Response of comammox <i>Nitrospira</i> to nitrogen fertilization in acidic paddy soil

FU Yajun; GAO Wenlong; CHEN Miao

doi:10.15886/j.cnki.rdswxb.20230128

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Volume 15 Issue 5

Sep. 2024

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Article Navigation > Journal of Tropical Biology > 2024 > 15(5): 509-519

FU Yajun, GAO Wenlong, CHEN Miao. Response of comammox Nitrospira to nitrogen fertilization in acidic paddy soil[J]. Journal of Tropical Biology, 2024, 15(5): 509-519. doi: 10.15886/j.cnki.rdswxb.20230128

Citation:

FU Yajun, GAO Wenlong, CHEN Miao. Response of comammox Nitrospira to nitrogen fertilization in acidic paddy soil[J]. Journal of Tropical Biology, 2024, 15(5): 509-519. doi: 10.15886/j.cnki.rdswxb.20230128

Response of comammox Nitrospira to nitrogen fertilization in acidic paddy soil

doi: 10.15886/j.cnki.rdswxb.20230128

FU Yajun¹,
GAO Wenlong^2,3,
CHEN Miao^{2,3
,
,}

1. College of Ecology and Environment, Hainan University, Haikou, Hainan 570228;
2. Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan 571101;
3. Hainan Danzhou Tropical Agro-ecosystem National Observation and Research Station, Danzhou 571737, Hainan, China

Received Date: 2023-11-28
Rev Recd Date: 2024-02-25

Abstract

In order to reveal the differences in response and sensitivity of comamox Nitrospira and incomplete nitrifiers to nitrogen addition in acidic rice fields, a pot experiment was conducted to investigate the impact of urea fertilization, in conjunction with growth stage, on complete nitrifiers, and to compare their responsiveness to nitrogen（N） fertilization with that of incomplete nitrifiers in acidic paddy soils. The research results revealed that irrespective of fertilization conditions, comammox Nitrospira(Clade A: 3.24×10⁸-7.24×10⁸ copies·g^-1, Clade B: 2.14×10⁸-1.48×10⁹ copies · g^-1) rather than ammonia-oxidizing archaea(AOA: 2.00×10⁷-4.37×10⁷ copies·g^-1) and nitriteoxidizing bacteria(AOB: 1.35×10⁷-3.31×10⁷ copies·g^-1), were the dominant ammonia oxidizers across tillering,heading, and maturity stages. Neither urea fertilization（Clade A: P = 0.762, Clade B: P = 0.398） nor growth stage（Clade A: P = 0.264, Clade B: P = 0.237）, nor their interaction（Clade A: P = 0.316, Clade B: P = 0.294）,significantly influenced comammox Nitrospira clades A and B, as their populations remained consistent across the fertilizer treatments and seasons. It is plausible that the environmental factors governing comammox bacterial abundance in urea-fertilized and unfertilized soils may vary. In the absence of urea, the abundance of comammox Nitrospira clades A（R =-0.73, P = 0.027） and B（R =-0.75, P = 0.019） exhibited a negative correlation with soil N, suggesting that increased ammonia, ammonification, and organic N may not be conducive to comammox bacterial growth and activity in unfertilized soils. Conversely, in the presence of urea, comammox bacteria,especially clade A, were notably influenced by soil pH and redox potential（Eh）. Notably, urea application had the potential to alter the interplay between complete and incomplete nitrifiers, as evidenced by the absence of a positive mode of population co-variation of clade B with AOA and AOB following urea application.
- comammox Nitrospira,
- incomplete nitrifiers,
- urea application,
- growth stage,
- acidic paddy soil

References

[1]	LI Y, CHAPMAN S, NICOL G, et al. Nitrification and nitrifiers in acidic soils[J]. Soil Biology&Biochemistry,2018, 116:290-301.
[2]	DAIMS H, LEBEDEVA E V, PJEVAC P, et al. Complete nitrification by Nitrospira bacteria[J]. Nature, 2015, 528:504-509.
[3]	VAN KESSEL M A H J, SPETH D R, ALBERTSEN M, et al. Complete nitrification by a single microorganism[J].Nature, 2015, 528:555-559.
[4]	KITS K D, SEDLACEK C J, LEBEDEVA E V, et al.Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle[J]. Nature, 2017, 549:269-272.
[5]	HU H W, HE J Z. Comammox-a newly discovered nitrification process in the terrestrial nitrogen cycle[J]. Journal of Soils and Sediments, 2017, 17(12):2709-2717.
[6]	XIA F, WANG J G, ZHU T, et al. Ubiquity and diversity of complete ammonia oxidizers (comammox)[J]. Applied and Environmental Microbiology, 2018, 84(24):e01390-e01318.
[7]	LIU S, WANG H, CHEN L, et al. Comammox Nitrospira within the Yangtze River continuum:community, biogeography, and ecological drivers[J]. The ISME Journal, 2020,14:2488-2504.
[8]	ZHOU L J, HAN P, ZHAO M, et al. Biotransformation of lincomycin and fluoroquinolone antibiotics by the ammonia oxidizers AOA, AOB and comammox:a comparison of removal, pathways, and mechanisms[J]. Water Research,2021, 196:117003.
[9]	PJEVAC P, SCHAUBERGER C, POGHOSYAN L, et al.AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammox Nitrospira in the environment[J]. Frontiers in Microbiology,2017, 8:1508.
[10]	PALOMO A, PEDERSEN A G, FOWLER S J, et al. Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira[J].The ISME Journal, 2018, 12(7):1779-1793.
[11]	GAO W, FU Y, FAN C, et al. Factors predictive of the biogeographic distribution of comammox Nitrospira in terrestrial ecosystems[J]. Soil Biology and Biochemistry,2023, 184:109079.
[12]	ZHU G, WANG X, WANG S, et al. Towards a more laborsaving way in microbial ammonium oxidation:a review on complete ammonia oxidization (comammox)[J]. The Science of the Total Environment, 2022, 829:154590.
[13]	KE X, ANGEL R, LU Y, et al. Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil[J].Environmental Microbiology, 2013, 15(8):2275-2292.
[14]	XU S, WANG B, LI Y, et al. Ubiquity, diversity, and activity of comammox Nitrospira in agricultural soils[J].The Science of the Total Environment, 2020, 706:135684.
[15]	ZHAO J, BELLO M, MENG Y, et al. Selective inhibition of ammonia oxidising Archaea by simvastatin stimulates growth of ammonia oxidising bacteria[J]. Soil Biology and Biochemistry. 2020, 141:107673.
[16]	KITS K D, SEDLACEK C J, LEBEDEVA E V, et al.Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle[J]. Nature, 2017, 549:269-272.
[17]	HU J, ZHAO Y, YAO X, et al. Dominance of comammox Nitrospira in soil nitrification[J]. The Science of the Total Environment, 2021, 780:146558.
[18]	ORELLANA L H, CHEE-SANFORD J C, SANFORD R A, et al. Year-round shotgun metagenomes reveal stable microbial communities in agricultural soils and novel ammonia oxidizers responding to fertilization[J]. Applied and Environmental Microbiology, 2018, 84(2):e01646-e01617.
[19]	TAKAHASHI Y, FUJITANI H, HIRONO Y, et al.Enrichment of comammox and nitrite-oxidizing Nitrospira from acidic soils[J]. Frontiers in Microbiology,2020, 11:1737.
[20]	SHEN J P, ZHANG L M, ZHU Y G, et al. Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing Archaea communities of an alkaline sandy loam[J]. Environmental Microbiology, 2008, 10(6):1601-1611.
[21]	XIE J, WANG Z, WANG Y, et al. Manure combined with biochar reduces rhizosphere nitrification potential and amoA gene abundance of ammonia-oxidizing microorganisms in acid purple soil[J]. Applied Soil Ecology, 2023,181:104660.
[22]	LI C, HE Z Y, HU H W, et al. Niche specialization of comammox Nitrospira in terrestrial ecosystems:Oligotrophic or copiotrophic?[J]. Critical Reviews in Environmental Science and Technology, 2023, 53(2):161-176.
[23]	陈娜,刘毅,肖谋良,等. CO2倍增和施氮对水稻不同生长期土壤反硝化细菌丰度的影响[J].环境科学研究, 2019, 32(4):683-691.
[24]	石秀丽,郭萌萌,张莹,等.单步硝化作用与全程氨氧化微生物研究进展[J].草业学报, 2018, 27(7):196-203.
[25]	LIU H, HU H, HUANG X, et al. Canonical ammonia oxidizers, rather than comammox Nitrospira, dominated autotrophic nitrification during the mineralization of organic substances in two paddy soils[J]. Soil Biology and Biochemistry, 2021, 156:108192.
[26]	LIU T, WANG Z, WANG S, et al. Responses of ammoniaoxidizers and comammox to different long-term fertilization regimes in a subtropical paddy soil[J]. European Journal of Soil Biology, 2019, 93:103087.
[27]	WANG J, WANG J, RHODES G, et al. 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[J]. The Science of the Total Environment, 2019, 668:224-233.
[28]	NIE S A, LI H, YANG X, et al. Nitrogen loss by anaerobic oxidation of ammonium in rice rhizosphere[J]. The ISME Journal, 2015, 9(9):2059-2067.
[29]	鲍士旦.土壤农化分析[M]. 3版.北京:中国农业出版社, 2008:39-89.
[30]	BEMAN J M, FRANCIS C A. Diversity of ammoniaoxidizing Archaea and bacteria in the sediments of a hypernutrified subtropical estuary:Bahía del Tóbari,Mexico[J]. Applied and Environmental Microbiology,2006, 72(12):7767-7777.
[31]	ROTTHAUWE J H, WITZEL K P, LIESACK W. The ammonia monooxygenase structural gene amoA as a functional marker:molecular fine-scale analysis of natural ammonia-oxidizing populations[J]. Applied and Environmental Microbiology, 1997, 63(12):4704-4712.
[32]	JIANG R, WANG J G, ZHU T, et al. Use of newly designed primers for quantification of complete ammonia-oxidizing (comammox) bacterial clades and strict nitrite oxidizers in the genus Nitrospira[J]. Applied and Environmental Microbiology, 2020, 86(20):e01775-e01720.
[33]	LI D, REN Z, ZHOU Y, et al. Comammox Nitrospira and ammonia-oxidizing Archaea are dominant ammonia oxidizers in sediments of an acid mine lake containing high ammonium concentrations[J]. Applied and Environmental Microbiology, 2023, 89(3):e0004723.
[34]	ZHOU X, WANG S, MA S, et al. Effects of commonly used nitrification inhibitors-dicyandiamide (DCD), 3, 4-dimethylpyrazole phosphate (DMPP), and nitrapyrin-on soil nitrogen dynamics and nitrifiers in three typical paddy soils[J]. Geoderma, 2020, 380:114637.
[35]	LI C, HU H W, CHEN Q L, et al. Comammox Nitrospira play an active role in nitrification of agricultural soils amended with nitrogen fertilizers[J]. Soil Biology and Biochemistry, 2019, 138:107609.
[36]	GAO F, LI Y, FAN H, et al. Main environmental drivers of abundance, diversity and community structure of comammox Nitrospira in paddy soils[J]. Pedosphere,2023, 33(5):808-818.
[37]	LI D, FANG F, LIU G. Efficient nitrification and lowlevel N₂O emission in a weakly acidic bioreactor at low dissolved-oxygen levels are due to comammox[J].Applied and Environmental Microbiology, 2021, 87(11):e00154-e00121.
[38]	LI C, HU H, CHEN Q, et al. Niche specialization of comammox Nitrospira clade A in terrestrial ecosystems[J].Soil Biology\&Biochemistry, 2021, 156:108231.
[39]	LIN Y, FAN J, HU H W, et al. Differentiation of individual clusters of comammox Nitrospira in an acidic Ultisol following long-term fertilization[J]. Applied Soil Ecology, 2022, 170:104267.

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通讯作者: 陈斌, bchen63@163.com

1.
沈阳化工大学材料科学与工程学院沈阳 110142

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Response of comammox Nitrospira to nitrogen fertilization in acidic paddy soil

1. College of Ecology and Environment, Hainan University, Haikou, Hainan 570228;

2. Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan 571101;

3. Hainan Danzhou Tropical Agro-ecosystem National Observation and Research Station, Danzhou 571737, Hainan, China

Received Date: 2023-11-28

Rev Recd Date: 2024-02-25

Key words:

Abstract: In order to reveal the differences in response and sensitivity of comamox Nitrospira and incomplete nitrifiers to nitrogen addition in acidic rice fields, a pot experiment was conducted to investigate the impact of urea fertilization, in conjunction with growth stage, on complete nitrifiers, and to compare their responsiveness to nitrogen（N） fertilization with that of incomplete nitrifiers in acidic paddy soils. The research results revealed that irrespective of fertilization conditions, comammox Nitrospira(Clade A: 3.24×10⁸-7.24×10⁸ copies·g^-1, Clade B: 2.14×10⁸-1.48×10⁹ copies · g^-1) rather than ammonia-oxidizing archaea(AOA: 2.00×10⁷-4.37×10⁷ copies·g^-1) and nitriteoxidizing bacteria(AOB: 1.35×10⁷-3.31×10⁷ copies·g^-1), were the dominant ammonia oxidizers across tillering,heading, and maturity stages. Neither urea fertilization（Clade A: P = 0.762, Clade B: P = 0.398） nor growth stage（Clade A: P = 0.264, Clade B: P = 0.237）, nor their interaction（Clade A: P = 0.316, Clade B: P = 0.294）,significantly influenced comammox Nitrospira clades A and B, as their populations remained consistent across the fertilizer treatments and seasons. It is plausible that the environmental factors governing comammox bacterial abundance in urea-fertilized and unfertilized soils may vary. In the absence of urea, the abundance of comammox Nitrospira clades A（R =-0.73, P = 0.027） and B（R =-0.75, P = 0.019） exhibited a negative correlation with soil N, suggesting that increased ammonia, ammonification, and organic N may not be conducive to comammox bacterial growth and activity in unfertilized soils. Conversely, in the presence of urea, comammox bacteria,especially clade A, were notably influenced by soil pH and redox potential（Eh）. Notably, urea application had the potential to alter the interplay between complete and incomplete nitrifiers, as evidenced by the absence of a positive mode of population co-variation of clade B with AOA and AOB following urea application.

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Reference (39)

[1]	LI Y, CHAPMAN S, NICOL G, et al. Nitrification and nitrifiers in acidic soils[J]. Soil Biology&Biochemistry,2018, 116:290-301.
[2]	DAIMS H, LEBEDEVA E V, PJEVAC P, et al. Complete nitrification by Nitrospira bacteria[J]. Nature, 2015, 528:504-509.
[3]	VAN KESSEL M A H J, SPETH D R, ALBERTSEN M, et al. Complete nitrification by a single microorganism[J].Nature, 2015, 528:555-559.
[4]	KITS K D, SEDLACEK C J, LEBEDEVA E V, et al.Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle[J]. Nature, 2017, 549:269-272.
[5]	HU H W, HE J Z. Comammox-a newly discovered nitrification process in the terrestrial nitrogen cycle[J]. Journal of Soils and Sediments, 2017, 17(12):2709-2717.
[6]	XIA F, WANG J G, ZHU T, et al. Ubiquity and diversity of complete ammonia oxidizers (comammox)[J]. Applied and Environmental Microbiology, 2018, 84(24):e01390-e01318.
[7]	LIU S, WANG H, CHEN L, et al. Comammox Nitrospira within the Yangtze River continuum:community, biogeography, and ecological drivers[J]. The ISME Journal, 2020,14:2488-2504.
[8]	ZHOU L J, HAN P, ZHAO M, et al. Biotransformation of lincomycin and fluoroquinolone antibiotics by the ammonia oxidizers AOA, AOB and comammox:a comparison of removal, pathways, and mechanisms[J]. Water Research,2021, 196:117003.
[9]	PJEVAC P, SCHAUBERGER C, POGHOSYAN L, et al.AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammox Nitrospira in the environment[J]. Frontiers in Microbiology,2017, 8:1508.
[10]	PALOMO A, PEDERSEN A G, FOWLER S J, et al. Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira[J].The ISME Journal, 2018, 12(7):1779-1793.
[11]	GAO W, FU Y, FAN C, et al. Factors predictive of the biogeographic distribution of comammox Nitrospira in terrestrial ecosystems[J]. Soil Biology and Biochemistry,2023, 184:109079.
[12]	ZHU G, WANG X, WANG S, et al. Towards a more laborsaving way in microbial ammonium oxidation:a review on complete ammonia oxidization (comammox)[J]. The Science of the Total Environment, 2022, 829:154590.
[13]	KE X, ANGEL R, LU Y, et al. Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil[J].Environmental Microbiology, 2013, 15(8):2275-2292.
[14]	XU S, WANG B, LI Y, et al. Ubiquity, diversity, and activity of comammox Nitrospira in agricultural soils[J].The Science of the Total Environment, 2020, 706:135684.
[15]	ZHAO J, BELLO M, MENG Y, et al. Selective inhibition of ammonia oxidising Archaea by simvastatin stimulates growth of ammonia oxidising bacteria[J]. Soil Biology and Biochemistry. 2020, 141:107673.
[16]	KITS K D, SEDLACEK C J, LEBEDEVA E V, et al.Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle[J]. Nature, 2017, 549:269-272.
[17]	HU J, ZHAO Y, YAO X, et al. Dominance of comammox Nitrospira in soil nitrification[J]. The Science of the Total Environment, 2021, 780:146558.
[18]	ORELLANA L H, CHEE-SANFORD J C, SANFORD R A, et al. Year-round shotgun metagenomes reveal stable microbial communities in agricultural soils and novel ammonia oxidizers responding to fertilization[J]. Applied and Environmental Microbiology, 2018, 84(2):e01646-e01617.
[19]	TAKAHASHI Y, FUJITANI H, HIRONO Y, et al.Enrichment of comammox and nitrite-oxidizing Nitrospira from acidic soils[J]. Frontiers in Microbiology,2020, 11:1737.
[20]	SHEN J P, ZHANG L M, ZHU Y G, et al. Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing Archaea communities of an alkaline sandy loam[J]. Environmental Microbiology, 2008, 10(6):1601-1611.
[21]	XIE J, WANG Z, WANG Y, et al. Manure combined with biochar reduces rhizosphere nitrification potential and amoA gene abundance of ammonia-oxidizing microorganisms in acid purple soil[J]. Applied Soil Ecology, 2023,181:104660.
[22]	LI C, HE Z Y, HU H W, et al. Niche specialization of comammox Nitrospira in terrestrial ecosystems:Oligotrophic or copiotrophic?[J]. Critical Reviews in Environmental Science and Technology, 2023, 53(2):161-176.
[23]	陈娜,刘毅,肖谋良,等. CO2倍增和施氮对水稻不同生长期土壤反硝化细菌丰度的影响[J].环境科学研究, 2019, 32(4):683-691.
[24]	石秀丽,郭萌萌,张莹,等.单步硝化作用与全程氨氧化微生物研究进展[J].草业学报, 2018, 27(7):196-203.
[25]	LIU H, HU H, HUANG X, et al. Canonical ammonia oxidizers, rather than comammox Nitrospira, dominated autotrophic nitrification during the mineralization of organic substances in two paddy soils[J]. Soil Biology and Biochemistry, 2021, 156:108192.
[26]	LIU T, WANG Z, WANG S, et al. Responses of ammoniaoxidizers and comammox to different long-term fertilization regimes in a subtropical paddy soil[J]. European Journal of Soil Biology, 2019, 93:103087.
[27]	WANG J, WANG J, RHODES G, et al. 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[J]. The Science of the Total Environment, 2019, 668:224-233.
[28]	NIE S A, LI H, YANG X, et al. Nitrogen loss by anaerobic oxidation of ammonium in rice rhizosphere[J]. The ISME Journal, 2015, 9(9):2059-2067.
[29]	鲍士旦.土壤农化分析[M]. 3版.北京:中国农业出版社, 2008:39-89.
[30]	BEMAN J M, FRANCIS C A. Diversity of ammoniaoxidizing Archaea and bacteria in the sediments of a hypernutrified subtropical estuary:Bahía del Tóbari,Mexico[J]. Applied and Environmental Microbiology,2006, 72(12):7767-7777.
[31]	ROTTHAUWE J H, WITZEL K P, LIESACK W. The ammonia monooxygenase structural gene amoA as a functional marker:molecular fine-scale analysis of natural ammonia-oxidizing populations[J]. Applied and Environmental Microbiology, 1997, 63(12):4704-4712.
[32]	JIANG R, WANG J G, ZHU T, et al. Use of newly designed primers for quantification of complete ammonia-oxidizing (comammox) bacterial clades and strict nitrite oxidizers in the genus Nitrospira[J]. Applied and Environmental Microbiology, 2020, 86(20):e01775-e01720.
[33]	LI D, REN Z, ZHOU Y, et al. Comammox Nitrospira and ammonia-oxidizing Archaea are dominant ammonia oxidizers in sediments of an acid mine lake containing high ammonium concentrations[J]. Applied and Environmental Microbiology, 2023, 89(3):e0004723.
[34]	ZHOU X, WANG S, MA S, et al. Effects of commonly used nitrification inhibitors-dicyandiamide (DCD), 3, 4-dimethylpyrazole phosphate (DMPP), and nitrapyrin-on soil nitrogen dynamics and nitrifiers in three typical paddy soils[J]. Geoderma, 2020, 380:114637.
[35]	LI C, HU H W, CHEN Q L, et al. Comammox Nitrospira play an active role in nitrification of agricultural soils amended with nitrogen fertilizers[J]. Soil Biology and Biochemistry, 2019, 138:107609.
[36]	GAO F, LI Y, FAN H, et al. Main environmental drivers of abundance, diversity and community structure of comammox Nitrospira in paddy soils[J]. Pedosphere,2023, 33(5):808-818.
[37]	LI D, FANG F, LIU G. Efficient nitrification and lowlevel N₂O emission in a weakly acidic bioreactor at low dissolved-oxygen levels are due to comammox[J].Applied and Environmental Microbiology, 2021, 87(11):e00154-e00121.
[38]	LI C, HU H, CHEN Q, et al. Niche specialization of comammox Nitrospira clade A in terrestrial ecosystems[J].Soil Biology\&Biochemistry, 2021, 156:108231.
[39]	LIN Y, FAN J, HU H W, et al. Differentiation of individual clusters of comammox Nitrospira in an acidic Ultisol following long-term fertilization[J]. Applied Soil Ecology, 2022, 170:104267.

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Response of comammox Nitrospira to nitrogen fertilization in acidic paddy soil

doi: 10.15886/j.cnki.rdswxb.20230128

Abstract

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通讯作者: 陈斌, bchen63@163.com

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Response of comammox Nitrospira to nitrogen fertilization in acidic paddy soil

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Response of comammox Nitrospira to nitrogen fertilization in acidic paddy soil

doi: 10.15886/j.cnki.rdswxb.20230128

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通讯作者: 陈斌, bchen63@163.com

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Response of comammox Nitrospira to nitrogen fertilization in acidic paddy soil

doi: 10.15886/j.cnki.rdswxb.20230128

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