Abstract
Purpose
The complete ammonia oxidizers (comammox) capable of catalyzing nitrification, oxidizing ammonia to nitrate, via activity of only one type of microbes were recently discovered which has updated our knowledge of traditional two-step nitrification. The extent of contribution of comammox and canonical ammonia oxidizers including ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) to soil nitrification, especially in soils with long-term input of nitrogen (N) fertilizers, remains unknown.
Materials and methods
The transcriptional abundance of amoA gene from comammox, AOA, and AOB in soils fertilized for 29 years was investigated in different seasons and soil layers via quantitative PCR.
Results and discussion
The results showed that comammox were detected in all soil samples; however, AOA and AOB had significantly higher transcriptional abundance of amoA gene than comammox. Nitrification activity was most significantly correlated with the transcriptional abundance of AOA amoA gene (Pearson correlation, r = 0.217, P < 0.05) suggesting AOA were the dominant contributors to soil potential nitrification. Lower abundances of amoA gene transcripts were observed in July than in April and November. The application of high level of mineral N fertilizer decreased the abundance of both AOA and AOB; however, long-term input of organic manure combined with mineral N fertilizer stabilized the abundances of ammonium-oxidizing microbes in soils. Seasonal variation and fertilization regimes substantially affected the abundance of both AOA and AOB, but AOB were not as sensitive in responding to the seasonal variation and fertilization as AOA. The analysis of RDA and VPA demonstrated that sampling month, soil depth, and fertilization regime explained 30.20%, 11.46%, and 5.40% of the variation in nitrification microorganism amoA gene composition, respectively. Seasonal variation exerted the most influences on the nitrifiers’ composition, and soil depth and fertilization regime were also important factors in shaping the nitrifier communities. According to the correlation analysis, NO3−–N content was the most important soil property in impacting the transcriptional abundance of amoA gene, and the amoA gene transcript abundance decreased with increasing NO3−–N content.
Conclusions
The results suggest that the activity of comammox may be more inhibited by the long-term nitrogen fertilization than canonical ammonia oxidizers in agricultural soils. This study provides insights into the different responses of comammox and canonical ammonia oxidizers to fertilization, seasonal variation, and soil depth and their relative contributions to nitrification in agricultural soil.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article and its supplementary information files.
Code availability
Not applicable.
References
Ai C, Liang GQ, Sun JW, Wang XB, 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 Boil Biochem 57:30–42. https://doi.org/10.1016/j.soilbio.2012.08.003
Bahram M, Hildebrand F, Forslund SK, Anderson JL, Soudzilovskaia NA, Bodegom PM, Bengtsson-Palme J, Anslan S, Coelho LP, Harend H, Huerta-Cepas J, Medema WH, Maltz MR, Mundra S, Olsson PA, Pent M, Põlme S, Sunagawa S, Ryberg M, Tedersoo L, Tedersoo P (2018) Structure and function of the global topsoil microbiome. Nature 560:233–237. https://doi.org/10.1038/s41586-018-0386-6
Bandyopadhyay KK, Misra AK, Ghosh PK, Hati KM (2010) Effect of integrated use of farmyard manure and chemical fertilizers on soil physical properties and productivity of soybean. Soil Tillage Res 110:115–125. https://doi.org/10.1016/j.still.2010.07.007
Barnard RL, Osborne CA, Firestone MK (2015) Changing precipitation pattern alters soil microbial community response to wet-up under a Mediterranean-type climate. ISME J 9:946–957. https://doi.org/10.1038/ismej.2014.192
Berg P, Rosswall T (1985) Ammonium oxidizer numbers, potential and actual oxidation rates in two Swedish arable soils. Biol Fertil Soils 1:131–140. https://doi.org/10.1007/BF00301780
Carey CJ, Dove NC, Beman JM, Hart SC, Aronson EL (2016) Meta-analysis reveals ammonia-oxidizing bacteria respond more strongly to nitrogen addition than ammonia-oxidizing archaea. Soil Biol Biochem 99:158–166. https://doi.org/10.1016/j.soilbio.2016.05.014
Che R, Wang F, Wang W, Zhang J, Zhao X, Rui Y, Xu Z, Wang Y, Hao Y, Cui X (2017) Increase in ammonia-oxidizing microbe abundance during degradation of alpine meadows may lead to greater soil nitrogen loss. Biogeochemistry 136:341–352. https://doi.org/10.1007/s10533-017-0399-5
Chen D, Yuan L, Liu Y, Ji J, Hou H (2017a) Long-term application of manures plus chemical fertilizers sustained high rice yield and improved soil chemical and bacterial properties. Eur J Agron 90:34–42. https://doi.org/10.1016/j.eja.2017.07.007
Chen LJ, Feng Q, Wei YP, Li CS, Zhao Y, Li HY, Zhang BG (2017b) Effects of saline water irrigation and fertilization regimes on soil microbial metabolic activity. J Soils Sediments 17:376–383. https://doi.org/10.1007/s11368-016-1551-x
Cláudio NA (2016) Do it yourself nitrification. Nat Rev Microbiol 14:61–61. https://doi.org/10.1038/nrmicro.2015.20
Costa E, Pérez J, Kreft JU (2006) Why is metabolic labour divided in nitrification? Trends Microbiol 14:213–219. https://doi.org/10.1016/j.tim.2006.03.006
Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PR, Wagner M (2015) Complete nitrification by Nitrospira bacteria. Nature 528:504–509. https://doi.org/10.1038/nature16461
DeAngelis KM, Silver WL, Thompson AW, Firestone MK (2010) Microbial communities acclimate to recurring changes in soil redox potential status. Environ Microbiol 12:3137–3149. https://doi.org/10.1111/j.1462-2920.2010.02286.x
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
Di HJ, Cameron KC, Shen JP, Winefield CS, O'Callaghan M, Bowatte S, He JZ (2010) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol 72:386–394. https://doi.org/10.1111/j.1574-6941.2010.00861.x
Dytczak MA, Londry KL, Oleszkiewicz JA (2008) Nitrifying genera in activated sludge may influence nitrification rates. Water Environ Res 80:388–396. https://doi.org/10.2175/106143007X221373
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
Ernest D, Osburn JEB (2020) Abundance and functional importance of complete ammonia-oxidizing bacteria (comammox) versus canonical nitrifiers in temperate forest soils. Soil Boil Biochem 145:107801–117804. https://doi.org/10.1016/j.soilbio.2020.107801
Gao SJ, Chang DN, Zou CQ, Cao WD, Gao JS, Huang J, Bai JS, Zeng NH, Rees RM, Thorup-Kristensen K (2018a) Archaea are the predominant and responsive ammonia oxidizing prokaryotes in a red paddy soil receiving green manures. Eur J Soil Biol 88:27–35. https://doi.org/10.1016/j.ejsobi.2018.05.008
Gao SJ, Cao WD, Zou CQ, Gao JS, Huang J, Bai JS, Zeng NH, Shimizu KY, Wright A, Dou FG (2018b) 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
Giguere AT, Taylor AE, Myrold DD, Bottomley PJ (2015) Nitrification responses of soil ammonia-oxidizing archaea and bacteria to ammonium concentrations. Soil Sci Soc Am J 79:1366–1374. https://doi.org/10.2136/sssaj2015.03.0107
Gleeson D, Müller C, Banerjee S, Ma W, Siciliano S, Murphy D (2010) Response of ammonia oxidizing archaea and bacteria to changing water filled pore space. Soil Boil Biochem 42:1888–1891. https://doi.org/10.1016/j.soilbio.2010.06.020
Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KWT, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010. https://doi.org/10.1126/science.1182570
Hati KM, Mandal KG, Misra AK, Ghosh PK, Bandyopadhyay KK (2006) Effect of inorganic fertilizer and farmyard manure on soil physical properties, root distribution, and water-use efficiency of soybean in Vertisols of central India. Bioresour Technol 97:2182–2188. https://doi.org/10.1016/j.biortech.2005.09.033
Hatzenpichler R, Lebedeva EV, 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. https://doi.org/10.1073/pnas.0708857105
He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di HJ (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. https://doi.org/10.1111/j.1462-2920.2007.01358.x
Hu HW, He JZ (2017) Comammox-a newly discovered nitrification process in the terrestrial nitrogen cycle. J Soils Sediments 17:1–9. https://doi.org/10.1007/s11368-017-1851-9
Javelle A, Thomas G, Marini AM, Krämer R, Merrick M (2005) In vivo functional characterization of the Escherichia coli ammonium channel AmtB: evidence for metabolic coupling of AmtB to glutamine synthetase. Biochem J 390:215–222. https://doi.org/10.1042/BJ20042094
Ke XB, Angle R, Lu YH, Conrad R (2013) Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil. Environ Microbiol 15:2275–2292. https://doi.org/10.1111/1462-2920.12098
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
Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529. https://doi.org/10.1146/annurev.micro.55.1.485
Kuypers MMM (2017) A fight for scraps of ammonia. Nature 549:162–163. https://doi.org/10.1038/549162a
Lawson CE, Lücker S (2018) Complete ammonia oxidation: an important control on nitrification in engineered ecosystems? Curr Opin Biotechnol 50:158–165. https://doi.org/10.1016/j.copbio.2018.01.015
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809. https://doi.org/10.1038/nature04983
Li YY, Chapman SJ, Nicol GW, Yao HY (2018) Nitrification and nitrifiers in acidic soils. Soil Boil Biochem 116:290–301. https://doi.org/10.1016/j.soilbio.2017.10.023
Li CY, Hu HW, Chen LQ, Chen DL, He JZ (2019) Comammox Nitrospira play an active role in nitrification of agricultural soils amended with nitrogen fertilizers. Soil Boil Biochem 138:107609. https://doi.org/10.1016/j.soilbio.2019.107609
Liang X, Radosevich M, Löffler F, Schaeffer SM, Zhuang J (2019) Impact of microbial iron oxide reduction on the transport of diffusible tracers and non-diffusible nanoparticles in soils. Chemosphere 220(3):91–402. https://doi.org/10.1016/j.chemosphere.2018.12.165
Lily P, Alicia MC, Mary M, Fuensanta GO (2018) Restoration of nitrogen cycling community in grapevine soil by a decade of organic fertilization. Soil Tillage Res 179:11–19. https://doi.org/10.1016/j.still.2018.01.007
Ling J, Lin XC, Zhang YY, Zhou WG, Yang QS, Lin LY, Zeng SQ, Zhang Y, Wang C, Ahmad M, Long LJ, Dong JD (2018) Community composition and transcriptional activity of ammonia-oxidizing prokaryotes of seagrass Thalassia hemprichii in coral reef ecosystems. Front Microbiol 9:7–19. https://doi.org/10.3389/fmicb.2018.00007
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 TL, Wang ZH, Wang SL, Zhao YP, Wright AL, Jiang XJ (2019) Responses of ammonia-oxidizers and comammox to different long-term fertilization regimes in a subtropical paddy soil. Eur J Soil Biol 93:103807. https://doi.org/10.1016/j.ejsobi.2019.103087
Lu SD, Sun YJ, Lu BY, Zheng DY, Xu SW (2020) Change of abundance and correlation of Nitrospira inopinata-like comammox and populations in nitrogen cycle during different seasons. Chemosphere 241:125098. https://doi.org/10.1016/j.chemosphere.2019.125098
Norton JN, Alzerreca JJ, Suwa Y, Klotz MG (2001) Diversity of ammonia monooxygenase operon in autotrophic ammonia-oxidizing bacteria. Arch Microbiol 177:139–149. https://doi.org/10.1007/s00203-001-0369-z
Palomo A, Pedersen AG, Fowler SJ, Dechesne A, Sicheritz PT, Smets BF (2018) Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira. ISME J 12:1779–1793. https://doi.org/10.1038/s41396-018-0083-3
Paul R, Wang YB, Alex FR, James SG, Fabrizio S, Morgan P, Yang FH, Joseph AK, Zhang H, George FW (2019) Comammox Nitrospira are the dominant ammonia oxidizers in a mainstream low dissolved oxygen nitrification reactor. Water Res 157:396–405. https://doi.org/10.1016/j.watres.2019.03.060
Pierre O, Melina K, Anja S, Christa S (2014) Variability of the transporter gene complement in ammonia-oxidizing archaea. Trends Microbiol 22:665–675. https://doi.org/10.1016/j.tim.2014.07.007
Pjevac P, Schauberger C, Poghosyan L, Herbold CW, van Kessel MAHJ, Daebeler A, Steinberger M, Jetten MSM, Lücker S, Wagner M, Daims H (2017) AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammox Nitrospira in the environment. Front Micribiol 8:1508. https://doi.org/10.3389/fmicb.2017.01508
Roy K, Ghosh D, DeBruyn JM, Dasgupta T, Wommack KE, Liang X, Wagner RE, Radosevich M (2020) Temporal dynamics of soil virus and bacterial populations in agricultural and early plant successional soils. Front Microbiol 11:1494. https://doi.org/10.3389/fmicb.2020.01494
Serita DF, Lee JH, Jerry MM, Johan S (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nat. Clim Chang 3:395–398. https://doi.org/10.1038/nclimate1796
Sessitsch A, Gyamfi S, Stralis-Pavese N, Weilharter A, Pfeifer U (2002) RNA isolation from soil for bacterial community and functional analysis: evaluation of different extraction and soil conservation protocols. J Microbiol Methods 51:171–179. https://doi.org/10.1016/S0167-7012(02)00065-9
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
Shi XZ, Hu HW, Wang JQ, He JZ, Wan XH, Huang ZQ (2018) Niche separation of comammox Nitrospira and canonical ammonia oxidizers in an acidic subtropical forest soil under long-term nitrogen deposition. Soil Boil Biochem 126:114–122. https://doi.org/10.1016/j.soilbio.2018.09.004
Sims A, Horton J, Gajaraj S, McIntosh S, Miles RJ, Mueller R, Reed R, Hu ZQ (2012) Temporal and spatial distributions of ammonia-oxidizing archaea and bacteria and their ratio as an indicator of oligotrophic conditions in natural wetlands. Water Res 46:4121–4129. https://doi.org/10.1016/j.watres.2012.05.007
Tao R, Steven AW, 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 Boil Biochem 114:20–30. https://doi.org/10.1016/j.soilbio.2017.06.027
Tkaczyk P, Mocek-Płóciniak A, Skowrońska M, Bednarek W, Kuśmierz S, Zawierucha E (2020) The mineral fertilizer-dependent chemical parameters of soil acidification under field condition. Sustainability 12:7165. https://doi.org/10.3390/su12177165
Van Kessel MAHJ, Speth DR, Albertsen M, Nielsen PH, Op den Camp HZM, Kartal B, Jetten MSM, Lücker S (2015) Complete nitrification by a single microorganism. Nature 528:555–559. https://doi.org/10.1038/nature16459
Wan QH, Wang SL, Zhao WY, Ma LH, Jia ZJ, Jiang XJ (2019) Vertical abundance variations of “incomplete ammonia oxidizers” and “comammox ” in purple paddy soil in Chongqing. Acta Microbiol Sin 59:291–302. https://doi.org/10.13343/j.cnki.wsxb.20180132
Wang SY, Wang Y, Feng XJ, Zhai LM, Zhu GB (2011) Quantitative analyses of ammonia oxidizing archaea and bacteria in the sediments of four nitrogen-rich wet lands in China. Appl Microbiol Biotechnol 90:779–787. https://doi.org/10.1007/s00253-011-3090-0
Wang JC, Zhang L, Lu Q, Waseem R, Huang QW, Shen QR (2014) Ammonia oxidizer abundance in paddy soil profile with different fertilizer regimes. Appl Soil Ecol 84:38–44. https://doi.org/10.1016/j.apsoil.2014.06.009
Wang Y, Ma L, Mao Y, Jiang X, Xia Y, Yu K, Li B, Zhang T (2017) Comammox in drinking water systems. Water Res 116:332–341. https://doi.org/10.1016/j.watres.2017.03.042
Wang M, Wang ZH, Shi XJ, Jiang XJ (2018) Long-term fertilization effects on the abundance of complete ammonia oxidizing bacteria (comammox Nitrospira ) in a neutral paddy soil. Chin J Envir Sci 39:4727–4734. https://doi.org/10.13227/j.hjkx.201802032
Wang ZH, Cao YQ, Barker XZ, Nicol GW, Wright AL, Jia ZJ, Jiang XJ (2019a) Comammox Nitrospira clade B contributes to nitrification in soil. Soil Boil Biochem 135:392–395. https://doi.org/10.1016/j.soilbio.2019.06.004
Wang JC, Wang JL, Rhodes G, He JZ, Ge Y (2019b) 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
Wang XM, Wang SY, Jiang YY, Zhou JM, Han C, Zhu GB (2020) Comammox bacterial abundance, activity, and contribution in agricultural rhizosphere soils. Sci Total Environ 727:138563. https://doi.org/10.1016/j.scitotenv.2020.138563
Wardle DA (1992) A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biol Rev 67:321–358. https://doi.org/10.1111/j.1469-185X.1992.tb00728.x
Weidinger K, Neuhäuser B, Gilch S, Ludewig U, Meyer O, Schmidt I (2007) Functional and physiological evidence for a Rhesus-type ammonia transporter in Nitrosomonas europaea. FEMS Microbiol Lett 273:260–267. https://doi.org/10.1111/j.1574-6968.2007.00805.x
Wu Y, Ke X, Hemandez M, Wang BZ, Dumont MG, Jia ZJ, Conrad R (2013) Autotrophic growth of bacterial and archaeal ammonia oxidizers in freshwater sediment microcosms incubated at different temperatures. Appl Environ Microbiol 79:3076–3084. https://doi.org/10.1128/AEM.00061-13
Xia WW, Zhang CX, Zeng XW, Feng YZ, Weng JH, Lin XG, Zhu JG, Xiong ZQ, Xu J, Cai ZC, Jia ZJ (2011) Autotrophic growth of nitrifying community in an agricultural soil. Microb Ecol 5:1226–1236. https://doi.org/10.1038/ismej.2011.5
Xu SY, Wang BZ, Li Y, Jiang DQ, Zhou YT, Ding AQ, Zong YX, Ling XT, Zhang SY, Lu HJ (2019) Ubiquity, diversity, and activity of comammox Nitrospira in agricultural soils. Sci Total Environ 706:135684. https://doi.org/10.1016/j.scitotenv.2019.135684
Yang K, Zhu JJ, Zhang M, Sun OJ (2010) Soil microbial biomass carbon and nitrogen in forest ecosystems of Northeast China: a comparison between natural secondary forest and larch plantation. J Plant Ecol 3:175–182. https://doi.org/10.1093/jpe/rtq022
Yang YD, Ren YF, Wang XQ, Hu YG, Wang ZM, Zemg ZH (2018) Ammonia-oxidizing archaea and bacteria responding differently to fertilizer type and irrigation frequency as revealed by Illumina Miseq sequencing. J Soils Sediments 18:1029–1040. https://doi.org/10.1007/s11368-017-1792-3
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 ZR, Huang GH, He SS, Zhou N, Wang MY, Dang CY, Wang JW, Zheng MS (2019) Abundance and community composition of comammox bacteria in different ecosystems by a universal primer set. Sci Total Environ 691:146–155. https://doi.org/10.1016/j.scitotenv.2019.07.131
Zheng MS, Wang MY, Zhao ZR, Zhou N, He SS, Liu SF, Wang JW, Wang XK (2019) Transcriptional activity and diversity of comammox bacteria as a previously overlooked ammonia oxidizing prokaryote in full-scale waste water treatment plants. Sci Total Environ 656:717–722. https://doi.org/10.1016/j.scitotenv.2018.11.435
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
Funding
This study has been funded by the Basic Scientific Research Project of University in Liaoning, Grant numbers: LSNZD201705; and the Natural Science Foundation of Liaoning Province, Grant numbers: 2019-MS-271; the National Natural Science Foundation of China, Grant number: 31101504.
Author information
Authors and Affiliations
Contributions
LL and WJ designed the project. LX and WF did the statistical analysis and wrote the manuscript. WF and MS did the soil DNA isolation and qPCR. All the authors agreed with the final version of the manuscript, contributed to interpreting the results, and revised the manuscript critically
Corresponding authors
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
The manuscript is approved by all the authors for participate.
Consent for publication
The manuscript is approved by all the authors for publication.
Competing interests
The authors declare no competing interests.
Additional information
Responsible editor: Yuan Ge
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOC 62 kb)
Rights and permissions
About this article
Cite this article
Wang, F., Liang, X., Ma, S. et al. Ammonia-oxidizing archaea are dominant over comammox in soil nitrification under long-term nitrogen fertilization. J Soils Sediments 21, 1800–1814 (2021). https://doi.org/10.1007/s11368-021-02897-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-021-02897-z