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| Responses of N2O reductase gene (nosZ)-denitrifier communities to long-term fertilization follow a depth pattern in calcareous purplish paddy soil |
| WANG Ying-yan1, LU Sheng-e1, XIANG Quan-ju1, YU Xiu-mei1, ZHAO Ke1, ZHANG Xiao-ping1, TU Shi-hua2, GU Yun-fu1 |
1 Department of Microbiology, College of Resource, Sichuan Agricultural University, Chengdu 611130, P.R.China
2 Soil and Fertilizer Institute, Sichuan Academy of Agricultural Sciences, Chengdu 610066, P.R.China |
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Abstract The effect of long-term fertilization on soil denitrifying communities was analysed by measuring the abundance and diversity of the nitrous oxide (N2O) reductase gene, nosZ. Soil samples were collected from plots of a long-term fertilization experiment established in 1982 in Suining City, China. The fertilizer treatments were no fertilizer (CK), three chemical fertilizer (CF) treatments (N, NP, NPK), manure (M) alone, and manure with chemical fertilizers (NM, NPM, NPKM). The abundance and diversity of the denitrifying bacteria were assessed by real-time quantitative PCR, terminal restriction fragment length polymorphism (T-RFLP), and cloning and sequencing of nosZ genes. The diversity and abundance of nosZ-denitrifiers was higher in soil amended with manure and chemical fertilizers (CFM) than in soil amended with CF alone, and the highest in topsoil (0–20 cm). The nosZ-denitrifier community composition was more complex in CFM soil than in CF soil. Specific species were detected only in the CFM soil. The abundance of nosZ-denitrifier in the NPKM treatment was approximately two times higher than that in the CK, N, and NPK treatments. Most of the cloned nosZ sequences were closely related to nosZ sequences from Bradyrhizobiaceae and Rhodospirillaceae in Alphaproteobacteria. Of the measured abiotic factors, soil organic matter correlated significantly with the abundance (P<0.01); available phosphorus correlated significantly with the topsoil community composition (P<0.01), whereas soil organic matter correlated significantly with the subsoil (20–90 cm) community composition (P<0.01). This study demonstrated that long-term CFM fertilization affected both the abundance and composition of the nosZ-denitrifier community.
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Received: 18 January 2017
Accepted:
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| Fund: The study was funded by the National Natural Science Foundation of China (41201256). |
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Corresponding Authors:
Correspondence GU Yun-fu, Tel: +86-28-86920982, E-mail: gungyf@163.com
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| About author: WANG Ying-yan, Mobie: +86-13550865352, E-mail: 398766403@qq.com |
Cite this article:
WANG Ying-yan, LU Sheng-e, XIANG Quan-ju, YU Xiu-mei, ZHAO Ke, ZHANG Xiao-ping, TU Shihua, GU Yun-fu.
2017.
Responses of N2O reductase gene (nosZ)-denitrifier communities to long-term fertilization follow a depth pattern in calcareous purplish paddy soil. Journal of Integrative Agriculture, 16(11): 2597-2611.
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| Atlas R M, Bartha R. 1987. Microbial Ecology: Fundamentals and Applications. 2nd ed. Benjamin Cummings Publishing Co., Menlo Park.Aulakh M S, Rennie D A, Paul E A. 1983. The effect of various clover management practices on gaseous N losses and mineral N accumulation. Canadian Journal of Soil Science, 63, 593–605.Bossio D A, Scow K M, Gunapala N, Graham K J. 1998. Determinants of soil microbial communities: Effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microbial Ecology, 36, 1–12.Boz B, Rahman M M, Bottegal M, Basaglia M, Squartini A, Gumiero B, Casella S. 2013. Vegetation, soil and hydrology management influence denitrification activity and the composition of nirK-type denitrifier communities in a newly afforested riparian buffer. New Biotechnology, 30, 675–684.Campbell B J, Polson S W, Hanson T E, Mack M C, Schuur E A. 2010. The effect of nutrient deposition on bacterial communities in arctic tundra soil. Environmental Microbiology, 12, 1842–1854. Chen Z, Hou H J, Zheng Y, Qin H L, Zhu Y J, Wu J S, Wei W X. 2012. Influence of fertilisation regimes on a nosZ-containing denitrifying community in a rice paddy soil. Journal of the Science of Food & Agriculture, 92, 1064–1072.Chèneby D, Brauman A, Rabary B, Philippot L. 2009. Differential responses of nitrate reducer community size, structure, and activity to tillage systems. Applied and Environmental Microbiology, 75, 3180–3186.Coats V C, Pelletreau K N, Rumpho M E. 2014. Amplicon pyrosequencing reveals the soil microbial diversity associated with invasive Japanese barberry (Berberis thunbergii DC.). Molecular Ecology, 23, 1318–1332.?uhel J, Šimek M, Laughlin R J, Bru D, Chèneby D, Watson C J, Philippot L. 2010. Insights into the effect of soil pH on N2O and N2 emissions and denitrifier community size and activity. Applied and Environmental Microbiology, 76, 1870–1878. Dambreville C, Hallet S, Nguyen C, Morvan T, Germon J C, Philippot L. 2006a. Structure and activity of the denitrifying community in a maize-cropped field fertilized with composted pig manure or ammonium nitrate. FEMS Microbiology Ecology, 56, 119–131.Dambreville C, Hénault C, Bizouard F, Morvan T, Chaussod R, Germon J C. 2006b. Compared effects of long-term pig slurry applications and mineral fertilization on soil denitrification and its end products (N2O, N2). Biology and Fertility of Soils, 42, 490–500.Deslippe J R, Jamali H, Jha N, Saggar S. 2014. Denitrifier community size, structure and activity along a gradient of pasture to riparian soils. Soil Biology and Biochemistry, 71, 48–60.Donnell A O O, Melanie S, Andrew M, Ian W, John T D. 2001. Plants and fertilizers as drivers of change in microbial community structure and function in soils. Plant and Soil, 232, 135–145.Enwall K, Hallin S. 2009. Comparison of T-RFLP and DGGE techniques to assess denitri?er community composition in soil. Letters in Applied Microbiology, 48, 145–148.Enwall K, Philippot L, Hallin S. 2005. Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Applied and Environmental Microbiology, 71, 8335–8343.Fan T L, Stewart B A, Wang Y, Lou J J, Zhou G Y. 2005. Long-term fertilization effects on grain yield, water-use efficiency and soil fertility in the dry land of Loess Plateau in China. Agriculture Ecosystems & Environment, 106, 313–329.FAO. 2003. Selected Indicators of Food and Agriculture Development in Asia-Pacific Region (1992–2002). RAP Publication. pp. 23–24.Fierer N, Schimel J P, Holden P A. 2003. Variations in microbial community composition through two soil depth profiles. Soil Biology & Biochemistry, 35, 167–176.Finlay J C, Small G E, Sterner R W. 2013. Human influences on nitrogen removal in lakes. Science, 342, 247–250.Franke-Whittle I H, Klammer S H, Insam H. 2005. Design and application of an oligonucleotide microarray for the investigation of compost microbial communities. Journal of Microbiology Methods, 62, 37–56.Gans J, Wolinsky M, Dunbar J. 2005. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science, 309, 1387–1390.García-Lledó A, Vilar-Sanz A, Trias R, Hallin S, Bañeras L. 2011. Genetic potential for N2O emissions from the sediment of a free water surface constructed wetland. Water Research, 45, 5621–5632.Gu Y F, Wang, Y Y, Xiang, Q J, Yu X M, Zhao K, Zhang X, Liu S Q. 2017. Implications of wetland degradation for the potential denitrifying activity and bacterial populations with nirS genes as found in a succession in Qinghai-Tibet Plateau, China. European Journal of Soil Biology, 80, 19–26.Gu Y F, Zhang X P, Tu S, Lindström K. 2009. Soil microbial biomass, crop yields, and bacterial community structure as affected by long-term fertilizer treatments under wheat-rice cropping. European Journal of Soil Biology, 45, 239–246.Guan D W, Li L, Jiang X, Ma M C, Cao F M, Zhou B K, Li J. 2015. Influence of long-term fertilization on the community structure and diversity of soybean rhizobia in black soil. Biodiversity Science, 23, 68–78. Guo G X, Deng H, Qiao M, Yao H Y, Zhu Y G. 2013. Effect of long-term wastewater irrigation on potential denitrification and denitrifying communities in soils at the watershed scale. Environmental Science & Technology, 47, 3105–3113.Hallin S, Jones C M, Schloter M, Philippot L. 2009. Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. The ISME Journal, 3, 597–605.Henry S, Baudoin E, Lopez-Gutierrez J C, Martin-Laurent F, Baumann A, Philippot L. 2004. Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. Journal of Microbiological Methods, 59, 327–335.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. Applied and Environmental Microbiology, 72, 5181–5189.Horn M A, Drake H L, Schramm A. 2006. Nitrous oxide reductase genes (nosZ) of denitrifying microbial populations in soil and the earthworm gut are phylogenetically similar. Applied and Environmental Microbiology, 72, 1019–1026.Ibekwe A M , Kennedy A C., Frohne P S, Papiernik S K, Yang C H, Crowley D E. 2002. Microbial diversity along a transect ofagronomic zones. FEMS Microbiology Ecology, 39, 183–191.Ishii S, Ikeda S, Minamisawa K, Senoo K. 2011. Nitrogen cycling in rice paddy environments: Past achievements and future challenges. Microbes and Environments, 26, 282–292.Jangid K, Williams M A, Franzluebbers A J, Sanderlin J S, Reeves J H, Jenkins M B, Whitman W B. 2008. Relative impacts of land-use, management intensity and fertilization upon soil microbial community structure in agricultural systems. Soil Biology and Biochemistry, 40, 2843–2853.Joa J H, Weon H Y, Hyun H N, Jeun Y C, Koh S W. 2014. Effect of long-term different fertilization on bacterial community structures and diversity in citrus orchard soil of volcanic ash. Journal of Microbiology, 12, 995–1001.Kastl E M, Schloter H B, Buegger F, Schloter M. 2015. Impact of fertilization on the abundance of nitrifiers and denitrifiers at the root-soil interface of plants with different uptake strategies for nitrogen. Biology and Fertility of Soils, 51, 57–64.Kitagawa W, Takami S, Miyauchi K, Masai E, Kamagata Y, Tiedje J M, Fukuda M. 2002. Novel 2,4-dichlorophenoxyacetic acid degradation genes from oligotrophic Bradyrhizobium sp. strain HW13 isolated from a pristine environment. Journal of Bacteriology, 184, 509–518.Kloos K, Mergel A, Rosch C, Bothe H. 2001. Denitri?cation within the genus Azospirillum and other associative bacteria. Australian Journal of Plant Physiology, 28, 991–998. Kuntal M H, Anand S, Mishra B, Manna M C, Wanjari R H, Mandal K G, Misra A K. 2008. Impact of long-term application of fertilizer, manure and lime under intensive cropping on physical properties and organic carbon content of an Alfisol. Geoderma, 148, 173–179.Li J, Wang G, Allison S D, Mayes M A, Luo Y. 2014. Soil carbon sensitivity to temperature and carbon use efficiency compared across microbial-ecosystem models of varying complexity. Biogeochemistry, 119, 67–84.Li Y, Simunek J, Zhang Z T, Jing L F, Ni L X. 2015. Evaluation of nitrogen balance in a direct-seeded-rice field experiment using Hydrus-1D. Agricultural Water Management, 148, 213–222.Liesack W, Schnell S, Revsbech N P. 2000. Microbiology of flooded rice paddies. FEMS Microbiology Reviews, 24, 625–645.Liu B, Frostegard A, Bakken L R. 2014. Impaired reduction of N2O to N2 in acid soils is due to a posttranscriptional interference with the expression of nosZ. mBio, 5, e01383-14.Liu X, Chen C R, Wang W J, Hughes J M, Lewis T, Hou E Q, Shen J P. 2015. Vertical distribution of soil denitrifying communities in a wet sclerophyll forest under long-term repeated buring. Microbial Ecology, 70, 993–1003. Lu R K. 2000.The Methods of Agriculture Chemical Analysis. China Agricultural Sicentech Press, Beijing. pp. 146–165. (in Chinese)Ludemann H, Arth I, Liesack W. 2000. Spatial changes in the bacterial community structure along a vertical oxygen gradient in flooded paddy soil cores. Applied and Environmental Microbiology, 66, 754–762.Maeda K, Morioka R, Hanajima D, Osada T. 2010. The impact of using mature compost on nitrous oxide emission and the denitrifier community in the cattle manure composting process. Microbial Ecology, 59, 25–36.Orellana L H, Rodriguez R L M, Higgins S, Chee-Sanford J C, Sanford R A, Ritalahti K M, Loffler F E, Konstantinidis K T. 2014. Detecting nitrous oxide reductase (nosZ) genes in soil metagenomes: Method development and implications for the nitrogen cycle. mBio, 5, e01193-14.Parkin T B, Sexstone A J, Tiedje J M. 1985. Adaptation of denitrifying populations to low soil pH. Applied and Environmental Microbiology, 49, 1053–1056.Peacock A D, Mullen M D, Ringelberg D B, Tyler D D, Hedrick D B, Gale P M, White D C. 2001. Soil microbial community responses to dairy manure or ammonium nitrate applications. Soil Biology and Biochemistry, 33, 1011–1019.Philippot L. 2002. Denitrifying genes in bacterial and archaeal genomes. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression, 1577, 355–376.Plaza C, Hernández D, García-Gil J C. 2004. Microbial activity in pig slurry-amended soils under semiarid conditions. Soil Biology & Biochemistry, 36, 1577–1585.Ravishankara A, Daniel J S, Portmann R W. 2009. Nitrous oxide (N2O): The dominant ozone-depleting substance emitted in the 21st century. Science, 326, 123–125.Rich J J, Heichen R S, Bottomley P J, Cromack K, Myrold D D. 2003. Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Applied and Environmental Microbiology, 69, 5974–5982.Roberts T L. 2009. The role of fertilizer in growing the world’s food. Better Crops, 93, 2–9.Rösch C, Mergel A, Bothe H. 2002. Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Applied and Environmental Microbiology, 68, 3818–3829.Ryden J C, Lund L J. 1980. Nature and extent of directly measured denitrification losses from some irrigated vegetable crop production units. Soil Science Society of America Journal, 44, 505–511.Saito A, Mitsui H, Hattori R, Minamisawa K, Hattori T. 1998. Slow-growing and oligotrophic soil bacteria phylogenetically close to Bradyrhizobium japonicum. FEMS Microbiology Ecology, 25, 277–286.Salako F K, Babalola O, Hauser S, Kang B T. 1999. Soil macro-aggregate stability under different fallow management systems and cropping intensities in southwestern Nigeria. Geoderma, 91, 103–123.Sanford R A, Wagner D D, Wu Q Z, Chee-Sanford J C, Thomas S H, Cruz-Garcia C, Rodríguez G, Massol-Deya A, Krishnani K K, Ritalahti K M, Nissen S, Konstantinidis K T, Loffler F E. 2012. Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proceedings of the National Academy of Sciences of the United States of America, 109, 19709–19714.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, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537–7541.Shiina Y, Itakura M, Choi H, Saeki Y, Hayatsu M, Minamisawa K. 2014. Relationship between soil type and N2O reductase genotype (nosZ) of indigenous soybean bradyrhizobia: NosZ-minus populations are dominant in Andosols. Microbes and Environments, 29, 420–426. Stark C, Condron L M, Stewart A, Di H J, O’Callaghan M. 2007. Influence of organic and mineral amendments on microbial soil properties and processes. Applied Soil Ecology, 35, 79–93.Stone M M, Deforest J L, Plante A F. 2014. Changes in extracellular enzyme activity and microbial community structure with soil depth at the Luquillo Critical Zone Observatory. Soil Biology & Biochemistry, 75, 237–247.Stres B, Mahne I, Augustin C, Tiedje J M. 2004. Nitrous oxide reductase (nosZ) gene fragments differ between native and cultivated Michigan soils. Applied and Environmental Microbiology, 70, 301–309.Surekha K, Kumari A P P, Reddy M N, Satyanarayana K, Cruz P C S. 2003. Crop residue management to sustain soil fertility and irrigated rice yields. Nutrient Cycling in Agroecosystems, 67, 145–154.Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.Tang J C, Kanamori T, Inoue Y, Yasuta T, Yoshida S, Katayama A. 2004. Changes in the microbial community structure during thermophilic composting of manure as detected by the quinone profile method. Process Biochemistry, 39, 1999–2006.Tiedje J M. 1988. Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder A J B, ed., Biology of Anaerobic Microorganisms. John Wiley and Sons, New York, USA. pp. 179–244.Tirol-Padre A, Tsuchiya K, Inubushi K, Ladha J K. 2005. Enhancing soil quality through residue management in a rice-wheat system in Fukuoka, Japan. Soil Science & Plant Nutrition, 51, 849–860.Throback I N, Enwall K, Jarvis A, Hallin S. 2004. Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiology Ecology, 49, 407–417. Ulrich A, Becker R. 2006. Soil parent material is a key determinant of the bacterial community structure in arable soils. FEMS Microbiology Ecology, 56, 430–443.Wang C X, Zhu G B, Wang Y, Wang S Y, Yin C Q. 2012. Nitrous oxide reductase gene (nosZ) and N2O reduction along the littoral gradient of a eutrophic freshwater lake. Journal of Environmental Sciences, 25, 44–52.Wang H T, Su J Q, Zheng T L, Yang X R. 2014. Impacts of vegetation, tidal process, and depth on the activities, abundances, and community compositions of denitrifiers in mangrove sediment. Applied Microbiology and Biotechnology, 98, 9375–9387.Wolsing M, Prieme A. 2004. Observation of high seasonal variation in community structure of denitrifying bacteria in arable soil receiving artificial fertilizer and cattle manure by determining T-RFLP of nir gene fragments. FEMS Microbiology Ecology, 48, 261–271.Yi N, Gao Y, Zhang Z, Wang Y, Liu X, Zhang L. 2015. Response of spatial patterns of denitrifying bacteria communities to water properties in the stream inlets at Dianchi Lake, China. International Journal of Genomics, 9, 1–11.Yoshida M, Ishii S, Otsuka S, Senoo K. 2009. Temporal shifts in diversity and quantity of nirS and nirK in a rice paddy field soil. Soil Biology and Biochemistry, 41, 2044–2051.Yu W T, Jiang Z S, Ma Q, Zhou H. 2009. Effects of application of manure on soil fertility. Plant Nutrition and Fertilizer Science, 15, 1057–1064. (in Chinese)Zhang X, He L, Zhang F, Sun W, Li Z. 2013. The different potential of sponge bacterial symbionts in N2 release indicated by the phylogenetic diversity and abundance analyses of denitrification genes, nirK and nosZ. PLOS ONE, 8, e65142. Zhu B, Wang T, You X, Gao M R. 2008. Nutrient release from weathering of purplish rocks in the Sichuan Basin, China. Pedosphere, 18, 257–264.Zumft W G. 1997. Cell biology and molecular basis of denitrification. Microbiology and Molecular Biology Reviews, 61, 533–616. |
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