils. Biol Fertil Soils 54:853–860

    Article  CAS  Google Scholar 

  • Mohan SB, Schmid M, Jetten M, Cole J (2004) Detection and widespread distribution of the nrfA gene encoding nitrite reduction to ammonia, a short circuit in the biological nitrogen cycle that competes with denitrification. FEMS Microbiol Ecol 49:433–443

    Article  CAS  PubMed  Google Scholar 

  • Mueller C, Rütting T, Kattge J, Laughlin R, Stevens R (2007) Estimation of parameters in complex 15N tracing models by Monte Carlo sampling. Soil Biol Biochem 39:715–726

    Article  CAS  Google Scholar 

  • Müller C, Stevens R, Laughlin R (2004) A 15N tracing model to analyse N transformations in old grassland soil. Soil Biol Biochem 36:619–632

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Pandey A, Suter H, He J-Z, Hu H-W, Chen D (2018) Nitrogen addition decreases dissimilatory nitrate reduction to ammonium in rice paddies. Appl Environ Microbiol 84:e00870–e00818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Powlson D, Saffigna P, Kragt-Cottaar M (1988) Denitrification at sub-optimal temperatures in soils from different climatic zones. Soil Biol Biochem 20:719–723

    Article  CAS  Google Scholar 

  • Puri G, Ashman (1999) Microbial immobilization of 15N-labelled ammonium and nitrate in a temperate woodland soil. Soil Biol Biochem 31:929–931

    Article  CAS  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

    Article  Google Scholar 

  • Rice CW, Tiedje JM (1989) Regulation of nitrate assimilation by ammonium in soils and in isolated soil microorganisms. Soil Biol Biochem 21:597–602

    Article  CAS  Google Scholar 

  • Risgaard-Petersen N, Revsbech NP, Rysgaard S (1995) Combined microdiffusion-hypobromite oxidation method for determining nitrogen-15 isotope in ammonium. Soil Sci Soc Am J 59:1077–1080

    Article  CAS  Google Scholar 

  • Rütting T, Boeckx P, Müller C, Klemedtsson L (2011) Assessment of the importance of dissimilatory nitrate reduction to ammonium for the terrestrial nitrogen cycle. Biogeosciences 8:1779–1791

    Article  Google Scholar 

  • Schimel JP, Gulledge J (1998) Microbial community structure and global trace gases. Glob Chang Biol 4:745–758

    Article  Google Scholar 

  • Schmidt EL (1982) Nitrification in soil. In: Stevenson F (ed) Nitrogen in agricultural soil. American Soc. Agronomy, Madison, pp 253–267

  • Schmidt CS, Richardson DJ, Baggs EM (2011) Constraining the conditions conducive to dissimilatory nitrate reduction to ammonium in temperate arable soils. Soil Biol Biochem 43:1607–1611

    Article  CAS  Google Scholar 

  • Sierra J, Marban L (2000) Nitrogen mineralization pattern of an oxisol of Guadeloupe, French West Indies. Soil Sci Soc Am J 64:2002–2010

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Silver WL, Thompson A, Reich A, Ewel JJ, Firestone M (2005) Nitrogen cycling in tropical plantation forests: potential controls on nitrogen retention. Ecol Appl 15:1604–1614

    Article  Google Scholar 

  • Simon J (2002) Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol Rev 26:285–309

    Article  CAS  PubMed  Google Scholar 

  • Smirnoff N, Stewart G (1985) Nitrate assimilation and translocation by higher plants: comparative physiology and ecological consequences. Physiol Plant 64:133–140

    Article  CAS  Google Scholar 

  • Smith S, Cassel D (1991) Estimating nitrate leaching in soil materials. In: Follett R, Keeney D, Cruse R (eds) Managing nitrogen for groundwater quality and farm profitability. Soil Science Society of America, Madison, pp 165–188

  • Sotta ED, Corre MD, Veldkamp E (2008) Differing N status and N retention processes of soils under old-growth lowland forest in Eastern Amazonia, Caxiuanã, Brazil. Soil Biol Biochem 40:740–750

    Article  CAS  Google Scholar 

  • Stark JM, Firestone MK (1996) Kinetic characteristics of ammonium-oxidizer communities in a California oak woodland-annual grassland. Soil Biol Biochem 28:1307–1317

    Article  CAS  Google Scholar 

  • Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68:1312–1318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed) Environmental microbiology of anaerobes. John Wiley and Sons, New York, pp 179–244

    Google Scholar 

  • Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA (1982) Denitrification: ecological niches, competition and survival. Antonie Van Leeuwenhoek 48:569–583

    Article  CAS  PubMed  Google Scholar 

  • Welsh A, Chee-Sanford JC, Connor LM, Löffler FE, Sanford RA (2014) Refined NrfA phylogeny improves PCR-based nrfA gene detection. Appl Environ Microbiol 80:2110–2119

    Article  PubMed  PubMed Central  Google Scholar 

  • Woods DD (1938) The reduction of nitrate to ammonia by Clostridium welchii. Biochem J 32:2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yanni SF, Helgason BL, Janzen HH, Ellert BH, Gregorich EG (2020) Warming effects on carbon dynamics and microbial communities in soils of diverse texture. Soil Biol Biochem 140:107631

    Article  CAS  Google Scholar 

  • Yin S, Shen Q, Tang Y, Cheng L (1998) Reduction of nitrate to ammonium in selected paddy soils of China. Pedosphere 8:221–228

    CAS  Google Scholar 

  • Zaman M, Chang S (2004) Substrate type, temperature, and moisture content affect gross and net N mineralization and nitrification rates in agroforestry systems. Biol Fertil Soils 39:269–279

    Article  Google Scholar 

  • Zhou Z, Takaya N, Nakamura A, Yamaguchi M, Takeo K, Shoun H (2002) Ammonia fermentation, a novel anoxic metabolism of nitrate by fungi. J Biol Chem 277:1892–1896

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We acknowledge the assistance of Yi Zhou (University of Adelaide) for soil collection and the Australian Centre for Plant Functional Genomics for the analysis of qPCR data.

Funding

This study was funded by the Yitpi Foundation (UA0006005964).

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Authors and Affiliations

  1. School of Agriculture, Food & Wine, The University of Adelaide, Adelaide, SA, 5064, Australia

    Thang V. Lai, Maarten H. Ryder, Judith R. Rathjen, Adam E. Croxford & Matthew D. Denton

  2. Global Centre for Environmental Remediation, University of Newcastle, Callaghan, NSW, 2308, Australia

    Nanthi S. Bolan

  3. Cooperative Research Centre for High Performance Soils (Soil CRC), Newcastle, NSW, 2308, Australia

    Nanthi S. Bolan

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  1. Thang V. Lai
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  2. Maarten H. Ryder
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  3. Judith R. Rathjen
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  5. Adam E. Croxford
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  6. Matthew D. Denton
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Correspondence to Matthew D. Denton.

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Lai, T.V., Ryder, M.H., Rathjen, J.R. et al. Dissimilatory nitrate reduction to ammonium increased with rising temperature. Biol Fertil Soils 57, 363–372 (2021). https://doi.org/10.1007/s00374-020-01529-x

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  • DOI: https://doi.org/10.1007/s00374-020-01529-x

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