Impact of Long-Term Fertilization on Community Structure of Ammonia Oxidizing and Denitrifying Bacteria Based on amoA and nirK Genes in a Rice Paddy from Tai Lake Region, China

doi:10.1016/S2095-3119(14)60784-X

Journal of Integrative Agriculture ›› 2014, Vol. 13 ›› Issue (10): 2286-2298.DOI: 10.1016/S2095-3119(14)60784-X

Impact of Long-Term Fertilization on Community Structure of Ammonia Oxidizing and Denitrifying Bacteria Based on amoA and nirK Genes in a Rice Paddy from Tai Lake Region, China

JIN Zhen-jiang, LI Lian-qing, LIU Xiao-yu, PAN Gen-xing, Qaiser Hussein , LIU Yong-zhuo

1、Institute of Resource, Ecosystem and Environment of Agriculture, Nanjing Agricultural University, Nanjing 210095, P.R.China
2、Guilin University of Technology, Guilin 541004, P.R.China

收稿日期:2013-12-25 出版日期:2014-10-01 发布日期:2014-10-10
通讯作者: PAN Gen-xing, Tel: +86-25-84398657, E-mail: pangenxing@aliyun.com
作者简介:JIN Zhen-jiang, E-mail: zhenjiangjinjin@163.com
基金资助:
This work was supported by the National Natural Science Foundation of China (40830528 and 40710019002).

Impact of Long-Term Fertilization on Community Structure of Ammonia Oxidizing and Denitrifying Bacteria Based on amoA and nirK Genes in a Rice Paddy from Tai Lake Region, China

JIN Zhen-jiang, LI Lian-qing, LIU Xiao-yu, PAN Gen-xing, Qaiser Hussein , LIU Yong-zhuo

1、Institute of Resource, Ecosystem and Environment of Agriculture, Nanjing Agricultural University, Nanjing 210095, P.R.China
2、Guilin University of Technology, Guilin 541004, P.R.China

Received:2013-12-25 Online:2014-10-01 Published:2014-10-10
Contact: PAN Gen-xing, Tel: +86-25-84398657, E-mail: pangenxing@aliyun.com
About author:JIN Zhen-jiang, E-mail: zhenjiangjinjin@163.com
Supported by:
This work was supported by the National Natural Science Foundation of China (40830528 and 40710019002).

摘要/Abstract

摘要： Ammonia oxidizing (AOB) and denitrifying bacteria (DNB) play an important role in soil nitrogen transformation in natural and agricultural ecosystems. Effects of long-term fertilization on abundance and community composition of AOB and DNB were studied with targeting ammonia monooxygenase (amoA) and nitrite reductase (nirK) genes using polymerase chain reactiondenaturing gradient gel electrophoresis (PCR-DGGE) and real-time PCR, respectively. A field trial with different fertilization treatments in a rice paddy from Tai Lake region, centre East China was used in this study, including no fertilizer application (NF), balanced chemical fertilizers (CF), combined organic/inorganic fertilizer of balanced chemical fertilizers plus pig manure (CFM), and plus rice straw return (CFS). The abundances and richnesses of amoA and nirK were increased in CF, CFM and CFS compared to NF. Principle component analysis of DGGE profiles showed significant difference in nirK and amoA genes composition between organic amended (CFS and CFM) and the non-organic amended (CF and NF) plots. Number of amoA copies was significantly positively correlated with normalized soil nutrient richness (NSNR) of soil organic carbon (SOC) and total nitrogen (T-N), and that of nirK copies was with NSNR of SOC, T-N plus total phosphorus. Moreover, nitrification potential showed a positive correlation with SOC content, while a significantly lower denitrification potential was found under CFM compared to under CFS. Therefore, SOC accumulation accompanied with soil nutrient richness under long-term balanced and organic/inorganic combined fertilization promoted abundance and diversity of AOB and DNB in the rice paddy.

关键词: long-term fertilization , ammonia oxidizing bacteria , denitrifying bacteria , abundance , rice paddy

Abstract: Ammonia oxidizing (AOB) and denitrifying bacteria (DNB) play an important role in soil nitrogen transformation in natural and agricultural ecosystems. Effects of long-term fertilization on abundance and community composition of AOB and DNB were studied with targeting ammonia monooxygenase (amoA) and nitrite reductase (nirK) genes using polymerase chain reactiondenaturing gradient gel electrophoresis (PCR-DGGE) and real-time PCR, respectively. A field trial with different fertilization treatments in a rice paddy from Tai Lake region, centre East China was used in this study, including no fertilizer application (NF), balanced chemical fertilizers (CF), combined organic/inorganic fertilizer of balanced chemical fertilizers plus pig manure (CFM), and plus rice straw return (CFS). The abundances and richnesses of amoA and nirK were increased in CF, CFM and CFS compared to NF. Principle component analysis of DGGE profiles showed significant difference in nirK and amoA genes composition between organic amended (CFS and CFM) and the non-organic amended (CF and NF) plots. Number of amoA copies was significantly positively correlated with normalized soil nutrient richness (NSNR) of soil organic carbon (SOC) and total nitrogen (T-N), and that of nirK copies was with NSNR of SOC, T-N plus total phosphorus. Moreover, nitrification potential showed a positive correlation with SOC content, while a significantly lower denitrification potential was found under CFM compared to under CFS. Therefore, SOC accumulation accompanied with soil nutrient richness under long-term balanced and organic/inorganic combined fertilization promoted abundance and diversity of AOB and DNB in the rice paddy.

Key words: long-term fertilization , ammonia oxidizing bacteria , denitrifying bacteria , abundance , rice paddy

JIN Zhen-jiang, LI Lian-qing, LIU Xiao-yu, PAN Gen-xing, Qaiser Hussein , LIU Yong-zhuo. Impact of Long-Term Fertilization on Community Structure of Ammonia Oxidizing and Denitrifying Bacteria Based on amoA and nirK Genes in a Rice Paddy from Tai Lake Region, China[J]. Journal of Integrative Agriculture, 2014, 13(10): 2286-2298.

参考文献

Alden L, Demoling F, Baath E. 2001. Rapid method ofdetermining factors limiting bacterial growth in soil.Applied and Environmental Microbiology, 67, 1830-1838

Aulakh M S, Khera T S, Doran J W, Bronson K F. 2001.Denitrification, N2O and CO2 fluxes in rice-wheat croppingsystem as affected by crop residues, fertilizer N and legumegreen manure. Biology and Fertility of Soils, 34, 375-389

Avrahami S, Conrad R. 2003. Patterns of community changeamong ammonia oxidizers in meadow soils upon longtermincubation at different temperatures. Applied andEnvironmental Microbiology, 10, 6152-6164

Avrahami S, Conrad R, Braker G. 2002. Effect of soilammonium concentration on N2O release and on thecommunity structure of ammonia oxidizers and denitrifiers.Applied and Environmental Microbiology, 68, 5685-5692

Barnard R, Leadley P W. 2005. Global change, nitrification,and denitrification: A review. Global BiogeochemicalCycles, 19, GB1007, doi: 10.1029/2004GB002282

Bárta J, Melichová T, Van?k Daniel, Picek T. Šantr??kováH. 2010. Effect of pH and dissolved organic matter on theabundance of nirK and nirS denitrifiers in spruce forestsoil. Biogeochemistry, 101, 123-132

Belser L W. 1979. Population ecology of nitrifying bacteria.Annual Review of Microbiology, 33, 309-333

Cai Y F, Peng C, Zhao S Q, Cai A H, Li Y T. 2012. Balancedfertilization improved soil ammonia-oxidizing bacterialcommunity in latosolic red soil. Acta AgriculturaeScandinavica (Section B, Soil & Plant Science), 62, 531-540

Chen Z, Luo X Q, Hu R G, Wu M N, Wu J S, Wei W X. 2010.Impact of long-term fertilization on the composition ofdenitrifier communities based on nitrite reductase analysesin a paddy soil. Microbial Ecology, 60, 850-861

Chen Z, Yuan H Z, Wu J S, Wei W X. 2009. Activity andcomposition of the denitrifying bacterial communityrespond differently to long-term fertilization. ActaEcologica Sinica, 29, 5923-5929 (in Chinese)

Chu H Y, Fujii T, Morimoto S, Lin X G, Yagi K, Hu J L, ZhangJ B. 2007. Community structure of ammonia-oxidizingbacteria under long-term application of mineral fertilizerand organic manure in a sandy loam soil. Applied andEnvironmental Microbiology, 73, 485-491

Cruz A F, Hame C, Hanson K, Selles F, Zentner R P. 2009.Thirty-seven years of soil nitrogen and phosphorus fertilitymanagement shapes the structure and function of the soil microbial community in a Brown Chernozem. Plant andSoil, 315, 173-184

David T, David W, Johanner K. 1996. Productivity andsustainability influenced by biodiversity in grasslandecosystems. Nature, 379, 718-720

Dick R P. 1992. A review: long-term effects of agriculturalsystems on soil biochemical and microbial parameters.Agriculture, Ecosystems and Environment, 40, 25-36

Enwall K, Nyberg K, Bertilsson S, Cederlund H, StenströmJohn, Hallin S. 2007. Long-term impact of fertilizationon activity and composition of bacterial communitiesand metabolic guilds in agricultural soil. Soil Biology &Biochemistry, 39, 106-115

Enwall K, Philippot L, Hallin S. 2005. Activity andcomposition of the denitrifying bacterial communityrespond differently to long-term fertilization. Applied andEnvironmental Microbiology, 71, 8335-8343

Fan F L, Yang Q B, Li Z J, Wei D, Cui X A, Liang Y C. 2011.Impacts of organic and inorganic fertilizers on nitrificationin a cold climate soil are linked to the bacterial ammoniaoxidizer community. Microbial Ecology, 62, 982-990

Gong Z T. 1999. Chinese Soil Taxonomy, Theory Approachesand Application. Science Press, Beijing. pp. 160-165

(inChinese)He J Z, Hu H W, Zhang L M. 2012. Current insights into theautotrophic thaumarchaeal ammonia oxidation in acidicsoils. Soil Biology & Biochemistry, 55, 146-154

He J Z, Shen J P, Zhang L M, Zhu Y G, Zheng Y M, Xu MM, Di H J. 2007. Quantitative analyses of the abundanceand composition of ammonia-oxidizing bacteria andammonia-oxidizing archaea of a Chinese upland red soilunder long-term fertilization practices. EnvironmentalMicrobiology, 9, 2364-2374

Henry S, Baudoin E, López-Gutiérrez J C, Martin-LaurentF, Brauman A, Philippot L. 2004. Quantification ofdenitrifying bacteria in soils by nirK gene targeted realtimePCR. Journal of Microbiological Methods, 59,327-335

Jin Z J, Pan G X, Liu X Y, Li L Q. 2013. Community structurecharacters and differences of N2-fixing and CO2-fixingbacteria under long-term fertilization in paddy soils ofTailake region, China. Acta Metallurgica Sinica, 19, 86-96 (in Chinese)

Kandeler E, Deiglmayr K, Tscherko D, Bru D, Philippot L.2006. Abundance of narG, nirS, nirK, and nosZ genesof denitrifying bacteria during primary successions of aglacier foreland. Applied and Environmental Microbiology,72, 5957-5962

Kleineidam K, Sharma S, Kotzerke A, Heuer H, Thiele-BruhnS, Smalla K, Wilke B-M, Schloter M. 2010. Effect ofsulfadiazine on abundance and diversity of denitrifyingbacteria by determining nirK and nirS genes in two arablesoils. FEMS Microbiology Ecology, 60, 703-707

Kong A Y Y, Hristova K, Scow K M, Six J. 2010. Impacts ofdifferent N management regimes on nitrifier and denitrifiercommunities and N cycling in soil microenvironments. SoilBiology & Biochemistry, 42, 1523-1533

Li Y L, Zhang Y L, Hu J, Shen Q R. 2007. Contribution ofnitrification happened in rhizospheric soil growing withdifferent rice cultivars to N nutrition. Biology and Fertilityof Soils, 43, 417-425

Liu D W, Liu X Y, Li L Q, Pan G X, David C, TippkötterR. 2011. SOC accumulation in paddy soils under longtermagro-ecosystem experiments from South China. VI.Changes in microbial community structure and respiratoryactivity. Biogeosciences Discuss, 8, 1529-1554

Maeda K, Morioka R, Hanajima D, Osada T. 2010. The impactof using mature compost on nitrous oxide emission andthe denitrifier community in the cattle manure compostingprocess. FEMS Microbiology Ecology, 59, 25-36

Miller M N, Zebarth B J, Dandie C E, Burton D L, Goyera C,Trevors J T. 2008. Crop residue influence on denitrification,N2O emissions and denitrifier community abundance insoil. Soil Biology & Biochemistry, 40, 2553-2562

Muyzer G, Brinkhoff T, Nübel U, Santegoeds C, Schafer H,Wawer C. 1997. Denaturing gradient gel electrophoresis(DGGE) in microbial ecology. In: Akkermans A D L,van Elsas J D, de Bruijn F J, eds., Molecular MicrobialEcology Manual. Kluwer Academic Publishers, Dordrecht,The Netherlands. p. 1-27

Okano Y, Hristova K R, Leutenegger C M, Jackson L E,Denison R F, Gebreyesus B, Lebauer D, Scow K M.2004. Application of real-time PCR to study effects ofammonium on population size of ammonia-oxidizingbacteria in soil. Applied and Environmental Microbiology,70, 1008-1016

Pan G X, Li L Q, Wu L S, Zhang X H. 2003. Storage andsequestration potential of topsoil organic carbon in China‘spaddy soils. Global Change Biology, 10, 79-92

Pan G X, Smith P, Pan W N. 2009a. The role of soil organicmatter in maintaining the productivity and yield stability ofcereals in china. Agriculture Ecosystems and Environment,129, 344-348

Pan G X, Zhou P, Li Z P, Smith P, Li L Q, Qiu D S, Zhang X H,Xu X B, Shen S Y, Chen X M. 2009b. Combined inorganic/organic fertilization enhances N efficiency and increasesrice productivity through organic carbon accumulation ina rice paddy from the Tai Lake region, China. Agriculture,Ecosystem and Environment, 131, 274-280

Phillips C J, Harris D, Dollhopf S L, Gross K L, Prosser JI, Eldor A P. 2000. Effects of agronomic treatments onstructure and function of ammonia-oxidizing communities.Applied and Environmental Microbiology, 66, 5410-5418

Rotthauwe J H, Witzel K P, Liesack W. 1997. The ammoniamonooxygenase structural gene amoA as a functionalmarker, molecular fine scale analysis of natural ammoniaoxidizingpopulations. Applied and EnvironmentalMicrobiology, 63, 4704-4712

Schmidt I. 2009. Chemoorganoheterotrophic growth ofNitrosomonas europaea and Nitrosomonas eutropha.Current Microbiology, 59, 130-138

Schmidt M W I, Torn M S, Abiven S, Dittmar T, Guggenberger G, Janssens I A, Kleber M, Kögel-Knabner I, LehmannJ, Manning D A C, Nannipieri P, Rasse D P, Weiner S,Trumbore S E. 2011. Persistence of soil organic matter asan ecosystem property. Nature, 478, 49-56

Soil Survey Staff, USDA. 1994. Keys to Soil Taxonomy.6th ed. United States Department of Agriculture, SoilConservation Service, USA. pp. 161-186

Sooksa-Nguan T, Thies J E, Gypmantasiri P, Boonkerd N,Teaumroong N. 2009. Effect of rice cultivation systemson nitrogen cycling and nitrifying bacterial communitystructure. Applied Soil Ecology, 43, 139-149

Szukics U, Hackl E, Zechmeister-Boltenstern S, Sessitsch A.2009. Contrasting response of two forest soils to nitrogeninput, rapidly altered NO and N2O emissions and nirKabundance. Biology and Fertilizer of Soils, 45, 855-863

Throbäck I N, Enwall K, Jarwis A, Hallin S. 2004. ReassessingPCR primers targeting nirS, nirK and nosZ genes forcommunity surveys of denitrifying bacteria with DGGE.FEMS Microbiology Ecology, 49, 401-417

Vanderheijden M G A, John N K, Ursic M, Moutoglis P,Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR. 1998. Mycorrhizal fungal diversity determines plantbiodiversity, ecosystem variability and productivity.Nature, 396, 69-72

Wallenstein M D, Myrold D D, Firestone M, Voytek M. 2006.Environmental controls on denitrifying communities anddenirtrification rate, insight from molecular methods.Ecological Applications, 16, 2143-2152

Wang C J, Pan G X, Tian Y G, Li L Q, Zhang X H, Han XJ. 2010. Changes in cropland topsoil organic carbon withdifferent fertilizations under long-term agro-ecosystemexperiments across mainland China. Science China (LifeSciences), 53, 858-867

Wang S X, Liang X Q, Luo Q X，Fan F, Chen Y X, Li Z Z,Sun H X, Dai T F, Wan J N, Li X J. 2012. Fertilizationincreases paddy soil organic carbon density. Journalof Zhejiang University-SCIENCE B (Biomedicine &Biotechnology), 13, 274-282

Wang Y N, Ke X B, Wu L Q, Lu Y H. 2009. Communitycomposition of ammonia-oxidizing bacteria and archaeain rice field soil as affected by nitrogen fertilization.Systematic and Applied Microbiology, 32, 27-36

Wessén E, Nybergb K, Janssonc J K, Hallina S. 2010.Responses of bacterial and archaeal ammonia oxidizersto soil organic and fertilizer amendments under long-termmanagement. Applied Soil Ecology, 45, 193-200

Wu J S. 2011. Carbon accumulation in paddy ecosystemsin subtropical China, evidence from landscape studies.European Journal of Soil Science, 62, 29-34

Xu X B, Xu X D, Chu Q H, Qiu D S. 1999. Influence ofdifferent fertilizations in crop yield and soil fertility. In:Soil Science Society of Jiangsu, ed., Soil Science andTechnology of Jiangsu Facing the 21th Century. HohaiUniversity Press, Nanjing. pp. 107-110 (in Chinese)

Yu Z N, Li F D, He S J. 1996. Experiment And Techniqueof Agricultural Microbiology. China Agriculture Press,Beijing. pp. 125-126 (in Chinese)

Zhang P J, Li L Q, Pan G X, Zhang J W. 2004. Influence oflong- term fertilizer management on topsoil microbialbiomass and genetic diversity of a paddy soil from theTai Lake region, China. Acta Ecologica Sinica, 24, 2818-2824 (in Chinese)

Zhang P J, Zheng J F, Pan G X, Zhang X H, Li L Q, TippkötterR. 2007. Changes in microbial community structure andfunction with in particle size fractions of a paddy soilunder different long-term fertilization treatments fromthe Tai Lake region, China. Colloids and Surfaces B:Biointerfaces, 58, 264-270

Zhang W J, Xu M G, Wang X J, Huang Q H, Nie J, Li Z Z,Li S L, Hwang S W, Lee K B. 2012. Effects of organicamendments on soil carbon sequestration in paddy fieldsof subtropical China. Journal of Soils and Sediments, 12,457-470

Zheng J F, Zhang P J, Pan G X, Li L Q, Zhang X H. 2008.Effect of long-term different fertilization on methaneoxidation potential and diversity of methanotrophs ofpaddy soil. Acta Ecologica Sinica, 28, 4864-4872 (inChinese)

Zhong W H, Cai Z C, Yin L C, Zhang H. 2007. The effectsof the long-term application of inorganic fertilizers onmicrobial community diversity in rice-planting red soilas studied by PCR-DGGE. Acta Ecologica Sinica, 27,4011-4018 (in Chinese)

[1]	MIAO Hui-tian, Lü Jia-long, XU Ming-gang, ZHANG Wen-ju, HUANG Shao-min, PENG Chang, CHEN Li-ming. Carbon and nitrogen allocations in corn grown in Central and Northeast China: different responses to fertilization treatments[J]. Journal of Integrative Agriculture, 2015, 14(6): 1212-1221.
[2]	FAN Hong-zhu, CHEN Qing-rui, QIN Yu-sheng, CHEN Kun, TU Shi-hua, XU Ming-gang, ZHANG Wen-ju. Soil carbon sequestration under long-term rice-based cropping systems of purple soil in Southwest China[J]. Journal of Integrative Agriculture, 2015, 14(12): 2417-2425.
[3]	SHI Lin-lin, SHEN Ming-xing, LU Chang-yin, WANG Hai-hou, ZHOU Xin-wei, JIN Mei-juan, WU Tong-dong. Soil phosphorus dynamic, balance and critical P values in longterm fertilization experiment in Taihu Lake region, China[J]. Journal of Integrative Agriculture, 2015, 14(12): 2446-2455.
[4]	ZHA Yan, WU Xue-ping, GONG Fu-fei, XU Ming-gang, ZHANG Hui-min, CHEN Li-ming, HUANG Shao-min, CAI Dian-xiong. Long-term organic and inorganic fertilizations enhanced basic soil productivity in a fluvo-aquic soil[J]. Journal of Integrative Agriculture, 2015, 14(12): 2477-2489.
[5]	LI Juan, LI Yan-ting, YANG Xiang-dong, ZHANG Jian-jun, LIN Zhi-an, ZHAO Bing-qiang . Microbial community structure and functional metabolic diversity are associated with organic carbon availability in an agricultural soil[J]. Journal of Integrative Agriculture, 2015, 14(12): 2500-2511.
[6]	LIU Song-zhong, ZHANG Qiang, LIU Jun, SUN Jian , WEI Qin-ping. Effect of Partial Root-Zone Irrigating Deuterium Oxide on the Properties of Water Transportation and Distribution in Young Apple Trees[J]. Journal of Integrative Agriculture, 2014, 13(6): 1268-1275.
[7]	XU Yong-mei, LIU Hua, WANG Xi-he, XU Ming-gang, ZHANG Wen-ju , JIANG Gui-ying. Changes in Organic Carbon Index of Grey Desert Soil in Northwest China After Long-Term Fertilization[J]. Journal of Integrative Agriculture, 2014, 13(3): 554-561.
[8]	ZHA Yan, WU Xue-ping , HE Xin-hua, ZHANG Hui-min, GONG Fu-fei, CAI Dian-xiong, ZHU. Basic Soil Productivity of Spring Maize in Black Soil Under Long-Term Fertilization Based on DSSAT Model[J]. Journal of Integrative Agriculture, 2014, 13(3): 577-587.
[9]	SHEN Pu, HE Xin-hua, XU Ming-gang, ZHANG Hui-min, PENG Chang, GAO Hong-jun, LIU. Soil Organic Carbon Accumulation Increases Percentage of Soil Olsen-P to Total P at Two 15-Year Mono-Cropping Systems in Northern China[J]. Journal of Integrative Agriculture, 2014, 13(3): 597-603.
[10]	CHAI Yan-jun, ZENG Xi-bai, E Sheng-zhe, HUANG Tao, CHE Zong-xian, SU Shi-ming , BAI Ling-yu. Response of Soil Organic Carbon and Its Aggregate Fractions to Long- Term Fertilization in Irrigated Desert Soil of China[J]. Journal of Integrative Agriculture, 2014, 13(12): 2758-2767.
[11]	LIN Ying-hua, LU Ping, YANG Xue-yun , ZHANG Fu-dao. Soil Insect Diversity and Abundance Following Different Fertilizer Treatments on the Loess Plateau of China[J]. Journal of Integrative Agriculture, 2013, 12(9): 1644-1651.
[12]	Muhammad A R F Sultan, LIU Hui, CHENG Yu-Feng, ZHANG Pei-pei , ZHAO Hui-xian. Combining Phytate/Ca2+ Fractionation with Trichloroacetic Acid/Acetone Precipitation Improved Separation of Low-Abundant Proteins of Wheat (Triticum aestivum L.) Leaf for Proteomic Analysis[J]. Journal of Integrative Agriculture, 2013, 12(7): 1123-1129.
[13]	MENG Hong-qi, XU Ming-gang, Lü Jia-long, HE Xin-hua, LI Jian-wei, SHI Xiao-jun, PENG. Soil pH Dynamics and Nitrogen Transformations Under Long-Term Chemical Fertilization in Four Typical Chinese Croplands[J]. Journal of Integrative Agriculture, 2013, 12(11): 2092-2102.

Impact of Long-Term Fertilization on Community Structure of Ammonia Oxidizing and Denitrifying Bacteria Based on amoA and nirK Genes in a Rice Paddy from Tai Lake Region, China

Impact of Long-Term Fertilization on Community Structure of Ammonia Oxidizing and Denitrifying Bacteria Based on amoA and nirK Genes in a Rice Paddy from Tai Lake Region, China

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 13

编辑推荐

Metrics