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Sensitivity of soil nitrifying and denitrifying microorganisms to nitrogen deposition on the Qinghai–Tibetan plateau

Sensitivity of soil nitrifying and denitrifying microorganisms to nitrogen deposition on the... −1 −1 Purpose: Nitrogen deposition at rate not more than 50 kg ha year is generally considered to stimulate soil nitrifying and denitrifying microorganisms via increases in soil nitrogen content. However, this phenomenon in alpine ecosystems remains largely untested. Methods: We conducted an 8-year nitrogen deposition experiment on the Qinghai–Tibetan Plateau, with four −1 −1 nitrogen deposition rates of 10 (atmospheric deposition), 20, 30, and 50 kg ha year . Results: The abundances of two nitrifying genes and four denitrifying genes and the N O emission rate initially increased and subsequently decreased as the nitrogen deposition rate increased. The observed decrease in these −1 −1 + indices at the rate of 50 kg ha year was caused by the toxicity of excessive NH . Conclusions: Our study demonstrates the vulnerability of alpine microorganisms under global changes. Keywords: Ammonium toxicity, Denitrification, N O, Nitrification, Nitrogen deposition, Qinghai–Tibetan plateau Over the past few decades, environmental changes Zhang et al. 2012), yet depresses the microbial denitrifi- caused by anthropogenic activity, such as climate warm- cation process (Gao et al. 2015). However, it is unclear ing and nitrogen (N) deposition, have played a large role whether the N deposition at rate not more than 50 kg −1 −1 in the disturbance of biological diversity and ecosystem ha year will also stimulate microbial nitrification and functions (Klein et al. 2004; Chen et al. 2013). However, denitrification in alpine ecosystems. the effects of N deposition on soil microbial communi- In this study, we conducted an 8-year (2007–2015) N ties and their underlying mechanisms within the alpine addition experiment to simulate N deposition in a area are yet to be fully understood. In many tropical and meadow ecosystem on the Qinghai–Tibetan Plateau, temperate ecosystems, N deposition at rate not more China (N 37° 37′, E 101° 19′). The Qinghai–Tibetan −1 −1 than 50 kg ha year stimulates the nitrification and de- Plateau has served as the roof of the world, the water nitrification of soil microbial communities by elevating tower of Asia, and the third pole of the Earth for 65 mil- the substrate contents of the two processes (Erickson lion years (Zheng et al. 1979; Wu and Yin 2002; Sun et al. 2001; Baer and Blair 2008). N deposition at rate > et al. 2012). The current N deposition rate at the Qing- −1 −1 50 kg ha year often continues to stimulate the micro- hai–Tibetan Plateau is recorded at approximately 10 kg −1 −1 bial nitrification process (Lehtovirta-Morley et al. 2011; ha year , with an increasing trend predicted for the next few decades (Lu and Tian 2007). The vegetation type is a typical Kobresia humilis meadow. The soils de- * Correspondence: xghan@ibcas.ac.cn; zhangximei@caas.cn veloped in the Kobresia meadow are Mat–Gryic Cambi- State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China sol (Fang et al. 2012). Four N addition rates were Key Laboratory of Dryland Agriculture, Ministry of Agriculture, Institute of −1 −1 applied (0, 10, 20, and 40 kg ha year ), and thus, the Environment and Sustainable Development in Agriculture, Chinese Academy actual total N deposition rates (anthropogenically added of Agricultural Sciences, Beijing 100081, China © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Xu et al. Annals of Microbiology (2021) 71:6 Page 2 of 5 rate + naturally deposited rate) were approximately 10, each treatment. In 2015, the abundances of two nitrify- −1 −1 20, 30, and 50 kg ha year , respectively. Two types of ing (AOA-amoA and AOB-amoA) and four denitrifying nitrogenous compounds, NH Cl and KNO , were added genes (nirS, nirK, narG, and nosZ) of soil microbial com- 4 3 for each of the latter three rates. Thus, there were seven munities were quantified using real-time PCR analysis. treatments, with three replicates (in three blocks) for The N O emission rate was quantified in situ via gas Fig. 1 Relationship between community size of a, b nitrifying and c–f denitrifying microorganisms, g N O emission rate, and nitrogen deposition rate. Error bars represent one standard error Xu et al. Annals of Microbiology (2021) 71:6 Page 3 of 5 −1 −1 chromatography (Wang and Wang 2003). In addition, 30 to 50 kg ha year ) led to a decline in the index plant community biomass and soil physicochemical indi- values, differing from results in the literature (Frey et al. ces (soil water content, pH, dissolved organic carbon 2004;Tian et al. 2014;Zeng et al. 2016). − + content, NO -N content, and NH -N content) were This unexpected decline in the indices was not attrib- 3 4 also measured (see Method S1). uted to aboveground plant biomass, soil water content, The abundances of the two nitrifying and four denitrify- and dissolved organic carbon content, as these variables ing genes initially increased and subsequently decreased as responded non-significantly to the N deposition rate, as the N deposition rate increased, with maximum values as- revealed by a two-way analysis of variance (Fig. 2a, c–d). −1 −1 sociated with 30 kg ha year (Fig. 1a–f). The N Oemis- Furthermore, as the N deposition rate increased from 30 −1 −1 sion rate exhibited a similar trend as that of the gene to 50 kg ha year , no consistent changes were ob- abundances, especially for the treatments of KNO served for soil pH under the addition of NH Cl and 3 4 addition (Fig. 1g). Specifically, an increase in the N depos- KNO (Fig. 2b). Specifically, soil pH levels decreased −1 −1 ition rate from 10 to 30 kg ha year resulted in a rise in with the addition of NH Cl, yet remained constant with the gene abundances and N O emission rate due to ele- the addition of KNO . Thus, soil pH was not an influen- 2 3 vated soil N content. This is consistent with tropical and cing factor for the observed decline in the seven indices. temperate ecosystems (Xie et al. 2018; Zhang et al. 2018). Similarly, soil NO -N content remained unchanged However, further increases in the N deposition rate (from under the addition of both NH Cl and KNO (Fig. 2e). 4 3 Fig. 2 Effects of N deposition rate on a soil water content, b soil pH, c dissolved organic carbon content, d aboveground plant biomass, e soil − + NO -N content, and f NH -N content. Error bars represent one standard error. For clarity, the statistical results with P > 0.05 are not shown 3 4 Xu et al. Annals of Microbiology (2021) 71:6 Page 4 of 5 In contrast, soil NH -N content increased consistently Authors’ contributions MX designed the research, carried out the experiment, and drafted the with the rise in nitrogen deposition under the addition manuscript. XZ improved the writing of the manuscript. All authors have of both NH Cl and KNO (Fig. 2f) and is thus identified 4 3 read and approved the final manuscript. as a likely cause of the reduced index values. Funding Excessive soil NH concentrations are able to change This research was supported by the National Key Research and Development the ion balance in plants through their uptake of cations Program (2016YFC0500702) and the China Major Science and Technology and thus are toxic to plants (Britto and Kronzucker Program for Water Pollution Control and Treatment (2017ZX07101003). 2002; Esteban et al. 2016). Moreover, soil microorgan- Availability of data and materials isms are considered to be less resistant to environmental All data analyzed during this study are included in this published article and pressures compared to higher plants (Zhang et al. 2015; its supplementary information files. Zhang et al. 2016). Hence, the excessive NH concen- −1 Ethics approval and consent to participate tration under the nitrogen deposition rate of 50 kg ha Not applicable. −1 year is likely to be toxic to soil microorganisms, lead- ing to the observed decline in the seven indices (Fig. 1). Consent for publication Not applicable. Note the addition of NO -N (in the form of KNO ) 3 3 −1 −1 from 30 to 50 kg ha year was associated with a slight Competing interests − + reduction in soil NO -N content, while NH -N con- 3 4 The authors declare that there is no competing interest. tent slightly increased (Fig. 2e, f). This implies that a − + Received: 1 December 2020 Accepted: 28 December 2020 large amount of NO -N was transformed into NH -N, 3 4 possibly driven by plants and/or microorganisms (Este- ban et al. 2016). Both the transformation of NO -N to References + + Baer SG, Blair JM (2008) Grassland establishment under varying resource NH -N and the toxicity of excessive NH for microor- 4 4 availability: a test of positive and negative feedback. Ecology 89:1859–1871 ganisms require further exploration to fully understand Britto DT, Kronzucker HJ (2002) NH4+ toxicity in higher plants: a critical review. J the mechanisms. Plant Physiol 159:567–584 Chen H, Zhu QA, Peng CH, Wu N, Wang YF, Fang XQ, Gao YH, Zhu D, Yang G, In summary, N deposition at rate not more than 50 kg Tian JQ, Kang XM, Piao SL, Ouyang H, Xiang WH, Luo ZB, Jiang H, Song XZ, −1 −1 ha year may either stimulate nitrifying and denitrifying Zhang Y, Yu GR, Zhao XQ, Gong P, Yao TD, Wu JH (2013) The impacts of microorganisms through increases in soil N content or de- climate change and human activities on biogeochemical cycles on the Qinghai-Tibetan plateau. Glob Chang Biol 19:2940–2955 press these microorganisms via NH toxicity. In some Dupre C, Stevens CJ, Ranke T, Bleeker A, Peppler-Lisbach C, Gowing DJG, Dise NB, tropical and temperate ecosystems, many microorganisms Dorland E, Bobbink R, Diekmann M (2010) Changes in species richness and are resistant to NH toxicity, thus exhibiting a net posi- composition in European acidic grasslands over the past 70 years: the contribution of cumulative atmospheric nitrogen deposition. Glob Chang tive response to low deposition rates (Ning et al. 2015; Biol 16:344–357 Tian et al. 2018). In contrast, microorganisms found in al- Erickson H, Keller M, Davidson EA (2001) Nitrogen oxide fluxes and nitrogen pine ecosystems do not present such a resistance to NH cycling during postagricultural succession and forest fertilization in the humid tropics. Ecosystems 4:67–84 toxicity, highlighting the vulnerability of microorganisms Esteban R, Ariz I, Cruz C, Moran JF (2016) Review: mechanisms of ammonium in such unique ecosystems. Moreover, for other types of toxicity and the quest for tolerance. Plant Sci 248:92–101 ecosystems, N deposition is observed to have a cumulative Fang HJ, Cheng SL, Yu GR, Zheng JJ, Zhang PL, Xu MJ, Li YN, Yang XM (2012) Responses of CO efflux from an alpine meadow soil on the Qinghai Tibetan effect (Dupre et al. 2010). Thus, it is also important to plateau to multi-form and low-level N addition. Plant and Soil 351:177–190 identify whether N deposition rates at rate not more than Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment −1 −1 30 kg ha year can cause a net negative effect on micro- affects the structure and function of the soil microbial community in temperate hardwood and pine forests. Forest Ecol Manag 196:159–171 organisms for longer treatments. A further key point is to Gao WL, Yang H, Kou L, Li SG (2015) Effects of nitrogen deposition and determine whether the relationship observed on the Qing- fertilization on N transformations in forest soils: a review. J Soil Sediment 15: hai–Tibetan Plateau between the community size of nitri- 863–879 Klein JA, Harte J, Zhao XQ (2004) Experimental warming causes large and rapid fying and denitrifying microorganisms and nitrogen species loss, dampened by simulated grazing, on the Tibetan plateau. Ecol −1 −1 deposition at rate not more than 50 kg ha year also ap- Lett 7:1170–1179 plies to other alpine ecosystems in the world. Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. P Natl Acad Sci USA 108:15892–15897 Lu CQ, Tian HQ (2007) Spatial and temporal patterns of nitrogen deposition in Supplementary Information China: synthesis of observational data. J Geophys Res 112, D22S05. https:// The online version contains supplementary material available at https://doi. doi.org/10.1029/2006JD007990 org/10.1186/s13213-020-01619-z. Ning QS, Gu Q, Shen JP, Lv XT, Yang JJ, Zhang XM, He JZ, Huang JH, Wang H, Xu ZH, Han XG (2015) Effects of nitrogen deposition rates and frequencies on Additional file 1: Methods the abundance of soil nitrogen-related functional genes in temperate grassland of northern China. J Soil Sediment 15:694–704 Sun H, Zheng D, Yao T, Zhang Y (2012) Protection and construction of the Acknowledgements national ecological security shelter zone on Tibetan plateau. Acta Geograph Not applicable. Sin 67:3–12 Chinese with English abstract Xu et al. Annals of Microbiology (2021) 71:6 Page 5 of 5 Tian D, Du EZ, Jiang L, Ma SH, Zeng WJ, Zou AL, Feng CY, Xu LC, Xing AJ, Wang W, Zheng CY, Ji CJ, Shen HH, Fang JY (2018) Responses of forest ecosystems to increasing N deposition in China: a critical review. Environ Pollut 243:75–86 Tian XF, Hu HW, Ding Q, Song MH, Xu XL, Zheng Y, Guo LD (2014) Influence of nitrogen fertilization on soil ammonia oxidizer and denitrifier abundance, microbial biomass, and enzyme activities in an alpine meadow. Biol Fertil Soils 50:703–713 Wang YS, Wang YH (2003) Quick measurement of CH ,CO and N O emissions 4 2 2 from a short-plant ecosystem. Adv Atmos Sci 20:842–844 Wu SH, Yin YH (2002) Climatic trends over the Tibetan plateau during 1971-2000. In: The editorial Committee of the eco-environment of nature reserves in the three Rivers’ source region (ECENRTR) (Eds), the eco-environment of nature reserves in the three Rivers’ source. Qinghai People’s Press, Xining, pp 179–180 Xie DN, Si GY, Zhang T, Mulder J, Duan L (2018) Nitrogen deposition increases N O emission from an N-saturated subtropical forest in Southwest China. Environ Pollut 243:1818–1824 Zeng J, Liu XJ, Song L, Lin XG, Zhang HY, Shen CC, Chu HY (2016) Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol Biochem 92:41–49 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 Zhang TA, Chen HYH, Ruan HH (2018) Global negative effects of nitrogen deposition on soil microbes. ISME J 12:1817–1825 Zhang XM, Johnston ER, Liu W, Li LH, Han XG (2016) Environmental changes affect the assembly of soil bacterial community primarily by mediating stochastic processes. Glob Chang Biol 22:198–207 Zhang XM, Liu W, Zhang GM, Jiang L, Han XG (2015) Mechanisms of soil acidification reducing bacterial diversity. Soil Biol Biochem 81:275–281 Zheng D, Zhang R, Yang Q (1979) On the natural zonation in the Qinghai-Xizang plateau. Acta Geograph Sin 1–11(Chinese with English abstract):34 Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Annals of Microbiology Springer Journals

Sensitivity of soil nitrifying and denitrifying microorganisms to nitrogen deposition on the Qinghai–Tibetan plateau

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Abstract

−1 −1 Purpose: Nitrogen deposition at rate not more than 50 kg ha year is generally considered to stimulate soil nitrifying and denitrifying microorganisms via increases in soil nitrogen content. However, this phenomenon in alpine ecosystems remains largely untested. Methods: We conducted an 8-year nitrogen deposition experiment on the Qinghai–Tibetan Plateau, with four −1 −1 nitrogen deposition rates of 10 (atmospheric deposition), 20, 30, and 50 kg ha year . Results: The abundances of two nitrifying genes and four denitrifying genes and the N O emission rate initially increased and subsequently decreased as the nitrogen deposition rate increased. The observed decrease in these −1 −1 + indices at the rate of 50 kg ha year was caused by the toxicity of excessive NH . Conclusions: Our study demonstrates the vulnerability of alpine microorganisms under global changes. Keywords: Ammonium toxicity, Denitrification, N O, Nitrification, Nitrogen deposition, Qinghai–Tibetan plateau Over the past few decades, environmental changes Zhang et al. 2012), yet depresses the microbial denitrifi- caused by anthropogenic activity, such as climate warm- cation process (Gao et al. 2015). However, it is unclear ing and nitrogen (N) deposition, have played a large role whether the N deposition at rate not more than 50 kg −1 −1 in the disturbance of biological diversity and ecosystem ha year will also stimulate microbial nitrification and functions (Klein et al. 2004; Chen et al. 2013). However, denitrification in alpine ecosystems. the effects of N deposition on soil microbial communi- In this study, we conducted an 8-year (2007–2015) N ties and their underlying mechanisms within the alpine addition experiment to simulate N deposition in a area are yet to be fully understood. In many tropical and meadow ecosystem on the Qinghai–Tibetan Plateau, temperate ecosystems, N deposition at rate not more China (N 37° 37′, E 101° 19′). The Qinghai–Tibetan −1 −1 than 50 kg ha year stimulates the nitrification and de- Plateau has served as the roof of the world, the water nitrification of soil microbial communities by elevating tower of Asia, and the third pole of the Earth for 65 mil- the substrate contents of the two processes (Erickson lion years (Zheng et al. 1979; Wu and Yin 2002; Sun et al. 2001; Baer and Blair 2008). N deposition at rate > et al. 2012). The current N deposition rate at the Qing- −1 −1 50 kg ha year often continues to stimulate the micro- hai–Tibetan Plateau is recorded at approximately 10 kg −1 −1 bial nitrification process (Lehtovirta-Morley et al. 2011; ha year , with an increasing trend predicted for the next few decades (Lu and Tian 2007). The vegetation type is a typical Kobresia humilis meadow. The soils de- * Correspondence: xghan@ibcas.ac.cn; zhangximei@caas.cn veloped in the Kobresia meadow are Mat–Gryic Cambi- State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China sol (Fang et al. 2012). Four N addition rates were Key Laboratory of Dryland Agriculture, Ministry of Agriculture, Institute of −1 −1 applied (0, 10, 20, and 40 kg ha year ), and thus, the Environment and Sustainable Development in Agriculture, Chinese Academy actual total N deposition rates (anthropogenically added of Agricultural Sciences, Beijing 100081, China © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Xu et al. Annals of Microbiology (2021) 71:6 Page 2 of 5 rate + naturally deposited rate) were approximately 10, each treatment. In 2015, the abundances of two nitrify- −1 −1 20, 30, and 50 kg ha year , respectively. Two types of ing (AOA-amoA and AOB-amoA) and four denitrifying nitrogenous compounds, NH Cl and KNO , were added genes (nirS, nirK, narG, and nosZ) of soil microbial com- 4 3 for each of the latter three rates. Thus, there were seven munities were quantified using real-time PCR analysis. treatments, with three replicates (in three blocks) for The N O emission rate was quantified in situ via gas Fig. 1 Relationship between community size of a, b nitrifying and c–f denitrifying microorganisms, g N O emission rate, and nitrogen deposition rate. Error bars represent one standard error Xu et al. Annals of Microbiology (2021) 71:6 Page 3 of 5 −1 −1 chromatography (Wang and Wang 2003). In addition, 30 to 50 kg ha year ) led to a decline in the index plant community biomass and soil physicochemical indi- values, differing from results in the literature (Frey et al. ces (soil water content, pH, dissolved organic carbon 2004;Tian et al. 2014;Zeng et al. 2016). − + content, NO -N content, and NH -N content) were This unexpected decline in the indices was not attrib- 3 4 also measured (see Method S1). uted to aboveground plant biomass, soil water content, The abundances of the two nitrifying and four denitrify- and dissolved organic carbon content, as these variables ing genes initially increased and subsequently decreased as responded non-significantly to the N deposition rate, as the N deposition rate increased, with maximum values as- revealed by a two-way analysis of variance (Fig. 2a, c–d). −1 −1 sociated with 30 kg ha year (Fig. 1a–f). The N Oemis- Furthermore, as the N deposition rate increased from 30 −1 −1 sion rate exhibited a similar trend as that of the gene to 50 kg ha year , no consistent changes were ob- abundances, especially for the treatments of KNO served for soil pH under the addition of NH Cl and 3 4 addition (Fig. 1g). Specifically, an increase in the N depos- KNO (Fig. 2b). Specifically, soil pH levels decreased −1 −1 ition rate from 10 to 30 kg ha year resulted in a rise in with the addition of NH Cl, yet remained constant with the gene abundances and N O emission rate due to ele- the addition of KNO . Thus, soil pH was not an influen- 2 3 vated soil N content. This is consistent with tropical and cing factor for the observed decline in the seven indices. temperate ecosystems (Xie et al. 2018; Zhang et al. 2018). Similarly, soil NO -N content remained unchanged However, further increases in the N deposition rate (from under the addition of both NH Cl and KNO (Fig. 2e). 4 3 Fig. 2 Effects of N deposition rate on a soil water content, b soil pH, c dissolved organic carbon content, d aboveground plant biomass, e soil − + NO -N content, and f NH -N content. Error bars represent one standard error. For clarity, the statistical results with P > 0.05 are not shown 3 4 Xu et al. Annals of Microbiology (2021) 71:6 Page 4 of 5 In contrast, soil NH -N content increased consistently Authors’ contributions MX designed the research, carried out the experiment, and drafted the with the rise in nitrogen deposition under the addition manuscript. XZ improved the writing of the manuscript. All authors have of both NH Cl and KNO (Fig. 2f) and is thus identified 4 3 read and approved the final manuscript. as a likely cause of the reduced index values. Funding Excessive soil NH concentrations are able to change This research was supported by the National Key Research and Development the ion balance in plants through their uptake of cations Program (2016YFC0500702) and the China Major Science and Technology and thus are toxic to plants (Britto and Kronzucker Program for Water Pollution Control and Treatment (2017ZX07101003). 2002; Esteban et al. 2016). Moreover, soil microorgan- Availability of data and materials isms are considered to be less resistant to environmental All data analyzed during this study are included in this published article and pressures compared to higher plants (Zhang et al. 2015; its supplementary information files. Zhang et al. 2016). Hence, the excessive NH concen- −1 Ethics approval and consent to participate tration under the nitrogen deposition rate of 50 kg ha Not applicable. −1 year is likely to be toxic to soil microorganisms, lead- ing to the observed decline in the seven indices (Fig. 1). Consent for publication Not applicable. Note the addition of NO -N (in the form of KNO ) 3 3 −1 −1 from 30 to 50 kg ha year was associated with a slight Competing interests − + reduction in soil NO -N content, while NH -N con- 3 4 The authors declare that there is no competing interest. tent slightly increased (Fig. 2e, f). This implies that a − + Received: 1 December 2020 Accepted: 28 December 2020 large amount of NO -N was transformed into NH -N, 3 4 possibly driven by plants and/or microorganisms (Este- ban et al. 2016). Both the transformation of NO -N to References + + Baer SG, Blair JM (2008) Grassland establishment under varying resource NH -N and the toxicity of excessive NH for microor- 4 4 availability: a test of positive and negative feedback. Ecology 89:1859–1871 ganisms require further exploration to fully understand Britto DT, Kronzucker HJ (2002) NH4+ toxicity in higher plants: a critical review. J the mechanisms. Plant Physiol 159:567–584 Chen H, Zhu QA, Peng CH, Wu N, Wang YF, Fang XQ, Gao YH, Zhu D, Yang G, In summary, N deposition at rate not more than 50 kg Tian JQ, Kang XM, Piao SL, Ouyang H, Xiang WH, Luo ZB, Jiang H, Song XZ, −1 −1 ha year may either stimulate nitrifying and denitrifying Zhang Y, Yu GR, Zhao XQ, Gong P, Yao TD, Wu JH (2013) The impacts of microorganisms through increases in soil N content or de- climate change and human activities on biogeochemical cycles on the Qinghai-Tibetan plateau. Glob Chang Biol 19:2940–2955 press these microorganisms via NH toxicity. In some Dupre C, Stevens CJ, Ranke T, Bleeker A, Peppler-Lisbach C, Gowing DJG, Dise NB, tropical and temperate ecosystems, many microorganisms Dorland E, Bobbink R, Diekmann M (2010) Changes in species richness and are resistant to NH toxicity, thus exhibiting a net posi- composition in European acidic grasslands over the past 70 years: the contribution of cumulative atmospheric nitrogen deposition. Glob Chang tive response to low deposition rates (Ning et al. 2015; Biol 16:344–357 Tian et al. 2018). In contrast, microorganisms found in al- Erickson H, Keller M, Davidson EA (2001) Nitrogen oxide fluxes and nitrogen pine ecosystems do not present such a resistance to NH cycling during postagricultural succession and forest fertilization in the humid tropics. Ecosystems 4:67–84 toxicity, highlighting the vulnerability of microorganisms Esteban R, Ariz I, Cruz C, Moran JF (2016) Review: mechanisms of ammonium in such unique ecosystems. Moreover, for other types of toxicity and the quest for tolerance. Plant Sci 248:92–101 ecosystems, N deposition is observed to have a cumulative Fang HJ, Cheng SL, Yu GR, Zheng JJ, Zhang PL, Xu MJ, Li YN, Yang XM (2012) Responses of CO efflux from an alpine meadow soil on the Qinghai Tibetan effect (Dupre et al. 2010). Thus, it is also important to plateau to multi-form and low-level N addition. Plant and Soil 351:177–190 identify whether N deposition rates at rate not more than Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment −1 −1 30 kg ha year can cause a net negative effect on micro- affects the structure and function of the soil microbial community in temperate hardwood and pine forests. Forest Ecol Manag 196:159–171 organisms for longer treatments. A further key point is to Gao WL, Yang H, Kou L, Li SG (2015) Effects of nitrogen deposition and determine whether the relationship observed on the Qing- fertilization on N transformations in forest soils: a review. J Soil Sediment 15: hai–Tibetan Plateau between the community size of nitri- 863–879 Klein JA, Harte J, Zhao XQ (2004) Experimental warming causes large and rapid fying and denitrifying microorganisms and nitrogen species loss, dampened by simulated grazing, on the Tibetan plateau. Ecol −1 −1 deposition at rate not more than 50 kg ha year also ap- Lett 7:1170–1179 plies to other alpine ecosystems in the world. Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. P Natl Acad Sci USA 108:15892–15897 Lu CQ, Tian HQ (2007) Spatial and temporal patterns of nitrogen deposition in Supplementary Information China: synthesis of observational data. J Geophys Res 112, D22S05. https:// The online version contains supplementary material available at https://doi. doi.org/10.1029/2006JD007990 org/10.1186/s13213-020-01619-z. Ning QS, Gu Q, Shen JP, Lv XT, Yang JJ, Zhang XM, He JZ, Huang JH, Wang H, Xu ZH, Han XG (2015) Effects of nitrogen deposition rates and frequencies on Additional file 1: Methods the abundance of soil nitrogen-related functional genes in temperate grassland of northern China. J Soil Sediment 15:694–704 Sun H, Zheng D, Yao T, Zhang Y (2012) Protection and construction of the Acknowledgements national ecological security shelter zone on Tibetan plateau. Acta Geograph Not applicable. Sin 67:3–12 Chinese with English abstract Xu et al. Annals of Microbiology (2021) 71:6 Page 5 of 5 Tian D, Du EZ, Jiang L, Ma SH, Zeng WJ, Zou AL, Feng CY, Xu LC, Xing AJ, Wang W, Zheng CY, Ji CJ, Shen HH, Fang JY (2018) Responses of forest ecosystems to increasing N deposition in China: a critical review. Environ Pollut 243:75–86 Tian XF, Hu HW, Ding Q, Song MH, Xu XL, Zheng Y, Guo LD (2014) Influence of nitrogen fertilization on soil ammonia oxidizer and denitrifier abundance, microbial biomass, and enzyme activities in an alpine meadow. Biol Fertil Soils 50:703–713 Wang YS, Wang YH (2003) Quick measurement of CH ,CO and N O emissions 4 2 2 from a short-plant ecosystem. Adv Atmos Sci 20:842–844 Wu SH, Yin YH (2002) Climatic trends over the Tibetan plateau during 1971-2000. In: The editorial Committee of the eco-environment of nature reserves in the three Rivers’ source region (ECENRTR) (Eds), the eco-environment of nature reserves in the three Rivers’ source. Qinghai People’s Press, Xining, pp 179–180 Xie DN, Si GY, Zhang T, Mulder J, Duan L (2018) Nitrogen deposition increases N O emission from an N-saturated subtropical forest in Southwest China. Environ Pollut 243:1818–1824 Zeng J, Liu XJ, Song L, Lin XG, Zhang HY, Shen CC, Chu HY (2016) Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol Biochem 92:41–49 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 Zhang TA, Chen HYH, Ruan HH (2018) Global negative effects of nitrogen deposition on soil microbes. ISME J 12:1817–1825 Zhang XM, Johnston ER, Liu W, Li LH, Han XG (2016) Environmental changes affect the assembly of soil bacterial community primarily by mediating stochastic processes. Glob Chang Biol 22:198–207 Zhang XM, Liu W, Zhang GM, Jiang L, Han XG (2015) Mechanisms of soil acidification reducing bacterial diversity. Soil Biol Biochem 81:275–281 Zheng D, Zhang R, Yang Q (1979) On the natural zonation in the Qinghai-Xizang plateau. Acta Geograph Sin 1–11(Chinese with English abstract):34 Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Annals of MicrobiologySpringer Journals

Published: Jan 22, 2021

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