Abstract
Ammonia-oxidizing bacteria (AOB) and archaea (AOA) are very important in regulating the process of soil nitrification. However, little is known how responses of AOB and AOA communities to yak excreta application in wetland soils. We investigated AOB and AOA community composition using excreta application treatments to examine how nitrification response to yak excreta application by regulating the ammonia-oxidizing microorganism communities in meadow marsh soil (MMS) and marsh soil (MS). The microcosm experiments of excreta application were established in MMS and MS. The microcosms were subject to dung application (DA), urine application (UA) and control (CK). Molecular methods were applied to determine the compositions of AOA and AOB. Chao, ACE, Shannon and Simpson indices were applied to measure species richness and diversity. Potential nitrification rate (PNR) was higher in MMS than in MS. DA significantly increased PNR in MMS, whereas DA decreased PNR in MS. The urease activity was lower in MMS than in MS, whereas catalase activity was opposite. DA increased urease and catalase activities significantly in MMS and MS. Excreta application decreased the alpha diversity of AOB in MMS whereas the trend was opposite in MS, and it was higher in MMS than in MS. The canonical correspondence analysis (CCA) demonstrated that the urease and catalase activities were the important factors to change the AOB community structure in MS. Structural equation modelling (SEM) showed PNR was indirectly influenced by total phosphorus (TP) through mediation of the ACE index and Simpson index of AOB. Yak excreta application can alter soil environmental conditions resulted in changes in AOB community composition. However, the response of AOA to yak excreta application was much weaker than that of AOB in both MMS and MS.
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References
Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry. Academic, New York, pp 569–576. https://doi.org/10.1016/B978-0-12-513840-6.X5014-9
Ansola G, Arroyo P, Sáenz de Miera LE (2014) Characterisation of the soil bacterial community structure and composition of natural and constructed wetlands. Sci Total Environ 473–474:63–71. https://doi.org/10.1016/j.scitotenv.2013.11.125
Awasthi MK, Wang Q, Awasthia SK, Wang M, Chen H, Ren X, Zhao J, Zhang Z (2018) Influence of medical stone amendment on gaseous emissions, microbial biomass and abundance of ammonia oxidizing bacteria genes during biosolids composting. Bioresource Technol 247:970–979. https://doi.org/10.1016/j.biortech.2017.09.201
Boon A, Robinson JS, Chadwickm DR, Cardenas LM (2014) Effect of cattle urine addition on the surface emissions and subsurface concentrations of greenhouse gases from a UK lowland peatland. Agr Ecosyst Environ 186:23–32
Byrnes BH, Amberger A (1989) Fate of broadcast urea in a flooded soil when treated with N-(n-butyl) thiophospheric triamide, a urease inhibitor. Fertil Res 18:221–231. https://doi.org/10.1007/bf01049572
Cai X, Lin Z, Penttinen P, Li Y, Li Y, Luo Y, Yue T, Jiang P, Fu W (2018) Effects of conversion from a natural evergreen broadleaf forest to a Moso bamboo plantation on the soil nutrient pools, microbial biomass and enzyme activities in a subtropical area. Forest Ecol Manag 422:161–171. https://doi.org/10.1016/j.foreco.2018.04.022
Carrera AL, Mazzarino MJ, Bertiller MB, del Valle HF, Carretero EM (2009) Plant impacts on nitrogen and carbon cycling in the Monte Phytogeographical Province, Argentina. J Arid Environ 73:192–220. https://doi.org/10.1016/j.jaridenv.2008.09.016
Chen L, Zheng R, Guo X, Hou Y (2020) Effects of different grazing forms on ammonia-oxidizing microorganism communities in peat swamp soils of Northwest Yunnan. Acta Ecol Sin 7:2321–2332. https://doi.org/10.5846/stxb201901200157
Cui P, Fan F, Yin C, Li Z, Song A, Wan Y, Liang Y (2013) Urea- and nitrapyrin-affected N2O emission is coupled mainly with ammonia oxidizing bacteria growth in microcosms of three typical Chinese arable soils. Soil Biol Biochem 66:214–221. https://doi.org/10.1016/j.soilbio.2013.08.001
Das SK, Varma A (2011) Role of enzymes in maintaining soil health. Soil Biology 22:25–42. https://doi.org/10.1007/978-3-642-14225-3_2
Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624. https://doi.org/10.1038/ngeo613
Enriquez AS, Chimner RA, Cremona MV (2014) Long-term grazing negatively affects nitrogen dynamics in northern Patagonian wet meadows. J Arid Environ 109:1–5. https://doi.org/10.1016/j.jaridenv.2014.04.012
Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33:855–869. https://doi.org/10.1111/j.1574-6976.2009.00179.x
Fang X, Zheng RB, Guo XL, Fu Q, Zhang K (2020) Responses of denitrification rate and denitrifying bacterial communities carrying nirS and nirK genes to grazing in peatland. J Soil Sci Plant Nutr 20:1249–1260. https://doi.org/10.1007/s42729-020-00209-x
Fang X, Zheng RB, Guo XL, Fu Q, Fan FH, Liu S (2021) Yak excreta-induced changes in soil microbial communities increased the denitrification rate of marsh soil under warming conditions. Appl Soil Ecol 165:103935. https://doi.org/10.1016/j.apsoil.2021.103935
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. P Natl Acad Sci USA 102:14683–14688. https://doi.org/10.1073/pnas.0506625102
Guo XL, Chen L, Zheng RB, Zhang K, Qiu YP, Yue HT (2019) Differences in soil nitrogen availability and transformation in relation to land use in the Napahai Wetland, Southwest China. J Soil Sci Plant Nutr 19:92–97. https://doi.org/10.1007/s42729-019-0013-0
Guo YJ, Di HJ, Cameron KC, Li B (2014) Effect of application rate of a nitrification inhibitor, dicyandiamide (DCD), on nitrification rate, and ammonia-oxidizing bacteria and archaea growth in a grazed pasture soil: an incubation study. J Soil Sediment 14:897–903. https://doi.org/10.1007/s11368-013-0843-7
Haynes RJ, Williams PH (1993) Nutrient cycling and soil fertility in the grazed pasture ecosystem. Adv Agron 49:119–199. https://doi.org/10.1016/s0065-2113(08)60794-4
IPCC (2013) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V and Midgley PM, Eds., Cambridge University Press, Cambridge, 153. https://doi.org/10.1017/CBO9781107415324
Johnson J, Cummins T, Aherne J (2016) Critical loads and nitrogen availability under deposition and harvest scenarios for conifer forests in Ireland. Sci Total Environ 541:319–328. https://doi.org/10.1016/j.scitotenv.2015.08.140
Kandeler E, Gerber H (1988) Short term assay of soil urease activity using colorimetric determination of ammonium. Biol Fert Soils 6:68–72. https://doi.org/10.1007/bf00257924
Könneke M, Bernhard AE, dela Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546. https://doi.org/10.1038/nature03911
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
Lakhdar A, Scelza R, Scotti R, Rao MA, Jedidi N, Gianfreda L, Abdelly C (2010) The effect of compost and sewage sludge on soil biologic activities in salt affected soil. R c Suelo Nutr Veg 10:40–47. https://doi.org/10.4067/s0718-27912010000100005
Liang YK, Wang QH, Huang L, Liu ML, Wang N, Chen YC (2020) Insight into the mechanisms of biochar addition on pollutant removal enhancement and nitrous oxide emission reduction in subsurface flow constructed wetlands: microbial community structure, functional genes and enzyme activity. Biores Technol 307:123249. https://doi.org/10.1016/j.biortech.2020.123249
Li BX, Yang YY, Chen JF, Wu Z, Liu Y, Xie SG (2018) Nitrifying activity and ammonia-oxidizing microorganisms in a constructed wetland treating polluted surface water. Sci Total Environ 628–629:310–318. https://doi.org/10.1016/j.scitotenv.2018.02.041
Li CY, Di HJ, Cameron KC, Podolya A, Zhu BC (2016) Effect of different land use and land use change on ammonia oxidiser abundance and N2O emissions. Soil Biol Biochem 96:169–175. https://doi.org/10.1016/j.soilbio.2016.02.005
Li J, Cooper JM, Lin ZA, Li YT, Yang XD, Zhao BQ (2015) Soil microbial community structure and function are significantly affected by long-term organic and mineral fertilization regimes in the North China Plain. Appl Soil Ecol 96:75–87. https://doi.org/10.1016/j.apsoil.2015.07.001
Liu HY, Li J, Zhao Y, Xie KX, Tang XJ, Wang SX, Li ZP, Liao YL, Xu JM, Di HJ, Li Y (2018) Ammonia oxidizers and nitrite-oxidizing bacteria respond differently to long-term manure application in four paddy soils of south of China. Sci Total Environ 633:641–648. https://doi.org/10.1016/j.scitotenv.2018.03.108
Liu SY, Zheng RB, Guo XL, Wang X, Chen L, Hou YW (2019) Effects of yak excreta on soil organic carbon mineralization and microbial communities in alpine wetlands of southwest of China. J Soil Sediment 19:1490–1498. https://doi.org/10.1007/s11368-018-2149-2
Lovell RD, Jarvis SC (1996) Effect of cattle dung on soil microbial biomass C and N in a permanent pasture soil. Soil Biol Biochem 28:291–299. https://doi.org/10.1016/0038-0717(95)00140-9
López-Aizpún M, Arango-Mora C, Santamaría C, Lasheras E, Santamaría JM, Ciganda VS, Elustondo D (2018) Atmospheric ammonia concentration modulates soil enzyme and microbial activity in an oak forest affecting soil microbial biomass. Soil Biol Biochem 116:378–387. https://doi.org/10.1016/j.soilbio.2017.10.020
Luo L, Meng H, Gu J-D (2017) Microbial extracellular enzymes in biogeochemical cycling of ecosystems. J Environ Manag 197:539–549. https://doi.org/10.1016/j.jenvman.2017.04.023
Lupwayi NZ, Zhang YT, Hao XY, Thomas BW, Eastman AH, Schwinghamer TD (2019) Linking soil microbial biomass and enzyme activities to long-term manure applications and their nonlinear legacy. Pedobiologia 74:34–42. https://doi.org/10.1016/j.pedobi.2019.04.001
O’Callaghan M, Gerard EM, Carter PE, Lardner R, Sarathchandra U, Burch G, Ghani A, Bell N (2010) Effect of the nitrification inhibitor dicyandiamide (DCD) on microbial communities in a pasture soil amended with bovine urine. Soil Biol Biochem 42:1425–1436. https://doi.org/10.1016/j.soilbio.2010.05.003
Moghimian N, Hosseini SM, Kooch Y, Darki BZ (2017) Impacts of changes in land use/cover on soil microbial and enzyme activities. CATENA 157:407–414. https://doi.org/10.1016/j.catena.2017.06.003
Olivera NL, Prieto L, Carrera AL, Cisneros HS, Bertiller MB (2014) Do soil enzymes respond to long-term grazing in an arid ecosystem? Plant Soil 378(1–2):35–48. https://doi.org/10.1007/s11104-013-2010-8
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
Ravishankara AR, Daniel JS, Portmann RW (2009) The dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125
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 284:63–64. https://doi.org/10.1126/science.284.5411.63
Saiful Alam M, Ren G, Lu L, Zheng Y, Peng X, Jia Z (2013) Ecosystem-specific selection of microbial ammonia oxidizers in an acid soil. Biogeosciences Discussions 10:1717–1746
Shi SH, Tian L, Nasir F, Bahadur A, Batool A, Luo SS, Yang F, Wang ZC, Tian C (2019) Response of microbial communities and enzyme activities to amendments in saline-alkaline soils. Appl Soil Ecol 135:16–24. https://doi.org/10.1016/j.apsoil.2018.11.003
Sterngren AE, Hallin S, Bengtson P (2015) Archaeal ammonia oxidizers dominate in numbers, but bacteria drive gross nitrification in N-amended grassland soil. Front Microbiol 6:1350. https://doi.org/10.3389/fmicb.2015.01350
Suleiman AKA, Gonzatto R, Aita C, Lupatini M, Jacques RJS, Kuramae EE, Antoniolli ZI, Roesch LFW (2016) Temporal variability of soil microbial communities after application of dicyandiamide-treated swine slurry and mineral fertilizers. Soil Biol Biochem 97:71–82. https://doi.org/10.1016/j.soilbio.2016.03.002
Tang YQ, Zhang XY, Li DD, Wang HM, Chen FS, Fu XL, Fang XM, Sun XM, Yu GR (2016) Impacts of nitrogen and phosphorus additions on the abundance and community structure of ammonia oxidizers and denitrifying bacteria in Chinese fir plantations. Soil Biol and Biochem 103:284–293. https://doi.org/10.1016/j.soilbio.2016.09.001
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
Van Groenigen JW, Kuikman PJ, de Groot WJM, Velthof GL (2005) Nitrous oxide emission from urine-treated soil as influenced by urine composition and soil physical conditions. Soil Biol Biochem 37:463–473. https://doi.org/10.1016/j.soilbio.2004.08.009
Wakelin SA, Clough TJ, Gerard EM, O’Callaghan M (2013) Impact of short-interval, repeat application of dicyandiamide on soil N transformation in urine patches. Agr Ecosyst Environ 167:60–70. https://doi.org/10.1016/j.agee.2013.01.007
Wakelin SA, Gerard E, van Koten C, Banabas M, O’Callaghan M, Nelson PN (2016) Soil physicochemical properties impact more strongly on bacteria and fungi than conversion of grassland to oil palm. Pedobiologia 59:83–91. https://doi.org/10.1016/j.pedobi.2016.03.001
Wang JC, Ni L, Song Y, Rhodes G, Li J, Huang QW, Shen QR (2017a) Dynamics response of ammonia-oxidizers to four fertilization regimes across a wheat-rice rotation system. Front Microbiol 8:630
Wang YY, Chen J, Zhou SA, Wang XD, Chen Y, Lin XM, Yan Y, Ma X, Wu M, Han HC (2017b) 16S rRNA gene high-throughput sequencing reveals shift in nitrogen conversion related microorganisms in a CANON system in response to salt stress. Chem Eng J 317:512–521. https://doi.org/10.1016/j.cej.2017.02.096
Wang SF, Guo XL, Yu LC, Liu SY, Wang X, Tang SL (2017c) Soil nutrient and nitrous oxide flux of Bita Lake Peat Bogs under influence of Yak grazing. Wetland Science 15:244–249. https://doi.org/10.13248/j.cnki.wetlandsci.2017.02.012
Xiang XJ, He D, He JS, Myrold DD, Chu HY (2017) Ammonia-oxidizing bacteria rather than archaea respond to short-term urea amendment in an alpine grassland. Soil Biol Biochem 107:218–225. https://doi.org/10.1016/j.soilbio.2017.01.012
Xu XY, Liu XR, Li Y, Ran Y, Liu YP, Zhang QC, Li Z, He Y, Xu JM, Di HJ (2017) High temperatures inhibited the growth of soil bacteria and archaea but not that of fungi and altered nitrous oxide production mechanisms from different nitrogen sources in an acidic soil. Soil Biol Biochem 107:168–179. https://doi.org/10.1016/j.soilbio.2017.01.003
Yan L, Li ZG, Wang GX, Gao YM, Wang YJ, Gu JD, Wang WD (2016) Diversity of ammonia-oxidizing bacteria and archaea in response to different aeration rates during cattle manure composting. Ecol Eng 93:46–54. https://doi.org/10.1016/j.ecoleng.2016.05.002
Yang YD, Ren YF, Wang XQ, Hu YG, Wang ZM, Zeng ZH (2017) Ammonia-oxidizing archaea and bacteria responding differently to fertilizer type and irrigation frequency as revealed by Illumina Miseq sequencing. J Soil Sediment 18:1029–1040. https://doi.org/10.1007/s11368-017-1792-3
Yao HY, Campbell CD, Chapman SJ, Freitag TE, Nicol GW, Singh BK (2013) Multi-factorial drivers of ammonia oxidizer communities: evidence from a national soil survey. Environ Microbiol 15:2545–2556. https://doi.org/10.1111/1462-2920.12141
Zhang JP, Liu B, Zhou XH, Chu JY, Li YM, Wang MY (2015) Effects of emergent aquatic plants on abundance and community structure of ammonia-oxidising microorganisms. Ecol Eng 8:504–513. https://doi.org/10.1016/j.ecoleng.2015.04.029
Zhang LH, Song CC, Wang DX, Wang YY (2007) Effects of exogenous nitrogen on freshwater marsh plant growth and N2O fluxes in Sanjiang Plain, Northeast China. Atmos Environ 41:1080–1090. https://doi.org/10.1016/j.atmosenv.2006.09.029
Zhang MM, Luo P, Liu F, Li HF, Zhang SN, Xiao RL, Yin LMM, Zhou J, Wu JS (2017) Nitrogen removal and distribution of ammonia-oxidizing and denitrifying genes in an integrated constructed wetland for swine wastewater treatment. Ecol Eng 104:30–38. https://doi.org/10.1016/j.ecoleng.2017.04.022
Zhou H, Zhang DG, Jiang ZH, Sun P, Xiao HL, Wu YX, Chen JG (2018) Changes in the soil microbial communities of alpine steppe at Qinghai-Tibetan Plateau under different degradation levels. Sci. Total Environ 615:2281–2291. https://doi.org/10.1016/j.scitotenv.2018.09.336
Zhou J, Guan DW, Zhou BK, Zhao BS, Ma MC, Qin J, Jiang XJ, Chen SF, Cao FM, Shen DL, Li J (2015a) Influence of 34-years of fertilization on bacterial communities in an intensively cultivated black soil in northeast China. Soil Biol Bioch 90:42–51. https://doi.org/10.1016/j.soilbio.2015.07.005
Zhou X, Fornara D, Wasson EA, Wang DM, Ren G, Christie P, Jia ZJ (2015b) Effects of 44 years of chronic nitrogen fertilization on the soil nitrifying community of permanent grassland. Soil Biol Biochem 91:76–83. https://doi.org/10.1016/j.soilbio.2015.08.031
Zhou ZF, Shi XJ, Zheng Y, Qin ZX, Xie DT, Li ZL, Guo T (2014) Abundance and community structure of ammonia-oxidizing bacteria and archaea in purple soil under long-term fertilization. Eur J Soil Biol 60:24–33. https://doi.org/10.1016/j.ejsobi.2013.10.003
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This work was supported by the National Natural Science Foundation of China (No. 41563008), Yunnan Fundamental Research Projects (202001AS070041;202001AS070042), Academician and Expert Workstation of Yunnan Province (2019IC012) and the Plateau Wetlands Science Innovation Team of Yunnan Province (2012HC007).
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Chen, L., Zheng, R.B., Gao, J.Q. et al. Yak Excreta Application Alter Nitrification by Regulating the Ammonia-Oxidizing Bacterial Communities in Wetland Soils. J Soil Sci Plant Nutr 21, 2753–2764 (2021). https://doi.org/10.1007/s42729-021-00562-5
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DOI: https://doi.org/10.1007/s42729-021-00562-5