Journal of Soils and Sediments

, Volume 15, Issue 11, pp 2304–2309 | Cite as

Influence of temperature and moisture on the relative contributions of heterotrophic and autotrophic nitrification to gross nitrification in an acid cropping soil

  • Rui LiuEmail author
  • Helen Suter
  • Jizheng He
  • Helen Hayden
  • Deli Chen
Soils, Sec 5 • Soil and Landscape Ecology • Short Original Communication



Nitrate can be produced through autotrophic and heterotrophic nitrification. Soil temperature and moisture are key factors affecting nitrification; however, how they influence the relative importance of autotrophic and heterotrophic nitrification is still unknown. The aim of this study was to determine the effects of soil temperature and moisture on autotrophic and heterotrophic nitrification in an acid cropping soil.

Materials and methods

An acid cropping soil (pHH2O 4.5) with high organic matter content (6.2 %) was collected from a wheat cropping system and used in a laboratory incubation experiment. Nitrogen as 15NH4Cl and K15NO3 was applied to soil samples which were then incubated for 7 days under 15 °C, 25 °C and 35 °C and 50 % and 70 % water-filled pore space (WFPS). 15N dilution and acetylene (C2H2) inhibition techniques were used to distinguish autotrophic and heterotrophic nitrification. We measured nitrate (NO3 ) and ammonium (NH4 +) concentration and 15NO3 and 15NH4 + enrichment during the incubation.

Results and discussion

The result showed that more heterotrophic nitrification was observed under lower temperature (15 °C) conditions. Around 69 % of the NO3 produced was a result of heterotrophic nitrification at 15 °C and 50 % WFPS and 50 % at 15 °C and 70 % WFPS. However, at 25 and 35 °C, nitrification was largely autotrophic regardless of moisture.


Our results demonstrate that heterotrophic nitrification can be an important N transformation pathway in the studied soil. The contribution of heterotrophic nitrification decreased with increasing temperature and moisture.


15N dilution technique Acetylene Autotrophic nitrification Heterotrophic nitrification Moisture Temperature 



The authors would like to acknowledge the financial support of Incitec Pivot Limited and the Australian Government Department of Agriculture through the Grains Research and Development Corporation.


  1. Allen SC, Jose S, Nair PKR, Brecke BJ, Nair VD, Graetz DA, Ramsey CL (2005) Nitrogen mineralization in a pecan (Carya illinoensis K. Koch)-cotton (Gossypium hirsutum L.) ally cropping system in the southern United States. Biol Fertil Soils 41:28–37CrossRefGoogle Scholar
  2. Avrahami S, Bohannan BJM (2007) Response of Nitrosospira sp. strain AF-like ammonia oxidizers to changes in temperature, soil moisture content, and fertilizer concentration. Appl Environ Microbiol 73:1166–1173CrossRefGoogle Scholar
  3. Barraclough D, Puri G (1995) The use of 15N pool dilution and enrichment to separate the heterotrophic and autotrophic pathways of nitrification. Soil Biol Biochem 27:17–22CrossRefGoogle Scholar
  4. Breuer L, Kiese R, Butterbach-Bahl K (2002) Temperature and moisture effects on nitrification rates in tropical rain-forest soils. Soil Sci Soc Am J 66:834–844CrossRefGoogle Scholar
  5. Cabrera ML, Chiang SC (1994) Water content effect on denitrification and ammonia volatilization in poultry litter. Soil Sci Soc Am J 58:811–816CrossRefGoogle Scholar
  6. Cai Y, Ding W, Zhang X, Yu HY, Wang LF (2010) Contribution of heterotrophic nitrification to nitrous oxide production in a long-term N-fertilized arable black soil. Commun Soil Sci Plant Anal 41:2264–2278CrossRefGoogle Scholar
  7. De Boer W, Kowalchuk GA (2001) Nitrification in acid soils: microorganisms and mechanisms. Soil Biol Biochem 33:853–866CrossRefGoogle Scholar
  8. De Boer W, Tietema A, Gunnewiek PJA, Laanbroek HJ (1992) The chemolithotrophic ammonium-oxidizing community in a nitrogen-saturated acid forest soil in relation to pH-dependent nitrifying activity. Soil Biol Biochem 24:229–234CrossRefGoogle Scholar
  9. Forcht DD, Verstraete W (1977) Biochemical ecology of nitrification and denitrification. Adv Microb Ecol 1:135–214CrossRefGoogle Scholar
  10. Heubült J (1929) Untersuchungen über nitritbakterien. Planta 8:398–422CrossRefGoogle Scholar
  11. Insam H (1990) Are the soil microbial biomass and basal respiration governed by the climatic regime? Soil Biol Biochem 22:525–532CrossRefGoogle Scholar
  12. Islam A, Chen D, White RE (2007) Heterotrophic and autotrophic nitrification in two acid pasture soils. Soil Biol Biochem 39:972–975CrossRefGoogle Scholar
  13. Killham K (1986) Heterotrophic nitrification. In: Prosser JI (ed) Nitrification: special publications of the society for general microbiology, vol 20. IRL Press, Oxford, pp 117–126Google Scholar
  14. Kuroiwa M, Koba K, Isobe K, Tateno R, Nakanishi A, Inagaki Y, Toda H, Otsuka S, Senoo K, Suwa Y (2011) Gross nitrification rates in four Japanese forest soils: heterotrophic versus autotrophic and the regulation factors for the nitrification. J Environ Sci 16:363–373Google Scholar
  15. Li H, Liang XQ, Chen YX, Lian YF, Tian GM, Ni WZ (2008) Effect of nitrification inhibitor DMPP on nitrogen leaching, nitrifying organisms, and enzyme activities in a rice-oilseed rape cropping system. J Environ Sci 20:149–155CrossRefGoogle Scholar
  16. Liu R, Hayden H, Suter H, He JZ, Chen DL (2015) The effect of nitrification inhibitors in reducing nitrification and the ammonia oxidizer population in three pH-contrasting soils. J Soils Sediments 15:113–118Google Scholar
  17. Moir JWB, Crossman LC, Spiro S, Richardson DJ (1996) The purification of ammonia monooxygenase from Paracoccus denikjicans. FEBS Lett 387:71–74CrossRefGoogle Scholar
  18. Noyes HA, Conner SD (1919) Nitrates, nitrification, and bacterial contents of five typical acid soils as affected by lime, fertilizer, crops and moisture. J Agric Res 16:27–60Google Scholar
  19. Parton WJ, Schimel DS, Cole CV, Ojima DS (1987) Analysis of factors controlling soil organic matter levels in Great Plains grasslands. Soil Sci Soc Am J 51:1173–1179CrossRefGoogle Scholar
  20. Pennington PI, Ellis RC (1993) Autotrophic and heterotophic nitrificaiton in acidic forest and native grassland soils. Soil Biol Biochem 25:1399–1408CrossRefGoogle Scholar
  21. Robertson GP (1982a) Nitrification in forested ecosystems. Philos Trans R Soc B 296:445–457CrossRefGoogle Scholar
  22. Robertson GP (1982b) Factors regulating nitrification in primary and secondary succession. Ecology 63:1561–1573CrossRefGoogle Scholar
  23. Robertson LA, Niel E, Torremans R, Kuenen JG (1988) Simultaneous nitrification and denitrification in aerobic chemostat cultures of thiosphaera pantotropha. Appl Environ Microbiol 54:2812–2818Google Scholar
  24. Saghir NS, Mulvancy RL, Azam F (1993) Determination of nitrogen by microdiffusion in mason jars. I. Inorganic nitrogen in soil extracts. Commun Soil Sci Plan 24:1745–1762CrossRefGoogle Scholar
  25. Szukics U, Abell GCJ, Hödl V, Mitter B, Sessitsch A, Hackl E, Zechmeister-Boltenstern S (2010) Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiol Ecol 72:395–406CrossRefGoogle Scholar
  26. Tiedje JM, Sexstone AJ, Parkin TB, Revsbech NP, Shelton DR (1984) Anaerobic process in soil. Pant Soil 76:197–212CrossRefGoogle Scholar
  27. Troelstra SR, Wagenaar R, De Boer W (1990) Nitrate production in Dutch heathland soils. I. General soil characteristics and nitrification in undisturbed soil cores. PLoS 127:179–192Google Scholar
  28. Walker N, Wickramasinghe KN (1979) Nitrification and autotrophic nitrifying bacteria in acid tea soils. Soil Biol Biochem 11:231–236CrossRefGoogle Scholar
  29. Wallenstein MD, Myrold DD, Firestone M, Voytek M (2006) Environmental controls on denitrifying communities and denitrification rates: insights from molecular methods. Ecol Appl 16:2143–2152CrossRefGoogle Scholar
  30. Weber DF, Gainey PL (1962) Relative sensitivity of nitrifying organisms to hydrogen ions in soils and solutions. Soil Sci 94:138–145CrossRefGoogle Scholar
  31. Weiske A, Benckiser G, Herbert T, Ottow JCG (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 34:109–117CrossRefGoogle Scholar
  32. Wood TG (1988) Termites and the soil environment. Biol Fertil Soils 6:228CrossRefGoogle Scholar
  33. Yuan F, Ran W, Shen Q, Wang D (2005) Characterization of nitrifying bacteria communities of soils from different ecological regions of China by molecular and conventional methods. Biol Fertil Soils 41:21–27CrossRefGoogle Scholar
  34. Zaman M, Chang SX (2004) Substrate type, temperature, and moisture content affect gross and net N mineralization and nitrification rates in agroforestry systems. Biol Fertil Soils 39:269–279CrossRefGoogle Scholar
  35. Zhang YC, Zhang JB, Meng TZ, Zhu TB, Müller C, Cai ZC (2013) Heterotrophic nitrification is the predominant NO3 production pathway in acid coniferous forest soil in subtropical China. Biol Fertil Soils 49:955–957CrossRefGoogle Scholar
  36. Zhang JB, Sun WJ, Zhong WH, Cai ZC (2014) The substrate is an important factor in controlling the significance of heterotrophic nitrification in acidic forest soils. Soil Biol Biochem 76:143–148CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Rui Liu
    • 1
    Email author
  • Helen Suter
    • 1
  • Jizheng He
    • 1
  • Helen Hayden
    • 2
  • Deli Chen
    • 1
  1. 1.Faculty of Veterinary and Agricultural SciencesThe University of MelbourneVictoriaAustralia
  2. 2.Department of Economic DevelopmentJobs, Transport and ResourcesVictoriaAustralia

Personalised recommendations