Chronic Nitrogen Fertilization Modulates Competitive Interactions Among Microbial Ammonia Oxidizers in a Loess Soil
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摘要
Nitrogen(N) application may lead to niche segregation of soil ammonia-oxidizing archaea(AOA) and bacteria(AOB), thereby reducing the competitive interactions between AOA and AOB due to higher ammonium substrate availability. However, the adaptive mechanisms of AOA and AOB under N enrichment remain poorly understood. Stable isotope probing(SIP) microcosm incubation was employed to reveal community changes of active AOA and AOB in a loess soil from a field experiment growing potatoes that received no N(control, CK), low N(LN, 75 kg N ha~(-1)), and high N(HN, 375 kg N ha~(-1)). The results showed that the soil potential nitrification rate(PNR) was measured by culturing of the soil samples from the field experiment. Soil PNR was significantly increased in HN by87.5% and 67.5% compared with CK and LN, respectively. Compared with CK, the~(13)C-amoA genes of soil AOA and AOB in HN had 2.58 × 10~4 and 1.55 × 10~6 copies, representing 1.6-and 16.2-fold increase respectively. It was indicated that AOB dominated soil ammonia oxidation. A phylogenetic analysis of the~(13)C-amoA gene showed that N application significantly increased the proportion of54 d9-like AOA up to 90% in HN, while the Nitrososphaera gargensis-like and Nitrososphaera viennensis-like AOA were inhibited and completely disappeared. Nitrogen application also resulted in the community shift of active AOB-dominant group from Nitrosospira briensis-like to Nitrosospira sp. TCH711-like. Our study provides compelling evidence for the emergence and maintenance of active nitrifying communities under the intensified N input to an agricultural ecosystem.
Nitrogen(N) application may lead to niche segregation of soil ammonia-oxidizing archaea(AOA) and bacteria(AOB), thereby reducing the competitive interactions between AOA and AOB due to higher ammonium substrate availability. However, the adaptive mechanisms of AOA and AOB under N enrichment remain poorly understood. Stable isotope probing(SIP) microcosm incubation was employed to reveal community changes of active AOA and AOB in a loess soil from a field experiment growing potatoes that received no N(control, CK), low N(LN, 75 kg N ha~(-1)), and high N(HN, 375 kg N ha~(-1)). The results showed that the soil potential nitrification rate(PNR) was measured by culturing of the soil samples from the field experiment. Soil PNR was significantly increased in HN by87.5% and 67.5% compared with CK and LN, respectively. Compared with CK, the~(13)C-amoA genes of soil AOA and AOB in HN had 2.58 × 10~4 and 1.55 × 10~6 copies, representing 1.6-and 16.2-fold increase respectively. It was indicated that AOB dominated soil ammonia oxidation. A phylogenetic analysis of the~(13)C-amoA gene showed that N application significantly increased the proportion of54 d9-like AOA up to 90% in HN, while the Nitrososphaera gargensis-like and Nitrososphaera viennensis-like AOA were inhibited and completely disappeared. Nitrogen application also resulted in the community shift of active AOB-dominant group from Nitrosospira briensis-like to Nitrosospira sp. TCH711-like. Our study provides compelling evidence for the emergence and maintenance of active nitrifying communities under the intensified N input to an agricultural ecosystem.
Nitrogen(N) application may lead to niche segregation of soil ammonia-oxidizing archaea(AOA) and bacteria(AOB), thereby reducing the competitive interactions between AOA and AOB due to higher ammonium substrate availability. However, the adaptive mechanisms of AOA and AOB under N enrichment remain poorly understood. Stable isotope probing(SIP) microcosm incubation was employed to reveal community changes of active AOA and AOB in a loess soil from a field experiment growing potatoes that received no N(control, CK), low N(LN, 75 kg N ha~(-1)), and high N(HN, 375 kg N ha~(-1)). The results showed that the soil potential nitrification rate(PNR) was measured by culturing of the soil samples from the field experiment. Soil PNR was significantly increased in HN by87.5% and 67.5% compared with CK and LN, respectively. Compared with CK, the~(13)C-amoA genes of soil AOA and AOB in HN had 2.58 × 10~4 and 1.55 × 10~6 copies, representing 1.6-and 16.2-fold increase respectively. It was indicated that AOB dominated soil ammonia oxidation. A phylogenetic analysis of the~(13)C-amoA gene showed that N application significantly increased the proportion of54 d9-like AOA up to 90% in HN, while the Nitrososphaera gargensis-like and Nitrososphaera viennensis-like AOA were inhibited and completely disappeared. Nitrogen application also resulted in the community shift of active AOB-dominant group from Nitrosospira briensis-like to Nitrosospira sp. TCH711-like. Our study provides compelling evidence for the emergence and maintenance of active nitrifying communities under the intensified N input to an agricultural ecosystem.
引文
Ai C,Liang G Q,Sun J W,Wang X B,He P,Zhou W.2013.Different roles of rhizosphere effect and long-term fertilization in the activity and community structure of ammonia oxidizers in a calcareous fluvo-aquic soil.Soil Biol Biochem.57:30-42.
Allison S M,Prosser J I.1993.Ammonia oxidation at low pHby attached populations of nitrifying bacteria.Soil Biol Biochem.25:935-941.
Arp D J,Bottomley P J.2006.Nitrifiers:More than 100 years from isolation to genome sequences.Microbe.1:229-234.
Bates S T,Berg-Lyons D,Caporaso J G,Walters W A,Knight R,Fierer N.2011.Examining the global distribution of dominant archaeal populations in soil.ISME J.5:908-917.
Burton S A Q,Prosser J I.2001.Autotrophic ammonia oxidation at low pH through urea hydrolysis.Appl Environ Microbiol.67:2952-2957.
Chen Y L,Hu H W,Han H Y,Du Y,Wan S Q,Xu Z W,Chen BD.2014.Abundance and community structure of ammoniaoxidizing Archaea and Bacteria in response to fertilization and mowing in a temperate steppe in Inner Mongolia.FEMSMicrobiol Ecol.89:67-79.
Chu H Y,Fujii T,Morimoto S,Lin X G,Yagi K,Hu J L,Zhang JB.2007.Community structure of ammonia-oxidizing bacteria under long-term application of mineral fertilizer and organic manure in a sandy loam soil.Appl Environ Microbiol.73:485-491.
Dessureault-Rompr′e J,Zebarth B J,Georgallas A,Burton D L,Grant C A,Drury C F.2010.Temperature dependence of soil nitrogen mineralization rate:Comparison of mathematical models,reference temperatures and origin of the soils.Geoderma.157:97-108.
Di H J,Cameron K C,Shen J P,Winefield C S,O’Callaghan M,Bowatte S,He J Z.2009.Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils.Nat Geosci.2:621-624.
Erguder T H,Boon N,Wittebolle L,Marzorati M,Verstraete W.2009.Environmental factors shaping the ecological niches of ammonia-oxidizing archaea.FEMS Microbiol Rev.33:855-869.
Francis C A,Roberts K J,Beman J M,Santoro A E,Oakley B B.2005.Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean.Proc Natl Acad Sci USA.102:14683-14688.
Gubry-Rangin C,Nicol G W,Prosser J I.2010.Archaea rather than bacteria control nitrification in two agricultural acidic soils.FEMS Microbiol Ecol.74:566-574.
Hatzenpichler R,Lebedeva E V,Spieck E,Stoecker K,Richter A,Daims H,Wagner M.2008.A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring.Proc Natl Acad Sci USA.105:2134-2139.
He J Z,Shen J P,Zhang L M,Zhu Y G,Zheng Y M,Xu M G,Di H J.2007.Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices.Environ Microbiol.9:2364-2374.
He J Z,Zhang L M.2009.Advances in ammonia-oxidizing microorganisms and global nitrogen cycle.Acta Ecol Sinica(in Chinese).29:406-415.
He J Z,Zhang L M.2013.Key processes and microbial mechanisms of soil nitrogen transformation.Microbiol China(in Chinese).40:98-108.
Hu H W,He J Z.2017.Comammox-a newly discovered nitrification process in the terrestrial nitrogen cycle.J Soils Sediments 17:2709-2717.
Hyman M R,Arp D J.1992.14C2H2-and14CO2-labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase.J Biol Chem.267:1534-1545.
Jia Z J,Conrad R.2009.Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil.Environ Microbiol.11:1658-1671.
Jiang X J,Hou X Y,Zhou X,Xin X P,Wright A,Jia ZJ.2015.p H regulates key players of nitrification in paddy soils.Soil Biol Biochem.81:9-16.
Kemmitt S J,Wright D,Goulding K W T,Jones D L.2006.pHregulation of carbon and nitrogen dynamics in two agricultural soils.Soil Biol Biochem.38:898-911.
Kits K D,Sedlacek C J,Lebedeva E V,Han P,Bulaev A,Pjevac P,Daebeler A,Romano S,Albertsen M,Stein L Y,Daims H,Wagner M.2017.Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle.Nature.549:269-272.
K¨onneke M,Bernhard A E,De La Torre J R,Walker C B,Waterbury J B,Stahl D A.2005.Isolation of an autotrophic ammonia-oxidizing marine archaeon.Nature.437:543-546.
Kumar S,Stecher G,Tamura K.2016.MEGA7:Molecular evolutionary genetics analysis version 7.0 for bigger datasets.Mol Biol Evol.33:1870-1874.
Kurola J,Salkinoja-Salonen M,Aarnio T,Hultman J,Romantschuk M.2005.Activity,diversity and population size of ammonia-oxidising bacteria in oil-contaminated landfarming soil.FEMS Microbiol Lett.250:33-38.
Lehtovirta-Morley L E,Stoecker K,Vilcinskas A,Prosser JI,Nicol G W.2011.Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil.Proc Natl Acad Sci USA.108:15892-15897.
Li Y Y,Chapman S J,Nicol G W,Yao H Y.2018.Nitrification and nitrifiers in acidic soils.Soil Biol Biochem.116:290-301.
Lu L,Han W Y,Zhang J B,Wu Y C,Wang B Z,Lin X G,Zhu J G,Cai Z C,Jia Z J.2012.Nitrification of archaeal ammonia oxidizers in acid soils is supported by hydrolysis of urea.ISME J.6:1978-1984.
Lueders T,Manefield M,Friedrich M W.2004.Enhanced sensitivity of DNA-and r RNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients.Environ Microbiol.6:73-78.
Martens-Habbena W,Berube P M,Urakawa H,De La Torre JR,Stahl D A.2009.Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria.Nature.461:976-979.
Neufeld J D,Vohra J,Dumont M G,Lueders T,Manefield M,Friedrich M W,Murrell J C.2007.DNA stable-isotope probing.Nat Protoc.2:860-866.
Pratscher J,Dumont M G,Conrad R.2011.Ammonia oxidation coupled to CO2 fixation by archaea and bacteria in an agricultural soil.Proc Natl Acad Sci USA.108:4170-4175.
Prosser J I.1989.Autotrophic nitrification in bacteria.In Rose A H,Tempest D W(eds.)Advances in Microbial Physiology.Volume 30.Academic Press,London.pp.125-181.
Prosser J I.2010.Soil nitrifiers and nitrification.In Ward B B,Arp D J,Klotz M G(eds.)Nitrification.American Society for Microbiology Press,Washington D.C.pp.347-381.
Rotthauwe J H,Witzel K P,Liesack W.1997.The ammonia monooxygenase structural gene amoA as a functional marker:Molecular fine-scale analysis of natural ammonia-oxidizing populations.Appl Environ Microbiol.63:4704-4712.
Saitou N,Nei M.1987.The neighbor-joining method:A new method for reconstructing phylogenetic trees.Mol Biol Evol.4:406-425.
Schloss P D,Westcott S L,Ryabin T,Hall J R,Hartmann M,Hollister E B,Lesniewski R A,Oakley B B,Parks D H,Robinson C J.2009.Introducing mothur:Open-source,platformindependent,community-supported software for describing and comparing microbial communities.Appl Environ Microbiol.75:7537-7541.
Shen J P,Zhang L M,Zhu Y G,Zhang J B,He J Z.2008.Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam.Environ Microbiol.10:1601-1611.
Shen X Y,Zhang L M,Shen J P,Li L H,Yuan C L,He JZ.2011.Nitrogen loading levels affect abundance and composition of soil ammonia oxidizing prokaryotes in semiarid temperate grassland.J Soil Sediment.11:1243.
Stopniˇsek N,Gubry-Rangin C,H¨offerleˇS,Nicol G W,MandiˇcMulec I,Prosser J I.2010.Thaumarchaeal ammonia oxidation in an acidic forest peat soil is not influenced by ammonium amendment.Appl Environ Microbiol.76:7626-7634.
Tourna M,Stieglmeier M,Spang A,K¨onneke M,Schintlmeister A,Urich T,Engel M,Schloter M,Wagner M,Richter A,Schleper C.2011.Nitrososphaera viennensis,an ammonia oxidizing archaeon from soil.Proc Natl Acad Sci USA.108:8420-8425.
Treusch A H,Leininger S,Kletzin A,Schuster S C,Klenk H P,Schleper C.2005.Novel genes for nitrite reductase and amorelated proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling.Environ Microbiol.7:1985-1995.
Venter J C,Remington K,Heidelberg J F,Halpern A L,Rusch D,Eisen J A,Wu D Y,Paulsen I,Nelson K E,Nelson W,Fouts D E,Levy S,Knap A H,Lomas M W,Nealson K,White O,Peterson J,Hoffman J,Parsons R,Baden-Tillson H,Pfannkoch C,Rogers Y H,Smith H O.2004.Environmental genome shotgun sequencing of the Sargasso Sea.Science.304:66-74.
Wertz S,Leigh A K K,Grayston S J.2012.Effects of long-term fertilization of forest soils on potential nitrification and on the abundance and community structure of ammonia oxidizers and nitrite oxidizers.FEMS Microbiol Ecol.79:142-154.
Xi R J,Long X E,Huang S,Yao H Y.2017.pH rather than nitrification and urease inhibitors determines the community of ammonia oxidizers in a vegetable soil.AMB Express.7:129.
Xia W W,Zhang C X,Zeng X W,Feng Y Z,Weng J H,Lin XG,Zhu J G,Xiong Z Q,Xu J,Cai Z C,Jia Z J.2011.Autotrophic growth of nitrifying community in an agricultural soil.ISME J.5:1226-1236.
Xiao K C,Xu J M,Tang C X,Zhang J B,Brookes P C.2013.Differences in carbon and nitrogen mineralization in soils of differing initial pH induced by electrokinesis and receiving crop residue amendments.Soil Biol Biochem.67:70-84.
Yao H Y,Gao Y M,Nicol G W,Campbell C D,Prosser J I,Zhang L M,Han W Y,Singh B K.2011.Links between ammonia oxidizer community structure,abundance,and nitrification potential in acidic soils.Appl Environ Microbiol.77:4618-4625.
Ye C,Cheng X L,Zhang Y L,Wang Z X,Zhang Q F.2012.Soil nitrogen dynamics following short-term revegetation in the water level fluctuation zone of the Three Gorges Reservoir,China.Ecol Eng.38:37-44.
Zhang L M,Hu H W,Shen J P,He J Z.2012.Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils.ISMEJ.6:1032-1045.
Zhang M M,Alves R J E,Zhang D D,Han L L,He J Z,Zhang LM.2017.Time-dependent shifts in populations and activity of bacterial and archaeal ammonia oxidizers in response to liming in acidic soils.Soil Biol Biochem.112:77-89.
Zhou X,Fornara D,Wasson E A,Wang D M,Ren G D,Christie P,Jia Z J.2015.Effects of 44 years of chronic nitrogen fertilization on the soil nitrifying community of permanent grassland.Soil Biol Biochem.91:76-83.
Allison S M,Prosser J I.1993.Ammonia oxidation at low pHby attached populations of nitrifying bacteria.Soil Biol Biochem.25:935-941.
Arp D J,Bottomley P J.2006.Nitrifiers:More than 100 years from isolation to genome sequences.Microbe.1:229-234.
Bates S T,Berg-Lyons D,Caporaso J G,Walters W A,Knight R,Fierer N.2011.Examining the global distribution of dominant archaeal populations in soil.ISME J.5:908-917.
Burton S A Q,Prosser J I.2001.Autotrophic ammonia oxidation at low pH through urea hydrolysis.Appl Environ Microbiol.67:2952-2957.
Chen Y L,Hu H W,Han H Y,Du Y,Wan S Q,Xu Z W,Chen BD.2014.Abundance and community structure of ammoniaoxidizing Archaea and Bacteria in response to fertilization and mowing in a temperate steppe in Inner Mongolia.FEMSMicrobiol Ecol.89:67-79.
Chu H Y,Fujii T,Morimoto S,Lin X G,Yagi K,Hu J L,Zhang JB.2007.Community structure of ammonia-oxidizing bacteria under long-term application of mineral fertilizer and organic manure in a sandy loam soil.Appl Environ Microbiol.73:485-491.
Dessureault-Rompr′e J,Zebarth B J,Georgallas A,Burton D L,Grant C A,Drury C F.2010.Temperature dependence of soil nitrogen mineralization rate:Comparison of mathematical models,reference temperatures and origin of the soils.Geoderma.157:97-108.
Di H J,Cameron K C,Shen J P,Winefield C S,O’Callaghan M,Bowatte S,He J Z.2009.Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils.Nat Geosci.2:621-624.
Erguder T H,Boon N,Wittebolle L,Marzorati M,Verstraete W.2009.Environmental factors shaping the ecological niches of ammonia-oxidizing archaea.FEMS Microbiol Rev.33:855-869.
Francis C A,Roberts K J,Beman J M,Santoro A E,Oakley B B.2005.Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean.Proc Natl Acad Sci USA.102:14683-14688.
Gubry-Rangin C,Nicol G W,Prosser J I.2010.Archaea rather than bacteria control nitrification in two agricultural acidic soils.FEMS Microbiol Ecol.74:566-574.
Hatzenpichler R,Lebedeva E V,Spieck E,Stoecker K,Richter A,Daims H,Wagner M.2008.A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring.Proc Natl Acad Sci USA.105:2134-2139.
He J Z,Shen J P,Zhang L M,Zhu Y G,Zheng Y M,Xu M G,Di H J.2007.Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices.Environ Microbiol.9:2364-2374.
He J Z,Zhang L M.2009.Advances in ammonia-oxidizing microorganisms and global nitrogen cycle.Acta Ecol Sinica(in Chinese).29:406-415.
He J Z,Zhang L M.2013.Key processes and microbial mechanisms of soil nitrogen transformation.Microbiol China(in Chinese).40:98-108.
Hu H W,He J Z.2017.Comammox-a newly discovered nitrification process in the terrestrial nitrogen cycle.J Soils Sediments 17:2709-2717.
Hyman M R,Arp D J.1992.14C2H2-and14CO2-labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase.J Biol Chem.267:1534-1545.
Jia Z J,Conrad R.2009.Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil.Environ Microbiol.11:1658-1671.
Jiang X J,Hou X Y,Zhou X,Xin X P,Wright A,Jia ZJ.2015.p H regulates key players of nitrification in paddy soils.Soil Biol Biochem.81:9-16.
Kemmitt S J,Wright D,Goulding K W T,Jones D L.2006.pHregulation of carbon and nitrogen dynamics in two agricultural soils.Soil Biol Biochem.38:898-911.
Kits K D,Sedlacek C J,Lebedeva E V,Han P,Bulaev A,Pjevac P,Daebeler A,Romano S,Albertsen M,Stein L Y,Daims H,Wagner M.2017.Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle.Nature.549:269-272.
K¨onneke M,Bernhard A E,De La Torre J R,Walker C B,Waterbury J B,Stahl D A.2005.Isolation of an autotrophic ammonia-oxidizing marine archaeon.Nature.437:543-546.
Kumar S,Stecher G,Tamura K.2016.MEGA7:Molecular evolutionary genetics analysis version 7.0 for bigger datasets.Mol Biol Evol.33:1870-1874.
Kurola J,Salkinoja-Salonen M,Aarnio T,Hultman J,Romantschuk M.2005.Activity,diversity and population size of ammonia-oxidising bacteria in oil-contaminated landfarming soil.FEMS Microbiol Lett.250:33-38.
Lehtovirta-Morley L E,Stoecker K,Vilcinskas A,Prosser JI,Nicol G W.2011.Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil.Proc Natl Acad Sci USA.108:15892-15897.
Li Y Y,Chapman S J,Nicol G W,Yao H Y.2018.Nitrification and nitrifiers in acidic soils.Soil Biol Biochem.116:290-301.
Lu L,Han W Y,Zhang J B,Wu Y C,Wang B Z,Lin X G,Zhu J G,Cai Z C,Jia Z J.2012.Nitrification of archaeal ammonia oxidizers in acid soils is supported by hydrolysis of urea.ISME J.6:1978-1984.
Lueders T,Manefield M,Friedrich M W.2004.Enhanced sensitivity of DNA-and r RNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients.Environ Microbiol.6:73-78.
Martens-Habbena W,Berube P M,Urakawa H,De La Torre JR,Stahl D A.2009.Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria.Nature.461:976-979.
Neufeld J D,Vohra J,Dumont M G,Lueders T,Manefield M,Friedrich M W,Murrell J C.2007.DNA stable-isotope probing.Nat Protoc.2:860-866.
Pratscher J,Dumont M G,Conrad R.2011.Ammonia oxidation coupled to CO2 fixation by archaea and bacteria in an agricultural soil.Proc Natl Acad Sci USA.108:4170-4175.
Prosser J I.1989.Autotrophic nitrification in bacteria.In Rose A H,Tempest D W(eds.)Advances in Microbial Physiology.Volume 30.Academic Press,London.pp.125-181.
Prosser J I.2010.Soil nitrifiers and nitrification.In Ward B B,Arp D J,Klotz M G(eds.)Nitrification.American Society for Microbiology Press,Washington D.C.pp.347-381.
Rotthauwe J H,Witzel K P,Liesack W.1997.The ammonia monooxygenase structural gene amoA as a functional marker:Molecular fine-scale analysis of natural ammonia-oxidizing populations.Appl Environ Microbiol.63:4704-4712.
Saitou N,Nei M.1987.The neighbor-joining method:A new method for reconstructing phylogenetic trees.Mol Biol Evol.4:406-425.
Schloss P D,Westcott S L,Ryabin T,Hall J R,Hartmann M,Hollister E B,Lesniewski R A,Oakley B B,Parks D H,Robinson C J.2009.Introducing mothur:Open-source,platformindependent,community-supported software for describing and comparing microbial communities.Appl Environ Microbiol.75:7537-7541.
Shen J P,Zhang L M,Zhu Y G,Zhang J B,He J Z.2008.Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam.Environ Microbiol.10:1601-1611.
Shen X Y,Zhang L M,Shen J P,Li L H,Yuan C L,He JZ.2011.Nitrogen loading levels affect abundance and composition of soil ammonia oxidizing prokaryotes in semiarid temperate grassland.J Soil Sediment.11:1243.
Stopniˇsek N,Gubry-Rangin C,H¨offerleˇS,Nicol G W,MandiˇcMulec I,Prosser J I.2010.Thaumarchaeal ammonia oxidation in an acidic forest peat soil is not influenced by ammonium amendment.Appl Environ Microbiol.76:7626-7634.
Tourna M,Stieglmeier M,Spang A,K¨onneke M,Schintlmeister A,Urich T,Engel M,Schloter M,Wagner M,Richter A,Schleper C.2011.Nitrososphaera viennensis,an ammonia oxidizing archaeon from soil.Proc Natl Acad Sci USA.108:8420-8425.
Treusch A H,Leininger S,Kletzin A,Schuster S C,Klenk H P,Schleper C.2005.Novel genes for nitrite reductase and amorelated proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling.Environ Microbiol.7:1985-1995.
Venter J C,Remington K,Heidelberg J F,Halpern A L,Rusch D,Eisen J A,Wu D Y,Paulsen I,Nelson K E,Nelson W,Fouts D E,Levy S,Knap A H,Lomas M W,Nealson K,White O,Peterson J,Hoffman J,Parsons R,Baden-Tillson H,Pfannkoch C,Rogers Y H,Smith H O.2004.Environmental genome shotgun sequencing of the Sargasso Sea.Science.304:66-74.
Wertz S,Leigh A K K,Grayston S J.2012.Effects of long-term fertilization of forest soils on potential nitrification and on the abundance and community structure of ammonia oxidizers and nitrite oxidizers.FEMS Microbiol Ecol.79:142-154.
Xi R J,Long X E,Huang S,Yao H Y.2017.pH rather than nitrification and urease inhibitors determines the community of ammonia oxidizers in a vegetable soil.AMB Express.7:129.
Xia W W,Zhang C X,Zeng X W,Feng Y Z,Weng J H,Lin XG,Zhu J G,Xiong Z Q,Xu J,Cai Z C,Jia Z J.2011.Autotrophic growth of nitrifying community in an agricultural soil.ISME J.5:1226-1236.
Xiao K C,Xu J M,Tang C X,Zhang J B,Brookes P C.2013.Differences in carbon and nitrogen mineralization in soils of differing initial pH induced by electrokinesis and receiving crop residue amendments.Soil Biol Biochem.67:70-84.
Yao H Y,Gao Y M,Nicol G W,Campbell C D,Prosser J I,Zhang L M,Han W Y,Singh B K.2011.Links between ammonia oxidizer community structure,abundance,and nitrification potential in acidic soils.Appl Environ Microbiol.77:4618-4625.
Ye C,Cheng X L,Zhang Y L,Wang Z X,Zhang Q F.2012.Soil nitrogen dynamics following short-term revegetation in the water level fluctuation zone of the Three Gorges Reservoir,China.Ecol Eng.38:37-44.
Zhang L M,Hu H W,Shen J P,He J Z.2012.Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils.ISMEJ.6:1032-1045.
Zhang M M,Alves R J E,Zhang D D,Han L L,He J Z,Zhang LM.2017.Time-dependent shifts in populations and activity of bacterial and archaeal ammonia oxidizers in response to liming in acidic soils.Soil Biol Biochem.112:77-89.
Zhou X,Fornara D,Wasson E A,Wang D M,Ren G D,Christie P,Jia Z J.2015.Effects of 44 years of chronic nitrogen fertilization on the soil nitrifying community of permanent grassland.Soil Biol Biochem.91:76-83.