Soil pH and phosphorus drive the canonical nitrifiers and comammox Nitrospira communities in citrus orchards with different cultivation ages

Haiyang Liu , Zhikang Tao , Hongen Liu , Wei Xu , Yuanyi Qin , Zhaojun Nie , Wenfeng Tan

Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (2) : 230199

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Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (2) : 230199 DOI: 10.1007/s42832-023-0199-x
RESEARCH ARTICLE
RESEARCH ARTICLE

Soil pH and phosphorus drive the canonical nitrifiers and comammox Nitrospira communities in citrus orchards with different cultivation ages

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Abstract

● Comammox Nitrospira clade A and B showed contrasting responses to citrus planting.

● 54d9-like AOA and Nitrobacter -NOB dominated in the 5Y and 10Y soils.

Nitrososphaera -like AOA and Nitrospira -like NOB dominated in the 20Y and 30Y soils.

● Soil pH and P content were the major factors shaping nitrifying communities.

Ammonia oxidizing bacteria (AOB), archaea (AOA), nitrite oxidizing bacteria (NOB) and complete ammonia oxidizers (comammox Nitrospira) are major players in nitrification. However, the distribution and community composition of these nitrifiers in intensively managed orchard soils are still unclear. Here, we chose soil samples from citrus orchards that had been planted for 5 years (5Y), 10 years (10Y), 20 years (20Y) and 30 years (30Y), and adjacent woodland (NF), to study the response of nitrifiers to long-term citrus plantation using quantitative PCR and MiSeq sequencing. Our results revealed that the ammonia and nitrite oxidation potentials in the 5Y soil were the highest, and decreased with increasing plantation age. The AOB abundance was higher in 5Y and 10Y soils than that in 20Y and 30Y soils. The abundance of comammox Nitrospira clade A increased with increasing plantation age, but comammox Nitrospira clade B showed the opposite tendency. MiSeq sequencing results indicated 54d9-like AOA and Nitrobacter-NOB were the dominant populations in 5Y and 10Y soils whereas Nitrososphaera-like AOA and Nitrospira-like NOB dominated in 20Y and 30Y soils. The conversion of woodland to orchard resulted in a significant shift of AOB population from Nitrosospira cluster 3a.1 to cluster 3a.2. In addition, soil pH and phosphorus (P) content were the major factors shaping nitrifying communities. This work suggested citrus plantation altered the distribution of community composition of nitrifiers by affecting soil chemical and physical conditions, and comammox Nitrospira could potentially play an important role in nitrification in intensive managed orchard soils.

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Keywords

AOB / AOA / comammox Nitrospira / NOB / soil pH / phosphorus content

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Haiyang Liu, Zhikang Tao, Hongen Liu, Wei Xu, Yuanyi Qin, Zhaojun Nie, Wenfeng Tan. Soil pH and phosphorus drive the canonical nitrifiers and comammox Nitrospira communities in citrus orchards with different cultivation ages. Soil Ecology Letters, 2024, 6(2): 230199 DOI:10.1007/s42832-023-0199-x

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References

[1]

Attard, E., Poly, F., Commeaux, C., Laurent, F., Roux, X.L., 2010. Shifts between Nitrospira- and Nitrobacter-like nitrite oxidizers underlie the response of soil potential nitrite oxidation to changes in tillage practices. Environmental Microbiology12, 315–326.

[2]

Avrahami, S., Conrad, R., Braker, G., 2002. Effect of soil ammonium concentration on N2O release and on the community structure of ammonia oxidizers and denitrifiers. Applied and Environmental Microbiology68, 5685–5692.

[3]

Bahram, M., Hildebrand, F., Forslund, S.K., Anderson, J.L., Soudzilovskaia, N.A., Bodegom, P.M., Bengtsson-Palme, J., Anslan, S., Coelho, L.P., Harend, H., Huerta-Cepas, J., Medema, M.H., Maltz, M.R., Mundra, S., Olsson, P.A., Pent, M., Põlme, S., Sunagawa, S., Rryberg, M., Tedersoo, L., Bork, P., 2018. Structure and function of the global topsoil microbiome. Nature560, 233–237.

[4]

Bartosch, S., Hartwig, C., Bock, E.S., 2002. Immunological detection of Nitrospira-like bacteria in various Soils. Microbial Ecology43, 26–33.

[5]

Bauhus, J., Khanna, P.K., 1994. Carbon and nitrogen turnover in two acid forest soils of southeast Australia as affected by phosphorus addition and drying and rewetting cycles. Biology and Fertility of Soils17, 212–218.

[6]

Bertagnolli, A.D., Meinhardt, K.A., Pannu, M., Brown, S., Strand, S., Fransen, S.C., Stahl, D.A., 2015. Influence of edaphic and management factors on the diversity and abundance of ammonia‐oxidizing thaumarchaeota and bacteria in soils of bioenergy crop cultivars. Environmental Microbiology Reports7, 312–320.

[7]

Bortoluzzi, E.C., Moterle, D.F., Rheinheimer, D., Casali, C.A., Melo, G.W., Brunetto, G., 2012. Mineralogical changes caused by grape production in a regosol from subtropical Brazilian climate. Journal of Soils and Sediments12, 854–862.

[8]

Cao, S., Zhou, Y., Zhou, Y., Zhou, X., Zhou, W., 2021. Soil organic carbon and soil aggregate stability associated with aggregate fractions in a chronosequence of citrus orchards plantations. Journal of Environmental Management293, 112847.

[9]

Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods7, 335–336.

[10]

Daims, H., Lebedeva, E.V., Pjevac, P., Han, P., Herbold, C., Albertsen, M., Jehmlich, N., Palatinszky, M., Vierheilig, J., Bulaev, A., Kirkegaard, R.H., von Bergen, M., Rattei, T., Bendinger, B., Nielsen, P.H., Wagner, M., 2015. Complete nitrification by Nitrospira bacteria. Nature528, 504–509.

[11]

De Boer, W., Kowalchuk, G.A., 2001. Nitrification in acid soils: micro-organisms and mechanisms. Soil Biology & Biochemistry33, 853–866.

[12]

Di, H.J., Cameron, K.C., Shen, J.P., Winefield, C.S., O’Callaghan, M., Bowatte, S., He, J.Z., 2009. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nature Geoscience2, 621–624.

[13]

Di, H.J., Cameron, K.C., Shen, J.P., Winefield, C.S., O’Callaghan, M., Bowatte, S., He, J.Z., 2010. Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiology Ecology72, 386–394.

[14]

Dick, W.A., Blevins, R.L., Frye, W.W., Peters, S.E., Christenson, D.R., Pierce, F.J., Vitosh, M.L., 1998. Impacts of agricultural management practices on C sequestration in forest-derived soils of the eastern Corn Belt. Soil & Tillage Research47, 235–244.

[15]

Dong, X., Zhang, J., Qiu, H., Zhang, H., Luo, C., Deng, D., Shen, Q., Jia, Z., 2019. Chronic nitrogen fertilization modulates competitive interactions among microbial ammonia oxidizers in a loess soil. Pedosphere29, 24–33.

[16]

Edgar, R.C., 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England)26, 2460–2461.

[17]

FAO (Food and Agricultural Organization of the United Nations), 2021. FAOSTAT. fao.org

[18]

Garcia-Franco, N., Wiesmeier, M., Colocho Hurtarte, L.C., Fella, F., Martínez-Mena, M., Almagro, M., Martínez, E.G., Kögel-Knabner, I., 2021. Pruning residues incorporation and reduced tillage improve soil organic matter stabilization and structure of salt-affected soils in a semi-arid Citrus tree orchard. Soil & Tillage Research213, 105129.

[19]

Gruber, N., Galloway, J.N., 2008. An Earth-system perspective of the global nitrogen cycle. Nature451, 293–296.

[20]

Gubry-Rangin, C., Hai, B., Quince, C., Engel, M., Thomson, B.C., James, P., Schloter, M., Griffiths, R.I., Prosser, J.I., Nicol, G.W., 2011. Niche specialization of terrestrial archaeal ammonia oxidizers. Proceedings of the National Academy of Sciences of the United States of America108, 21206–21211.

[21]

Guo, J., Ling, N., Chen, H., Zhu, C., Kong, Y., Wang, M., Shen, Q., Guo, S., 2017. Distinct drivers of activity, abundance, diversity and composition of ammonia-oxidizers: evidence from a long-term field experiment. Soil Biology & Biochemistry115, 403–414.

[22]

Guo, J.H., Liu, X.J., Zhang, Y., Shen, J.L., Han, W.X., Zhang, W.F., Christie, P., Goulding, K.W., Vitousek, P.M., Zhang, F.S., 2010. Significant acidification in major Chinese croplands. Science327, 1008–1010.

[23]

Han, S., Zeng, L., Luo, X., Xiong, X., Wen, S., Wang, B., Chen, W., Huang, Q., 2018. Shifts in Nitrobacter- and Nitrospira-like nitrite-oxidizing bacterial communities under long-term fertilization practices. Soil Biology & Biochemistry124, 118–125.

[24]

Harayama, S., Rekik, M., Ngai, K.L., Ornston, L.N., 1989. Physically associated enzymes produce and metabolize 2-hydroxy-2,4-dienoate, a chemically unstable intermediate formed in catechol metabolism via meta cleavage in Pseudomonas putida. Journal of Bacteriology171, 6251–6258.

[25]

He, J.Z., Shen, J.P., Zhang, L.M., Zhu, Y.G., Zheng, Y.M., Xu, M.G., Di, H., 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. Environmental Microbiology9, 3152–3152.

[26]

Hu, B.L., Liu, S., Wang, W., Shen, L.D., Lou, L.P., Liu, W.P., Tian, G., Xu, X., Zheng, P., 2014a. pH dominated niche segregation of ammonia-oxidising microorganisms in Chinese agricultural soils. FEMS Microbiology Ecology90, 290–299.

[27]

Hu, H.W., He, J.Z., 2017. Comammox—a newly discovered nitrification process in the terrestrial nitrogen cycle. Journal of Soils and Sediments17, 2709–2717.

[28]

Hu, H.W., Xu, Z.H., He, J.Z., 2014b Ammonia oxidizing archaea play a predominant role in acid soil nitrification. Advances in Agronomy 125, 261–302

[29]

Hu, H.W., Zhang, L.M., Dai, Y., Di, H.J., He, J.Z., 2013. pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. Journal of Soils and Sediments13, 1439–1449.

[30]

Hu, J., Zhao, Y., Yao, X., Wang, J., Zheng, P., Xi, C., Hu, B., 2021. Dominance of comammox Nitrospira in soil nitrification. Science of the Total Environment780, 146558.

[31]

Jiang, X., Hou, X., Zhou, X., Xin, X., Wright, A., Jia, Z., 2015. pH regulates key players of nitrification in paddy soils. Soil Biology & Biochemistry81, 9–16.

[32]

Ke, X., Angel, R., Lu, Y., Conrad, R., 2013. Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil. Environmental Microbiology15, 2275–2292.

[33]

Kim, J.G., Jung, M.Y., Park, S.J., Rijpstra, W.I., Sinninghe Damste, J.S., Madsen, E.L., Min, D., Kim, J.S., Kim, G.J., Rhee, S.K., 2012. Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I.1b from an agricultural soil. Environmental Microbiology 14, 1528–1543

[34]

Kits, K.D., Sedlacek, C.J., Lebedeva, E.V., Han, P., Bulaev, A., Pjevac, P., Daebeler, A., Romano, S., Albertsen, M., Stein, L.Y., Daims, H., Wagner, M., 2017. Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature549, 269–272.

[35]

Könneke, M., Bernhard, A.E., De, L., Walker, C.B., Waterbury, J.B., Stahl, D.A., 2005. Isolation of an autotrophic ammoniaoxidizing marine archaeon. Nature437, 543–546.

[36]

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 Microbiology Letters250, 33–38.

[37]

Laganière, J.R.M., Angers, D.A., Paré, D., 2010. Carbon accumulation in agricultural soils after afforestation: a meta-analysis. Global Change Biology16, 439–453.

[38]

Li, C., Hu, H.W., Chen, Q.L., Chen, D., He, J.Z., 2019a. Comammox Nitrospira play an active role in nitrification of agricultural soils amended with nitrogen fertilizers. Soil Biology & Biochemistry138, 107609.

[39]

Li, C., Hu, H.W., Chen, Q.L., Chen, D., He, J.Z., 2020. Niche differentiation of clade A comammox Nitrospira and canonical ammonia oxidizers in selected forest soils. Soil Biology & Biochemistry149, 107925.

[40]

Li, C., Hu, H.W., Chen, Q.L., Yan, Z.Z., Thi Nguyen, B.A., Chen, D., He, J.Z., 2021. Niche specialization of comammox Nitrospira clade A in terrestrial ecosystems. Soil Biology & Biochemistry156, 108231.

[41]

Li, Y., Chapman, S.J., Nicol, G.W., Yao, H., 2018. Nitrifcation and nitrifers in acidic soils. Soil Biology & Biochemistry116, 290–301.

[42]

Li, Y.J., Yang, M., Zhang, Z.Z., Li, W.L., Zhang, X.D., 2019b. An ecological research on potential for zero-growth of chemical fertilizer use in citrus production in China. Ekoloji28, 1049–1059.

[43]

Lin, Y., Ye, G., Ding, W., Hu, H.W., Zheng, Y., Fan, J., Wan, S., Duan, C., He, J.Z., 2020. Niche differentiation of comammox Nitrospira and canonical ammonia oxidizers in soil aggregate fractions following 27-year fertilizations. Agriculture, Ecosystems & Environment304, 107147.

[44]

Liu, H., Ding, Y., Zhang, Q., Liu, X., Xu, J., Li, Y., Di, H., 2019. Heterotrophic nitrification and denitrification are the main sources of nitrous oxide in two paddy soils. Plant and Soil445, 39–53.

[45]

Liu, H., Hu, H., Huang, X., Ge, T., Li, Y., Zhu, Z., Liu, X., Tan, W., Jia, Z., Di, H., Xu, J., Li, Y., 2021. Canonical ammonia oxidizers, rather than comammox Nitrospira, dominated autotrophic nitrification during the mineralization of organic substances in two paddy soils. Soil Biology & Biochemistry156, 108192.

[46]

Liu, H., Qin, S., Li, Y., Zhao, P., Nie, Z., Liu, H., 2023. Comammox Nitrospira and AOB communities are more sensitive than AOA community to different fertilization strategies in a fluvo-aquic soil. Agriculture, Ecosystems & Environment342, 108224.

[47]

Lu, L., Jia, Z., 2013. Urease gene-containing Archaea dominate autotrophic ammonia oxidation in two acid soils. Environmental Microbiology15, 1795–1809.

[48]

Luo, G., Sun, B., Li, L., Li, M., Liu, M., Zhu, Y., Guo, S., Ling, N., Shen, Q., 2019. Understanding how long-term organic amendments increase soil phosphatase activities: Insight into phoD- and phoC-harboring functional microbial populations. Soil Biology & Biochemistry139, 107632.

[49]

Nguyen, L., Broughton, K., Osanai, Y., Anderson, I.C., Bange, M.P., Tissue, D.T., Singh, B.K., 2019. Effects of elevated temperature and elevated CO2 on soil nitrification and ammonia-oxidizing microbial communities in field-grown crop. Science of the Total Environment675, 81–89.

[50]

Nicol, G.W., Leininger, S., Schleper, C., Prosser, J.I., 2008. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environmental Microbiology10, 2966–2978.

[51]

Norman, J.S., Barrett, J.E., 2014. Substrate and nutrient limitation of ammonia-oxidizing bacteria and archaea in temperate forest soil. Soil Biology & Biochemistry69, 141–146.

[52]

Norton, J.M., Stark, J.M., 2011. Regulation and measurement of nitrification in terrestrial systems. Methods in Enzymology486, 343–368.

[53]

Olsen, S.R., 1954. Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate. United States Department of Agriculture, Washington, D.C

[54]

Orellana, L.H., Chee-Sanford, J.C., Sanford, R.A., Loffler, F.E., Konstantinidis, K.T., 2018. Year-round shotgun metagenomes reveal stable microbial communities in agricultural soils and novel ammonia oxidizers responding to fertilization. Applied and Environmental Microbiology84, 01646–17.

[55]

Palomo, A., Pedersen, A.G., Fowler, S.J., Dechesne, A., Sicheritz-Ponten, T., Smets, B.F., 2018. Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira. ISME Journal12, 1779–1793.

[56]

Sakoula, D., Koch, H., Frank, J., Jetten, M.S.M., van Kessel, M., Lucker, S., 2021. Enrichment and physiological characterization of a novel comammox Nitrospira indicates ammonium inhibition of complete nitrification. ISME Journal15, 1010–1024.

[57]

Scarlett, K., Denman, S., Clark, D.R., Forster, J., Vanguelova, E., Brown, N., Whitby, C., 2021. Relationships between nitrogen cycling microbial community abundance and composition reveal the indirect effect of soil pH on oak decline. ISME Journal15, 623–635.

[58]

Schroder, J.L., Zhang, H., Girma, K., Raun, W.R., Penn, C.J., Payton, M.E., 2011. Soil acidification from long-term use of nitrogen fertilizers on winter wheat. Soil Science Society of America Journal75, 957–964.

[59]

Shen, J.P., Zhang, L.M., Zhu, Y.G., Zhang, J.B., He, J.Z., 2008. Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environmental Microbiology10, 1601–1611.

[60]

Shi, Z., Li, X., Zhang, L., Wang, Y., 2015. Impacts of farmland conversion to apple (Malus domestica) orchard on soil organic carbon stocks and enzyme activities in a semiarid loess region. Journal of Plant Nutrition and Soil Science178, 440–451.

[61]

Stempfhuber, B., Richter-Heitmann, T., Regan, K.M., Kölbl, A., Wüst, P.K., Marhan, S., Sikorski, J., Overmann, J., Friedrich, M.W., Kandeler, E., Schloter, M., 2016. Spatial interaction of archaeal ammonia-oxidizers and nitrite-oxidizing bacteria in an unfertilized grassland soil. Frontiers in Microbiology6, 1567.

[62]

Sterngren, A.E., Hallin, S., Bengtson, P., 2015. Archaeal ammonia oxidizers dominate in numbers, but bacteria drive gross nitrification in N-amended grassland soil. Frontiers in Microbiology6, 1350.

[63]

Stubner, S., 2002. Enumeration of 16S rDNA of Desulfotomaculum lineage 1 in rice field soil by real-time PCR with SybrGreen™ detection. Journal of Microbiological Methods50, 155–164.

[64]

Sun, R., Myrold, D.D., Wang, D., Guo, X., Chu, H., 2019. AOA and AOB communities respond differently to changes of soil pH under long-term fertilization. Soil Ecology Letters1, 126–135.

[65]

Takahashi, Y., Fujitani, H., Hirono, Y., Tago, K., Wang, Y., Hayatsu, M., Tsuneda, S., 2020. Enrichment of comammox and nitrite-oxidizing Nitrospira from acidic soils. Frontiers in Microbiology11, 1737.

[66]

Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729

[67]

Tao, L., Li, F.B., Liu, C.S., Feng, X.H., Gu, L.L., Wang, B.R., Wen, S.L., Xu, M.G., 2019. Mitigation of soil acidification through changes in soil mineralogy due to long-term fertilization in southern China. Catena174, 227–234.

[68]

Tzanakakis, V.A., Taylor, A.E., Bakken, L.R., Bottomley, P.J., Myrold, D.D., Dörsch, P., 2019. Relative activity of ammonia oxidizing archaea and bacteria determine nitrification-dependent N2O emissions in Oregon forest soils. Soil Biology & Biochemistry139, 107612.

[69]

van Kessel, M.A., Speth, D.R., Albertsen, M., Nielsen, P.H., Op den Camp, H.J., Kartal, B., Jetten, M.S., Lucker, S., 2015. Complete nitrification by a single microorganism. Nature528, 555–559.

[70]

Wagner, M., Loy, A., Nogueira, R., Purkhold, U., Lee, N., Daims, H., 2002. Microbial community composition and function in wastewater treatment plants. Antonie van Leeuwenhoek81, 665–680.

[71]

Wang, B., Zhao, J., Guo, Z., Ma, J., Xu, H., Jia, Z., 2015. Differential contributions of ammonia oxidizers and nitrite oxidizers to nitrification in four paddy soils. ISME Journal9, 1062–1075.

[72]

Wang, B., Zheng, Y., Huang, R., Zhou, X., Wang, D., He, Y., Jia, Z., 2014. Active ammonia oxidizers in an acidic soil are phylogenetically closely related to neutrophilic archaeon. Applied and Environmental Microbiology80, 1684–1691.

[73]

Wang, J., Wang, J., Rhodes, G., He, J.Z., Ge, Y., 2019a. 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. Science of the Total Environment668, 224–233.

[74]

Wang, X., Wang, S., Shi, G., Wang, W., Zhu, G., 2019b. Factors driving the distribution and role of AOA and AOB in Phragmites communis rhizosphere in riparian zone. Journal of Basic Microbiology59, 425–436.

[75]

Wang, Z., Meng, Y., Zhu-Barker, X., He, X., Horwath, W.R., Luo, H., Zhao, Y., Jiang, X., 2019c. Responses of nitrification and ammonia oxidizers to a range of background and adjusted pH in purple soils. Geoderma334, 9–14.

[76]

Weidinger, K., Neuhäuser, B., Gilch, S., Ludewig, U., Meyer, O., Schmidt, I., 2007. Functional and physiological evidence for a Rhesustype ammonia transporter in Nitrosomonas europaea. FEMS Microbiology Letters273, 260–267.

[77]

Xia, F., Wang, J.G., Zhu, T., Zou, B., Rhee, S.K., Quan, Z.X., 2018. Ubiquity and diversity of complete ammonia oxidizers (comammox). Applied and Environmental Microbiology84, 13–18.

[78]

Xia, W., Zhang, C., Zeng, X., Feng, Y., Weng, J., Lin, X., Zhu, J., Xiong, Z., Xu, J., Cai, Z., Jia, Z., 2011. Autotrophic growth of nitrifying community in an agricultural soil. ISME Journal5, 1226–1236.

[79]

Xu, S., Wang, B., Li, Y., Jiang, D., Zhou, Y., Ding, A., Zong, Y., Ling, X., Zhang, S., Lu, H., 2020. Ubiquity, diversity, and activity of comammox Nitrospira in agricultural soils. Science of the Total Environment706, 135684.

[80]

Yang, K., Luo, S., Hu, L., Chen, B., Xie, Z., Ma, B., Ma, W., Du, G., Ma, X., Le Roux, X., 2020. Responses of soil ammonia-oxidizing bacteria and archaea diversity to N, P and NP fertilization: Relationships with soil environmental variables and plant community diversity. Soil Biology & Biochemistry145, 107795.

[81]

Yang, X.D., Ni, K., Shi, Y.Z., Yi, X.Y., Zhang, Q.F., Fang, L., Ma, L.F., Ruan, J., 2018. Effects of long-term nitrogen application on soil acidification and solution chemistry of a tea plantation in China. Agriculture, Ecosystems & Environment252, 74–82.

[82]

Zeng, M., de Vries, W., Bonten, L.T., Zhu, Q., Hao, T., Liu, X., Xu, M., Shi, X., Zhang, F., Shen, J., 2017. Model-based analysis of the long-term effects of fertilization management on cropland soil acidification. Environmental Science & Technology51, 3843–3851.

[83]

Zhang, J., Müller, C., Zhu, T., Cai, C.Z., 2011. Heterotrophic nitrification is the predominant NO3 production mechanism in coniferous but not broad-leaf acid forest soil in subtropical China. Biology and Fertility of Soils55, 288–336.

[84]

Zhang, L.M., Hu, H.W., Shen, J.P., He, J.Z., 2012. Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME Journal6, 1032–1045.

[85]

Zhang, Q., Li, Y., He, Y., Liu, H., Dumont, M.G., Brookes, P.C., Xu, J., 2019. Nitrosospira cluster 3-like bacterial ammonia oxidizers and Nitrospira-like nitrite oxidizers dominate nitrification activity in acidic terrace paddy soils. Soil Biology & Biochemistry131, 229–237.

[86]

Zhang, Y., He, X., Liang, H., Zhao, J., Zhang, Y., Xu, C., Shi, X., 2016. Long-term tobacco plantation induces soil acidification and soil base cation loss. Environmental Science and Pollution Research International23, 5442–5450.

[87]

Zhang, Y., Zhang, J., Meng, T., Zhu, T., Müller, C., Cai, Z., 2013. Heterotrophic nitrification is the predominant NO3 production pathway in acid coniferous forest soil in subtropical China. Biology and Fertility of Soils49, 955–957.

[88]

Zhang, Y., Zhang, J., Zhu, T., Muller, C., Cai, Z., 2015. Effect of orchard age on soil nitrogen transformation in subtropical China and implications. Journal of Environmental Sciences (China)34, 10–19.

[89]

Zhong, W., Bian, B., Gao, N., Min, J., Shi, W., Lin, X., Shen, W., 2016. Nitrogen fertilization induced changes in ammonia oxidation are attributable mostly to bacteria rather than archaea in greenhouse-based high N input vegetable soil. Soil Biology & Biochemistry93, 150–159.

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