Abstract
Ammonia oxidation process in soil has a great contribution to the emission of nitrous oxide, which is a hot issue in the study of N cycle of rice field ecosystem. Organic amendments which partially substitute chemical nitrogen fertilizer are widely adopted to optimizing N management and reduce the use of chemical nitrogen fertilizers in the paddy ecosystem, but their long-term effects on ammonia-oxidizing archaea (AOA) and bacteria (AOB) were not well understood. Thus, based on a 6-year field trial that comprised four fertilization strategies (CF, chemical fertilizer; PM, pig manure substituting for 20% chemical N; BF, biogas slurry substituting for 20% chemical N; and GM, milk vetch substituting for 20% chemical N) and no N fertilizer application as CK, the abundance and community structure of ammonia oxidizers were examined by using qPCR and Illumina Miseq sequencing approaches based on the functional marker genes (amoA) in a low-fertility paddy field. The results revealed that 6 years of organic-substitute fertilization significantly increased AOA abundance in comparison with NF and CF. However, only CF and PM had a higher AOB abundance than those in NF and no significant difference between CF and organic-substitute treatments was observed. Both AOA and AOB were significantly correlated with soil potential nitrification rate (PNR). Moreover, organic-substitute treatments showed the evident changes in the AOA community, while little were observed in the AOB community. Soil pH was the main predictor for AOA abundance, while NH4+–N and NO3−–N were the main predictors for AOB abundance. This study suggests that both AOA and AOB were jointly contributed to the variation of soil potential nitrification rate, while the AOA community was shown to be more responsive to organic-substitute fertilization strategies than AOB in the tested soils.
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References
Chen X, Zhang LM, Shen JP, Wei WX, He JZ (2011) Abundance and community structure of ammonia-oxidizing archaea and bacteria in an acid paddy soil. Biol Fertil Soils 47(3):323–331. https://doi.org/10.1007/s00374-011-0542-8
Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A (2015) Complete nitrification by Nitrospira bacteria. Nature 528:504–509. https://doi.org/10.1038/nature16461
Duan R, Long XE, Tang YF, Wen J, Su SM, Bai LY, Liu RL, Zeng XB (2018) Effects of different fertilizer application methods on the community of nitrifiers and denitrifiers in a paddy soil. J Soils Sediments 18:24–38. https://doi.org/10.1007/s11368-017-1738-9
Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33(5):855–869. https://doi.org/10.1111/j.1574-6976.2009.00179.x
Fang Y, Wang F, Jia X, Chen J (2019) Distinct responses of ammonia-oxidizing bacteria and archaea to green manure combined with reduced chemical fertilizer in a paddy soil. J Soils Sediments 19(4):1613–1623. https://doi.org/10.1007/s11368-018-2154-5
FAO (2018) Food and Agriculture Organization of the United Nations Corporate Statistical Database Available online at http://faostat.fao.org/beta/en/
Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci U S A 102:14683–14688. https://doi.org/10.1073/pnas.0506625102
Gao SJ, Cao WD, Zou CQ, Gao JS, Huang J, Bai JS, Zeng NH, Shimizu KY, Wright A, Dou FG (2018) Ammonia-oxidizing archaea are more sensitive than ammonia-oxidizing bacteria to long-term application of green manure in red paddy soil. Appl Soil Ecol 124:185–193. https://doi.org/10.1016/j.apsoil.2017.09.041
Gu BJ, Ge Y, Ren Y, Xu B, Luo WD, Jiang H, Gu BH, Chang J (2012) Atmospheric reactive nitrogen in China: sources, recent trends, and damage costs. Environ Sci Technol 46(17):9420–9427. https://doi.org/10.1021/es301446g
Gu BJ, Ju XT, Chang J, Ge Y, Vitousek PM (2015) Integrated reactive nitrogen budgets and future trends in China. Proc Natl Acad Sci U S A 112(28):8792–8797. https://doi.org/10.1073/pnas.1510211112
Guo JJ, Ling N, Chen H, Zhu C, Kong YL, Wang M, Shen QR, Guo SW (2017) Distinct drivers of activity, abundance, diversity and composition of ammonia-oxidizers: evidence from a long-term field experiment. Soil Biol Biochem 115:403–414. https://doi.org/10.1016/j.soilbio.2017.09.007
He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di HJ (2007) Quantitative analyses of theabundance 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. https://doi.org/10.1111/j.1462-2920.2007.01358.x
Hu HW, Zhang LM, Dai Y, Di HJ, He JZ (2013) pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. J Soils Sediments 13:1439–1449. https://doi.org/10.1007/s11368-013-0726-y
Jiang HC, Huang LQ, Deng Y, Wang S, Zhou Y, Liu L, Dong HL (2014) Latitudinal distribution of ammonia-oxidizing bacteria and archaea in the agricultural soils of eastern China. Appl Environ Microbiol 80:5593–5602. https://doi.org/10.1128/AEM.01617-14
Jiang XJ, Hou X, Zhou X, Xin X, Wright A, Jia Z (2015) pH regulates key players of nitrification in paddy soils. Soil Biol Biochem 81:9–16. https://doi.org/10.1016/j.soilbio.2014.10.025
Ke X, Lu Y (2012) Adaptation of ammonia-oxidizing microorganisms to environment shift of paddy field soil. FEMS Microbiol Ecol 80(1):87–97. https://doi.org/10.1111/j.1574-6941.2011.01271.x
Ke X, Angel R, Lu Y, Conrad R (2013) Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil. Environ Microbiol 15(8):2275–2292. https://doi.org/10.1111/1462-2920.12098
Khaliq A, Abbasi MK, Hussain T (2006) Effects of integrated use of organic and inorganic nutrient sources with effective microorganisms (EM) on seed cotton yield in Pakistan. Bioresour Technol 97(8):967–972. https://doi.org/10.1016/j.biortech.2005.05.002
Kits KD, Sedlacek CJ, Lebedeva EV, Han P, Bulaev A, Pjevac P, Daebeler A, Romano S, Albertsen M, Stein LY, Daims H, Wagner M (2017) Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature 549:269–272. https://doi.org/10.1038/nature23679
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. https://doi.org/10.1016/j.femsle.2005.06.057
Li H, Weng BS, Huang FY, Su JQ, Yang XR (2015) pH regulates ammonia-oxidizing bacteria and archaeain paddy soils in Southern China. Appl Microbiol Biotechnol 99(14):6113–6123. https://doi.org/10.1007/s00253-015-6488-2
Li YY, Chapman SJ, Nicol GW, Yao HY (2018) Nitrification and nitrifiers in acidic soils. Soil Biol Biochem 116:290–301. https://doi.org/10.1016/j.soilbio.2017.10.023
Liu MQ, Hu F, Chen XY, Huang QR, Jiao JG, Zhang B, Li HX (2009) Organic amendments with reduced chemical fertilizer promote soil microbial development and nutrient availability in a subtropical paddy field: the influence of quantity, type and application time of organic amendments. Appl Soil Ecol 42(2):166–175. https://doi.org/10.1016/j.apsoil.2009.03.006
Mukhtar H, Lin YP, Anthony J (2017) Ammonia oxidizing archaea and bacteria in east Asian paddy soils-a mini review. Environments 4(4):84. https://doi.org/10.3390/environments4040084
Ouyang Y, Norton JM, Stark JM, Reeve JR, Habteselassie MY (2016) Ammonia-oxidizing bacteria are more responsive than archaea to nitrogen source in an agricultural soil. Soil Biol Biochem 96:4–15. https://doi.org/10.1016/j.soilbio.2016.01.012
Pjevac P, Schauberger C, Poghosyan L, Herbold CW, van Kessel MA, Daebeler A, Steinberger M, Jetten MS, Lücker S, Wagner M (2017) AmoA-targeted polymerasechain reaction primers for the specific detection and quantification of comammox Nitrospira in the environment. Front Microbiol 8:1508. https://doi.org/10.3389/fmicb.2017.01508
Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20(11):523–531. https://doi.org/10.1016/j.tim.2012.08.001
Rotthauwe JH, Witzel KP, 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
Saiful Alam M, Ren G, Lu L, Zheng Y, Peng X, Jia ZJ (2013) Ecosystem-specific selection of microbial ammonia oxidizers in an acid soil. Biogeosci Discuss 10:1717–1746. https://doi.org/10.5194/bgd-10-1717-2013
Shen JP, Zhang LM, Di HJ, He JZ (2012) A review of ammonia-oxidizing bacteria and archaea in Chinese soils. Front Microbiol 3:296. https://doi.org/10.3389/fmicb.2012.00296
Shen WS, Xu TT, Liu JJ, Huang QR, Gu GY, Zhong WH (2015) Long-term application of organic manure changes abundance and composition of ammonia-oxidizing archaea in an acidic red soil. J Soil Sci Plant Nut 61(4):620–628. https://doi.org/10.1080/00380768.2015.1023687
Simonin M, Le Roux XL, Poly F, Lerondelle C, Hungate BA, Nunan N, Niboyet A (2015) Coupling between and among ammonia oxidizers and nitrite oxidizers in grassland mesocosms submitted to elevated CO2 and nitrogen supply. Microb Ecol 70(3):809–818. https://doi.org/10.1007/s00248-015-0604-9
Song H, Che Z, Cao WC, Huang T, Wang JG, Dong ZR (2016) Changing roles of ammonia-oxidizing bacteria and archaea in a continuously acidifying soil caused by over-fertilization with nitrogen. Environ Sci Pollut Res 23:11964–11974. https://doi.org/10.1007/s11356-016-6396-8
Sun RB, Guo X, Wang D, Chu HY (2015) Effects of long-term application of chemical and organic fertilizers on the abundance of microbial communities involved in the nitrogen cycle. Appl Soil Ecol 95:171–178. https://doi.org/10.1016/j.apsoil.2015.06.010
Sun RB, Myrold DD, Wang D, Wang DZ, Guo XS, Chu HY (2019) AOA and AOB communities respond differently to changes of soil pH under long-term fertilizatio. Soil Ecology Letters 1(3–4):126–135. https://doi.org/10.1007/s42832-019-0016-8
Tao R, Wakelin SA, Liang YC, Chu GX (2017) Response of ammonia oxidizing archaea and bacteria in calcareous soil to mineral and organic fertilizer application and their relative contribution to nitrification. Soil Biol Biochem 114:20–30. https://doi.org/10.1016/j.soilbio.2017.06.027
Taylor AE, Zeglin LH, Wanzek TA, Myrold DD, Bottomley PJ (2012) Dynamics of ammonia-oxidizing archaea and bacteria populations and contributions to soil nitrification potentials. ISME J 6:2024–2032. https://doi.org/10.1038/ismej.2012.51
Taylor AE, Giguere AT, Zoebelein CM, Myrold DD, Bottomley PJ (2017) Modeling of soil nitrification responses to temperature reveals thermodynamic differences between ammonia-oxidizing activity of archaea and bacteria. ISME J 11(4):896–908. https://doi.org/10.1038/ismej.2016.179
Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5:1067–1071. https://doi.org/10.1038/ismej.2010.191
Wang YF, Gu JD (2013) Higher diversity of ammonia/ammonium-oxidizing prokaryotes in constructed freshwater wetland than natural coastal marine wetland. Appl Microbiol Biotechnol 97(15):7015–7033. https://doi.org/10.1007/s00253-012-4430-4
Wang BZ, Zhao J, Guo ZY, Ma J, Xu H, Jia ZJ (2015) Differential contributions of ammonia oxidizers and nitrite oxidizers to nitrification in four paddy soils. ISME J 9:1062–1075. https://doi.org/10.1038/ismej.2014.194
Wang JC, Ni L, Song Y, Rhodes G, Li J, Huang QW, Shen QR (2017) Dynamics response of ammonia-oxidizers to four fertilization regimes across a wheat-rice rotation system. Front Microbiol 8:630. https://doi.org/10.3389/fmicb.2017.00630
Wang JC, Wang JL, Rhodes G, He JZ, Ge Y (2019) Adaptive responses of comammox Nitrospira and canonical ammonia oxidizers to long-term fertilizations: Implications for the relative contributions of different ammonia oxidizers to soil nitrogen cycling. Sci Total Environ. 668:224–233. https://doi.org/10.1016/j.scitotenv.2019.02.427
Wessen E, Nyberg K, Jansson JK, Hallin S (2010) Responses of bacterial and archaeal ammonia oxidizers to soil organic and fertilizer amendments under long-term management. Appl Soil Ecol 45:193–200. https://doi.org/10.1016/j.apsoil.2010.04.003
Wu YC, Lu L, Wang BZ, Lin XG, Zhu JG, Cai ZC, Yan XY, Jia ZJ (2011) Long-term field fertilization significantly alters community structure of ammonia-oxidizing bacteria rather than archaea in a paddy soil. Soil Sci Soc Am J 75(4):1431–1439. https://doi.org/10.2136/sssaj20l0.0434
Xia WW, Zhang CX, Zeng XW, Feng YZ, Weng JH, Lin XG, Jia ZJ (2011) Autotrophic growth of nitrifyingcommunity in an agricultural soil. ISME J 5:1226–1236. https://doi.org/10.1038/ismej.2011.5
Xia LL, Lam SK, Yan XY, Chen DL (2017) How does recycling of livestock manure in agroecosystems affect crop productivity, reactive nitrogen losses and soil carbon balance? Environ Sci Technol 51(13):7450–7457. https://doi.org/10.1021/acs.est.6b06470
Yang XR, Li H, Nie SA, Su JQ, Weng BS, Zhu GB, Yao HY, Gilbert JA, Zhu YG (2015) Potential contribution of anammox to nitrogen loss from paddy soils in Southern China. Appl Environ Microbiol 81(3):938–947. https://doi.org/10.1128/AEM.02664-14
Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045. https://doi.org/10.1038/ismej.2011.168
Zhao J, Ni T, Li J, Lu Q, Fang ZY, Huang QW, Zhang RF, Li R, Shen B, Shen QR (2016) Effects of organic-inorganic compound fertilizer with reduced chemical fertilizer application on crop yields, soil biological activity and bacterial community structure in a rice-wheat cropping system. Appl Soil Ecol 99:1–12. https://doi.org/10.1016/j.apsoil.2015.11.006
Acknowledgments
We would like to appreciate the helpful suggestion from Lei Guo, XuHong Ye, and YueKai Wang. We also thank YingXin Ma, Jinheng Bai, and Ping Sun for their strong assistance in the soil sampling and measurement of soil properties.
Funding
This research is financially supported by the National Key Research and Development Program of China (NO.2016YFD0201200).
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Yang, D., Xiao, X., He, N. et al. Effects of reducing chemical fertilizer combined with organic amendments on ammonia-oxidizing bacteria and archaea communities in a low-fertility red paddy field. Environ Sci Pollut Res 27, 29422–29432 (2020). https://doi.org/10.1007/s11356-020-09120-5
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DOI: https://doi.org/10.1007/s11356-020-09120-5