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RESEARCH ARTICLE

Effects of pH and mineralisation on nitrification in a subtropical acid forest soil

Wei Zhao A B , Jin-bo Zhang A C D E H , Christoph Müller F G and Zu-cong Cai A C D E
+ Author Affiliations
- Author Affiliations

A School of Geography Sciences, Nanjing Normal University, Nanjing 210023, China.

B School of Environmental Science and Engineering, Nanjing Tech University, Nanjing 211816, Jiangsu, China.

C Key Laboratory of Virtual Geographic Environment (Nanjing Normal University), Ministry of Education, Nanjing, 210023, China.

D State Key Laboratory Cultivation Base of Geographical Environment Evolution (Jiangsu Province), Nanjing, 210023, China.

E Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and Application, Nanjing, 210023, China.

F Department of Plant Ecology (IFZ), Justus-Liebig University Giessen, Heinrich-Buff-Ring 26, 35392 Giessen, Germany.

G School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland.

H Corresponding author. Email: zhangjinbo@njnu.edu.cn

Soil Research 56(3) 275-283 https://doi.org/10.1071/SR17087
Submitted: 20 March 2017  Accepted: 12 October 2017   Published: 7 December 2017

Abstract

Effects of pH on nitrification have been explored widely; however, few researchers have investigated the compound effects of pH and mineralisation on nitrification and responsible nitrifiers in subtropical forest soils. An acid subtropical forest soil was subjected to pH treatments by liming for 40 days at 25°C and 60% water holding capacity. After 40 days, gross N transformation rates in the samples were evaluated using the 15N tracing technique and model. Ammonia-oxidising bacteria (AOB) and ammonia-oxidising archaea (AOA) were quantified by quantitative polymerase chain reaction. The results showed that gross rates of mineralisation (P < 0.01), NH4+ oxidation to NO3 (P < 0.01), and dissimilatory NO3 reduction to ammonium (DNRA, P < 0.05) significantly increased with elevated soil pH. The NH4+ oxidation to NO3 rates and N mineralisation rates were significantly correlated (P < 0.05). The abundance of AOB (P < 0.05) but not AOA amoA genes dramatically increased in the elevated pH treatments after 40 days. We suggest that the N mineralisation was sensitive to elevated pH in the subtropical acid forest soil, which increased the supply rate of nitrification substrate and the favourable pH microsites for nitrifiers. Interactions between elevated pH and mineralisation have a synergistic and stimulatory effect on development of AOB and their associated nitrifying activity.

Additional Keywords: 15N tracing model, AOB, gross N transformation, liming, pH microsite.


References

Bäckman JSK, Klemedtsson ÅK (2003) Increased nitrification in acid coniferous forest soil due to high nitrogen deposition and liming. Scandinavian Journal of Forest Research 18, 514–524.
Increased nitrification in acid coniferous forest soil due to high nitrogen deposition and liming.Crossref | GoogleScholarGoogle Scholar |

Burton S, Prosser J (2001) Autotrophic ammonia oxidation at low pH through urea hydrolysis. Applied and Environmental Microbiology 67, 2952–2957.
Autotrophic ammonia oxidation at low pH through urea hydrolysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvFSntLs%3D&md5=b359b114f3c6b9e8ef5d90dc481e016bCAS |

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? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 368, 20130122
Nitrous oxide emissions from soils: how well do we understand the processes and their controls?Crossref | GoogleScholarGoogle Scholar |

Carrino-Kyker SR, Kluber LA, Petersen SM, Coyle KP, Hewins CR, DeForest JL, Smemo KA, Burke DJ (2016) Mycorrhizal fungal communities respond to experimental elevation of soil pH and P availability in temperate hardwood forests. FEMS Microbiology Ecology 92, fiw024
Mycorrhizal fungal communities respond to experimental elevation of soil pH and P availability in temperate hardwood forests.Crossref | GoogleScholarGoogle Scholar |

Cheng Y, Wang J, Mary B, Zhang J-b, Cai Z-c, Chang SX (2013) Soil pH has contrasting effects on gross and net nitrogen mineralizations in adjacent forest and grassland soils in central Alberta, Canada. Soil Biology & Biochemistry 57, 848–857.
Soil pH has contrasting effects on gross and net nitrogen mineralizations in adjacent forest and grassland soils in central Alberta, Canada.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslejsbbN&md5=5e1f8d7f3bbb2c2b86d964bf32b0f351CAS |

Curtin D, Campbell CA, Jalil A (1998) Effects of acidity on mineralization: pH-dependence of organic matter mineralization in weakly acidic soils. Soil Biology & Biochemistry 30, 57–64.
Effects of acidity on mineralization: pH-dependence of organic matter mineralization in weakly acidic soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtVantQ%3D%3D&md5=9d5d7c365cde905b7ba97c89b2138d73CAS |

De Boer W, Kowalchuk GA (2001) Nitrification in acid soils: micro-organisms and mechanisms. Soil Biology & Biochemistry 33, 853–866.
Nitrification in acid soils: micro-organisms and mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksVOrtb8%3D&md5=f4d087c32508179ab2d074118b948f6aCAS |

de Boer W, Duyts H, Laanbroek HJ (1988) Autotrophic nitrification in a fertilized acid heath soil. Soil Biology & Biochemistry 20, 845–850.
Autotrophic nitrification in a fertilized acid heath soil.Crossref | GoogleScholarGoogle Scholar |

De Boer W, Tietema A, Gunnewiek P, Laanbroek HJ (1992) The chemolithotrophic ammonium-oxidizing community in a nitrogen-saturated acid forest soil in relation to pH-dependent nitrifying activity. Soil Biology & Biochemistry 24, 229–234.
The chemolithotrophic ammonium-oxidizing community in a nitrogen-saturated acid forest soil in relation to pH-dependent nitrifying activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFKjurg%3D&md5=ad9785bc388d5d47f6c89f130b686e77CAS |

Guggenberger G, Christensen BT, Zech W (1994) Land-use effects on the composition of organic matter in particle-size separates of soil: I. Lignin and carbohydrate signature. European Journal of Soil Science 45, 449–458.
Land-use effects on the composition of organic matter in particle-size separates of soil: I. Lignin and carbohydrate signature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXltlamsrg%3D&md5=72d6eed89a7d6ceed566662c38bd3e79CAS |

Guo X, Chen HYH, Meng M, Biswas SR, Ye L, Zhang J (2016) Effects of land use change on the composition of soil microbial communities in a managed subtropical forest. Forest Ecology and Management 373, 93–99.
Effects of land use change on the composition of soil microbial communities in a managed subtropical forest.Crossref | GoogleScholarGoogle Scholar |

He JZ, Hu HW, Zhang LM (2012) Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biology & Biochemistry 55, 146–154.
Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlWltrbK&md5=e8c50498200707b0a1bf4d358e99f36dCAS |

Herrmann A, Witter E, Kätterer T (2005) A method to assess whether ‘preferential use’ occurs after 15N ammonium addition; implication for the 15N isotope dilution technique. Soil Biology & Biochemistry 37, 183–186.
A method to assess whether ‘preferential use’ occurs after 15N ammonium addition; implication for the 15N isotope dilution technique.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVKntb4%3D&md5=5aa34bed25dd5ae45061f7faf84ec804CAS |

Jiang XJ, Hou XY, Zhou X, Xin XP, Wright A, Ji ZJ (2015) pH regulates key players of nitrification in paddy soils. Soil Biology & Biochemistry 81, 9–16.
pH regulates key players of nitrification in paddy soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFWitrzF&md5=9a1a0c09a33fe1a7e629999ea0a5e286CAS |

Kemmitt SJ, Wright D, Goulding KWT, Jones DL (2006) pH regulation of carbon and nitrogen dynamics in two agricultural soils. Soil Biology & Biochemistry 38, 898–911.
pH regulation of carbon and nitrogen dynamics in two agricultural soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvFSisb4%3D&md5=4445664d04340f8154043848827a93edCAS |

Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proceedings of the National Academy of Sciences of the United States of America 108, 15892–15897.
Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1emtbzK&md5=c5b1c3252fe5061bdd703dfb4b142445CAS |

Müller C, Stevens RJ, Laughlin RJ (2004) A 15N tracing model to analyse N transformations in old grassland soil. Soil Biology & Biochemistry 36, 619–632.
A 15N tracing model to analyse N transformations in old grassland soil.Crossref | GoogleScholarGoogle Scholar |

Müller C, Rütting T, Kattge J, Laughlin RJ, Stevens RJ (2007) Estimation of parameters in complex 15N tracing models by Monte Carlo sampling. Soil Biology & Biochemistry 39, 715–726.
Estimation of parameters in complex 15N tracing models by Monte Carlo sampling.Crossref | GoogleScholarGoogle Scholar |

Murphy DV, Recous S, Stockdale EA, Fillery IRP, Jensen LS, Hatch DJ, Goulding KWT (2003) Gross nitrogen fluxes in soil: Theory, measurement and application of 15N pool dilution techniques. Advances in Agronomy 79, 69–118.
Gross nitrogen fluxes in soil: Theory, measurement and application of 15N pool dilution techniques.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltlGqsr8%3D&md5=fbd143768b028ec89f029c77a9ee0510CAS |

Noyes HA, Conner SD (1919) Nitrates, nitrification, and bacterial contents of five typical acid soils as affected by lime, fertilizer, crops, and moisture. Journal of Agricultural Research 16, 27–42.

Nugroho RA, Röling WFM, Laverman AM, Verhoef HA (2007) Low nitrification rates in acid scots pine forest soils are due to pH-related factors. Microbial Ecology 53, 89–97.
Low nitrification rates in acid scots pine forest soils are due to pH-related factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFWisLw%3D&md5=6f7ad4ddee2d0a86de36d90b2d0bf4f2CAS |

O’Sullivan CA, Wakelin SA, Fillery IRP, Roper MM (2013) Factors affecting ammonia-oxidising microorganisms and potential nitrification rates in southern Australian agricultural soils. Soil Research 51, 240–252.
Factors affecting ammonia-oxidising microorganisms and potential nitrification rates in southern Australian agricultural soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVWmur7M&md5=56eb1852cff2fa052d57437e23de730fCAS |

Aciego Pietri JC, Brookes PC (2008) Nitrogen mineralisation along a pH gradient of a silty loam UK soil. Soil Biology & Biochemistry 40, 797–802.
Nitrogen mineralisation along a pH gradient of a silty loam UK soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisFKrtg%3D%3D&md5=b3544906445253ea21ccf2a9e6ccf666CAS |

Prosser JI (1989) Autotrophic nitrification in bacteria. Advances in Microbial Physiology 30, 125–181.
Autotrophic nitrification in bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXls1ymt7Y%3D&md5=34c04bb6134a4b5f069d993b4d1e4fd9CAS |

Roth VN, Dittmar T, Gaupp R, Gleixner G (2015) The molecular composition of dissolved organic matter in forest soils as a function of pH and temperature. PLoS One 10, e0119188
The molecular composition of dissolved organic matter in forest soils as a function of pH and temperature.Crossref | GoogleScholarGoogle 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.
Assessment of the importance of dissimilatory nitrate reduction to ammonium for the terrestrial nitrogen cycle.Crossref | GoogleScholarGoogle Scholar |

Sierra J (2006) A hot-spot approach applied to nitrification in tropical acid soils. Soil Biology & Biochemistry 38, 644–652.
A hot-spot approach applied to nitrification in tropical acid soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XivVaqsb8%3D&md5=6f050620b1702e04afb39f2e0ec0c548CAS |

Silver WL, Herman DJ, Firestone MK (2001) Dissimilatory Nitrate Reduction to Ammonium in Upland Tropical Forest Soils. Ecology 82, 2410–2416.
Dissimilatory Nitrate Reduction to Ammonium in Upland Tropical Forest Soils.Crossref | GoogleScholarGoogle Scholar |

Stempfhuber B, Engel M, Fischer D, Neskovic-Prit G, Wubet T, Schöning I, Gubry-Rangin C, Kublik S, Schloter-Hai B, Rattei T, Welzl G, Nicol GW, Schrumpf M, Buscot F, Prosser JI, Schloter M (2015) pH as a driver for ammonia-oxidizing archaea in forest soils. Microbial Ecology 69, 879–883.
pH as a driver for ammonia-oxidizing archaea in forest soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitV2gtLfP&md5=785c4f4d8c94c437130582231445085dCAS |

Suzuki I, Dular U, Kwok SC (1974) Ammonia or ammonium ion as substrate for oxidation by Nitrosomonas europaea cells and extracts. Journal of Bacteriology 120, 556–558.

Tietema A, Warmerdam B, Lenting E, Riemer L (1992) Abiotic factors regulating nitrogen transformations in the organic layer of acid forest soils: Moisture and pH. Plant and Soil 147, 69–78.
Abiotic factors regulating nitrogen transformations in the organic layer of acid forest soils: Moisture and pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXht1emu70%3D&md5=df2280e64b9c26b961277c5e9fda85cbCAS |

Tonon G, Sohi S, Francioso O, Ferrari E, Montecchio D, Gioacchini P, Ciavatta C, Panzacchi P, Powlson D (2010) Effect of soil pH on the chemical composition of organic matter in physically separated soil fractions in two broadleaf woodland sites at Rothamsted, UK. European Journal of Soil Science 61, 970–979.
Effect of soil pH on the chemical composition of organic matter in physically separated soil fractions in two broadleaf woodland sites at Rothamsted, UK.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXks1Ki&md5=bf9966f46233c97f70d51a7613b8aa41CAS |

van Bergen PF, Nott CJ, Bull ID, Poulton PR, Evershed RP (1998) Organic geochemical studies of soils from the Rothamsted Classical Experiments - IV. Preliminary results from a study of the effect of soil pH on organic matter decay. Organic Geochemistry 29, 1779–1795.
Organic geochemical studies of soils from the Rothamsted Classical Experiments - IV. Preliminary results from a study of the effect of soil pH on organic matter decay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXpvVertg%3D%3D&md5=cdd5c129a35881a392e3b068ae0cfed5CAS |

Wang X, Tang C, Baldock JA, Butterly CR, Gazey C (2016) Long-term effect of lime application on the chemical composition of soil organic carbon in acid soils varying in texture and liming history. Biology and Fertility of Soils 52, 295–306.
Long-term effect of lime application on the chemical composition of soil organic carbon in acid soils varying in texture and liming history.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVaqsrrE&md5=e746f41004c033bea22638262190702cCAS |

Weber DF, Gainey PL (1962) Relative sensitivity of nitrifying organisms to hydrogen ions in soils and solutions. Soil Science 94, 138–145.
Relative sensitivity of nitrifying organisms to hydrogen ions in soils and solutions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXkvVeqsbk%3D&md5=90761a4d77d5b24390d0922087e8bf26CAS |

Weier KL, Gilliam JW (1986) Effect of acidity on nitrogen mineralization and nitrification in Atlantic coastal plain soils. Soil Science Society of America Journal 50, 1210–1214.
Effect of acidity on nitrogen mineralization and nitrification in Atlantic coastal plain soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xmt1Ghsr4%3D&md5=0959c0d1d3c341a43ac4de892a88863bCAS |

Zhang JB, Cai ZC, Zhu TB (2011a) N2O production pathways in the subtropical acid forest soils in China. Environmental Research 111, 643–649.
N2O production pathways in the subtropical acid forest soils in China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVWms7k%3D&md5=6da9e8e7a00c88caaba715fff55cef60CAS |

Zhang JB, Müller C, Zhu TB, Cheng Y, Cai ZC (2011b) Heterotrophic nitrification is the predominant NO3 − production mechanism in coniferous but not broad-leaf acid forest soil in subtropical China. Biology and Fertility of Soils 47, 533–542.
Heterotrophic nitrification is the predominant NO3 production mechanism in coniferous but not broad-leaf acid forest soil in subtropical China.Crossref | GoogleScholarGoogle Scholar |

Zhang JB, Cai ZC, Zhu TB, Yang WY, Müller C (2013a) Mechanisms for the retention of inorganic N in acidic forest soils of southern China. Scientific Reports 3, 2342

Zhang Y, Zhang J, Meng T, Zhu T, Müller C, Cai Z (2013b) Heterotrophic nitrification is the predominant NO3 − production pathway in acid coniferous forest soil in subtropical China. Biology and Fertility of Soils 49, 955–957.
Heterotrophic nitrification is the predominant NO3 production pathway in acid coniferous forest soil in subtropical China.Crossref | GoogleScholarGoogle Scholar |

Zhang JB, Lan T, Müller C, Cai ZC (2015) Dissimilatory nitrate reduction to ammonium (DNRA) plays an important role in soil nitrogen conservation in neutral and alkaline but not acidic rice soil. Journal of Soils and Sediments 15, 523–531.
Dissimilatory nitrate reduction to ammonium (DNRA) plays an important role in soil nitrogen conservation in neutral and alkaline but not acidic rice soil.Crossref | GoogleScholarGoogle Scholar |

Zhang J, Tian P, Tang J, Yuan L, Ke Y, Cai Z, Zhu B, Mueller C (2016) The characteristics of soil N transformations regulate the composition of hydrologic N export from terrestrial ecosystem. Journal of Geophysical Research. Biogeosciences 121, 1409–1419.
The characteristics of soil N transformations regulate the composition of hydrologic N export from terrestrial ecosystem.Crossref | GoogleScholarGoogle Scholar |

Zhao W, Cai ZC (2011) Nitrification model of the time course characteristics of subtropical red soils and factor analysis. Ecology and Environmental Sciences 20, 1387–1394. [In Chinese]

Zhao W, Cai ZC, Xu ZH (2007) Does ammonium-based N addition influence nitrification and acidification in humid subtropical soils of China? Plant and Soil 297, 213–221.
Does ammonium-based N addition influence nitrification and acidification in humid subtropical soils of China?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptFegsbs%3D&md5=1ff1e482d5b87ed3de46f8c0224e64afCAS |

Zhao W, Cai Z, Xu Z (2015) Net and gross N transformation rates in subtropical forest soils under aerobic and anaerobic conditions. Journal of Soils and Sediments 15, 96–105.
Net and gross N transformation rates in subtropical forest soils under aerobic and anaerobic conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFWktbjE&md5=c8f866028b22d3125f83a978094a77c5CAS |

Zhao W, Zhang JB, Müller C, Cai ZC (2017) Mechanisms behind the stimulation of nitrification by N input in subtropical acid forest soil. Journal of Soils and Sediments 17, 2338–2345.
Mechanisms behind the stimulation of nitrification by N input in subtropical acid forest soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XptFSktrw%3D&md5=c44dc637abf687e73a38164e2b076e6eCAS |