Opposing effects of maize straw and its biochar on soil N₂O emissions by mediating microbial nitrification and denitrification in a subtropical Moso bamboo forest

Abstract

Abstract

Straw and biochar amendments markedly influence soil N₂O emissions in subtropical Moso bamboo forests, but the microbial mechanisms driving these responses remain elusive. This study aimed to assess the contrasting influences of maize straw and its derived biochar on soil N₂O emissions in a subtropical Moso bamboo forest. Straw amendment (5 t C ha⁻¹) stimulated N₂O emission by 16–27% (P<0.05). However, biochar addition (5 t C ha⁻¹) decreased the concentrations of NH₄⁺ by 11–14%, NO₃⁻ by 11–15% and water-soluble organic nitrogen for 14–17%, and decreased the abundances of ammonia-oxidising bacterial amoA by 40–45%, nirK by 30–36%, nirS by 24–32% and associated genera Nitrosospira, Mesorhizobium, Bradyrhizobium, Rhizobium, Pseudomonas, and Cupriavidus. Biochar also decreased the activities of enzymes related to organic N hydrolysis (protease and urease) and denitrification (nitrate reductase and nitrite reductase), and thus decreased N₂O emissions by 17–20% (P<0.05). Furthermore, biochar enhanced the abundance of nosZ gene (by 40–46%) and its dominant genera (Mesorhizobium, Bradyrhizobium, and Azospirillum), which facilitated N₂O reduction. In contrast, straw inhibited the growth of these dominant genera and lowered the abundance of nosZ gene (by 24–38%). These results highlight the varied responses of nitrification and denitrification processes and hence N₂O emission to the application of straw and biochar in soils of a subtropical Moso bamboo forest.

Highlights

•	Maize straw enhances but its biochar lowers N2O emissions
•	Biochar decreases organic N hydrolysis and denitrifying enzyme activities
•	Biochar reduces the abundances of AOB amoA, nirK and nirS and dominant genera
•	Biochar promotes the abundances of nosZ gene and its dominant genera

Keywords

Nitrous oxide emission / Microbial functional community / Microbial gene abundance / Nitrogen dynamics / Organic amendments

References

[1] Aamer M, Shaaban M, Hassan MU, Huang G, Liu Y, Tang H, Rasul F, Ma Q, Li Z, Rasheed A, Zhang P. Biochar mitigates the N₂O emissions from acidic soil by increasing the nosZ and nirK gene abundance and soil pH. J Environ Manage, 2020, 255 109891

[2] Abdelmagid HM, Tabatabai MA. Nitrate reductase activity of soils. Soil Biol Biochem, 1987, 19: 421-427

[3] Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods, 2016, 13: 581-583

[4] Cao L, Yu X, Liu C, Liu M, Chen J, Qin H, Liang C, Xu Q, Penttinen P. Alteration of soil nitrifiers and denitrifiers and their driving factors during intensive management of Moso bamboo (Phyllostachys pubescens). Sci Total Environ, 2020, 705 135236

[5] Chen S, Jiang H, Cai Z, Zhou X, Peng C. The response of the net primary production of Moso bamboo forest to the on and off-year management: a case study in Anji County, Zhejiang, China. For Ecol Manag, 2018, 409: 1-7

[6] Cordero I, Snell H, Bardgett RD. High throughput method for measuring urease activity in soil. Soil Biol Biochem, 2019, 134: 72-77

[7] Ding Y, Liu Y, Liu S, Li Z, Tan X, Huang X, Zeng G, Zhou L, Zheng B. Biochar to improve soil fertility. A review. Agron Sustain Dev, 2016, 36 36

[8] Gai X, Wang H, Liu J, Zhai L, Liu S, Ren T, Liu H. Effects of feedstock and pyrolysis temperature on biochar adsorption of ammonium and nitrate. PLoS ONE, 2014, 9 e113888

[9] Gao Y, Long X, Liao Y, Lin Y, He Z, Kong Q, Kong X, He X. Influence of arbuscular mycorrhizal fungi on nitrogen dynamics during Cinnamomum camphora litter decomposition. Microorganisms, 2025, 13: 151

[10] He Z, Hu H, Zhang L. Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biol Biochem, 2012, 55: 146-154

[11] Hoyweghen LV, Beer TD, Deforce D, Heyerick A. Phenolic compounds and anti-oxidant capacity of twelve morphologically heterogeneous bamboo species. Phytochem Anal, 2012, 23: 433-443

[12] Hulse CL, Tiedje JM, Averill BA. A spectrophotometric assay for dissimilatory nitrite reductases. Anal Biochem, 1988, 172: 420-426

[13] Ji C, Li S, Geng Y, Miao Y, Ding Y, Liu S, Zou J. Differential responses of soil N₂O to biochar depend on the predominant microbial pathway. Appl Soil Ecol, 2020, 145 103348

[14] Ji D, Ge L, Van Zwieten L, An T, Li S, Kuzyakov Y, Ding F, Wang J. Contrasting effects of maize straw and its biochar on aggregation and soil organic matter stabilization. Plant Soil, 2024, 495: 221-233

[15] Jiang W, Zhang H, Fang Y, Chen Y, Zhuo S, Chen Z, Liang C, Van Zwieten L, Fu S, Li Y, Yu B, Cai Y, Chang SX. Understory N application overestimates the effect of atmospheric N deposition on soil N₂O emissions. Geoderma, 2023, 437 116611

[16] Jiang Z, Vancov T, Fang Y, Tang C, Zhang W, Xiao M, Song X, Zhou J, Ge T, Cai Y, Yu B, White JC, Li Y. Sustained superiority of biochar over straw for enhancing soil biological-phosphorus via the mediation of phoD-harboring bacteria in subtropical Moso bamboo forests. For Ecol Manage, 2025, 584 122606

[17] Knicker H. “Black nitrogen”—an important fraction in determining the recalcitrance of charcoal. Org Geochem, 2010, 41: 947-950

[18] Kuypers MMM, Marchant HK, Kartal B. The microbial nitrogen-cycling network. Nat Rev Microbiol, 2018, 16: 263-276

[19] Greenfield LM, Puissant J, Jones DL. Synthesis of methods used to assess soil protease activity. Soil Biol Biochem, 2021, 158 108277

[20] Li Z, Zhang L, Deng B, Liu Y, Kong F, Huang G, Zou Q, Liu Q, Guo X, Fu Y, Niu D, Siemann E. Effects of moso bamboo (Phyllostachys edulis) invasions on soil nitrogen cycles depend on invasion stage and warming. Environ Sci Pollut Res, 2017, 24: 24989-24999

[21] Li Y, Hu S, Chen J, Müller K, Li Y, Fu W, Lin Z, Wang H. Effects of biochar application in forest ecosystems on soil properties and greenhouse gas emissions: a review. J Soil Sediment, 2018, 18: 546-563

[22] Li Z, Li D, Ma L, Yu Y, Zhao B, Zhang J. Effects of straw management and nitrogen application rate on soil organic matter fractions and microbial properties in North China Plain. J Soil Sediment, 2019, 19: 618-628

[23] Li Y, Zhang S, Fang Y, Hui D, Tang C, Van Zwieten L, Zhou J, Jiang Z, Cai Y, Yu B, Hu J, Zhou G, Gu B, Chang SX. Nitrogen deposition-induced stimulation of soil heterotrophic respiration is counteracted by biochar in a subtropical forest. Agric for Meteorol, 2024, 349 109940

[24] Lin Y, Ye G, Liu D, Ledgard S, Luo J, Fan J, Yuan J, Chen Z, Ding W. Long-term application of lime or pig manure rather than plant residues suppressed diazotroph abundance and diversity and altered community structure in an acidic Ultisol. Soil Biol Biochem, 2018, 123: 218-228

[25] Liu Q, Zhang Y, Liu B, Amonette JE, Lin Z, Liu G, Ambus P, Xie Z. How does biochar influence soil N cycle? A meta-analysis. Plant Soil, 2018, 426: 211-225

[26] Liu Y, Dai Q, Jin X, Dong X, Peng J, Wu M, Liang N, Pan B, Xing B. Negative impacts of biochars on urease activity: High pH, heavy metals, polycyclic aromatic hydrocarbons, or free radicals?. Environ Sci Technol, 2018, 52: 12740-12747

[27] Liu Y, Li C, Cai G, Sauheitl L, Xiao M, Shibistova O, Ge T, Guggenberger G. Meta-analysis on the effects of types and levels of N, P, and K fertilization on organic carbon in cropland soils. Geoderma, 2023, 437 116580

[28] Lu R. Analytical methods for soil agrochemistry, 2000, Beijing, Chinese Agricultural Science and Technology Publishing House

[29] Lv N, Gong P, Sun H, Sun X, Liu Z, Xie X, Xue Y, Song Y, Wu K, Wang T, Wu Z, Zhang L. Agricultural ecosystems rather than fertilization strategies drives structure and composition of the ureolytic microbial functional guilds. J Environ Manage, 2024, 372 123148

[30] McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. An improved greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J, 2012, 6: 610-618

[31] Nguyen TTN, Xu C, Tahmasbian I, Che R, Xu Z, Zhou X, Wallace HM, Bai SH. Effects of biochar on soil available inorganic nitrogen: a review and meta-analysis. Geoderma, 2017, 288: 79-96

[32] Ouyang Y, Evans SE, Friesen ML, Tiemann LK. Effect of nitrogen fertilization on the abundance of nitrogen cycling genes in agricultural soils: a meta-analysis of field studies. Soil Biol Biochem, 2018, 127: 71-78

[33] Prosser JI, Nicol GW. Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol, 2012, 20: 523-531

[34] Rafiq MK, Bachmann RT, Rafiq MT, Shang Z, Joseph S, Long R. Influence of pyrolysis temperature on physico-chemical properties of corn stover (Zea mays L.) biochar and feasibility for carbon capture and energy balance. PLoS ONE, 2016, 11 e0156894

[35] Sánchez C, Itakura M, Mitsu H, Minamisawa K. Linked expressions of nap and nos genes in a Bradyrhizobium japonicum mutant with increased N₂O reductase activity. Appl Environ Microbiol, 2013, 79: 4178-4180

[36] Sciotti MA, Chanfon A, Hennecke H, Fischer HM. Disparate oxygen responsiveness of two regulatory cascades that control expression of symbiotic genes in Bradyrhizobium japonicum. J Bacteriol, 2003, 185: 5639-5642

[37] Shi M, Yang W, Zhang J, Sun J, Ji H, Li Q, Cao T, Wang Z, Zhang C, Song X. Effects of N rhizodeposition on rhizosphere N transformation in clonal ramets of Moso bamboo forest. Plant Soil, 2024, 503: 717-732

[38] Starr SF, Mortazavi B, Tatariw C, Kuehn KA, Cherry JA, Ledford T, Smyth E, Wood AG, Sebren SE. Labile organic matter promotes nitrogen retention in natural and constructed gulf coast marshes. Biogeochemistry, 2024, 167: 269-285

[39] Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC. Measurement of soil microbial biomass C by fumigation extraction—an automated procedure. Soil Biol Biochem, 1990, 22: 1167-1169

[40] Xia H, Riaz M, Tang X, Yan L, El-Desouki Z, Li Y, Wang X, Cuncang J. Insight into mechanisms of biochar-fertilizer induced of microbial community and microbiology of nitrogen cycle in acidic soil. J Environ Manag, 2023, 336 117602

[41] Xiao M, Tang C, Jiang Z, Zhou J, Luo Y, Ge T, Pan L, Yu B, Cai Y, White JC, Li Y. Data for opposing effects of maize straw and its biochar on soil N₂O emissions by mediating microbial nitrification and denitrification in a subtropical Moso bamboo forest2025figshare,

[42] Xie Z, Yu Z, Li Y, Wang G, Tang C, Mathesius U, Liu X, Liu J, Liu J, Chen Y, Zhang S, Herbert SJ, Wu J, Jin J. Rhizosphere-induced shift in the composition of bacterial community favors mineralization of crop residue nitrogen. Plant Soil, 2024, 502: 135-148

[43] Xiong W, Li J, Liu J, Li C, He Z, Li X. Quantification of microbially induced soil N₂O emissions by an inhibitory cocktail in mountain forest ecosystems. Geoderma, 2024, 443 116835

[44] Xu L, Chen H, Zhou Y, Zhang J, Nadeem MY, Miao C, You J, Li W, Jiang Y, Ding Y, Li G. Long-term straw returning improved soil nitrogen sequestration by accelerating the accumulation of amino acid nitrogen. Agric Ecosyst Environ, 2024, 362 108846

[45] Zhang J, Yang X, Guo C, De Lajudie P, Singh RP, Wang E, Chen W. Mesorhizobium muleiense and Mesorhizobium gsp. nov. are symbionts of Cicer arietinum L. in alkaline soils of Gansu, Northwest China. Plant Soil, 2017, 410: 103-112

[46] Zhang J, Wei Y, Liu J, Yuan J, Liang Y, Ren J, Cai H. Effects of maize straw and its biochar application on organic and humic carbon in water-stable aggregates of a Mollisol in Northeast China: a five-year field experiment. Soil till Res, 2019, 190: 1-9

[47] Zhang S, Zhou J, Chen J, Ge T, Cai Y, Yu B, Wang H, White JC, Li Y. Changes in soil CO₂ and N₂O emissions in response to urea and biochar-based urea in a subtropical Moso bamboo forest. Soil till Res, 2023, 228 105625

[48] Zhao Z, Tao C, Liu X, Cheng X, Zhou C, Huang S, Shou M, Zhang Q, Huang B, Li C, Tu G, Zhou Y. Effects of different management measures on carbon stocks and soil carbon stocks in Moso bamboo forests: meta-analysis and control experiment. Forests, 2024

[49] Zhou J, Qu T, Li Y, Van Zwieten L, Wang H, Chen J, Song X, Lin Z, Zhang X, Luo Y, Cai Y, Zhong Z. Biochar-based fertilizer decreased while chemical fertilizer increased soil N₂O emissions in a subtropical Moso bamboo plantation. CATENA, 2021, 202 105257

[50] Zhou J, Tang C, Kuzyakov Y, Vancov T, Fang Y, Song X, Zhou X, Jiang Z, Ge T, Xu L, Cai Y, Yu B, White JC, Gu B, Chen X, Ciais P, Li Y. Biochar-based urea increases soil methane uptake in a subtropical forest. Geoderma, 2024, 449 116994

[51] Zhou J, Zhang S, Hui D, Vancov T, Fang Y, Tang C, Jiang Z, Ge T, Cai Y, Yu B, White JC, Li Y. Pyrogenic organic matter decreases while fresh organic matter increases soil heterotrophic respiration through modifying microbial activity in a subtropical forest. Biol Fertil Soils, 2024, 60: 509-524

[52] Zhou J, Zhang S, Lv J, Tang C, Zhang H, Fang Y, Tavakkoli E, Ge T, Luo Y, Cai Y, Yu B, White JC, Li Y. Maize straw increases while its biochar decreases native organic carbon mineralization in a subtropical forest soil. Sci Total Environ, 2024, 939 173606

[53] Zhou J, Delgado-Baquerizo M, Vancov T, Liu Y, Zhou X, Chen J, Fang Y, Liu S, Yu B, Zhou G, Gu B, White JC, Chen X, Li Y. Biochar mitigates nitrogen deposition-induced enhancement of soil N₂O emissions in a subtropical forest. Biol Fertil Soils, 2025

[54] Zhou J, Tang C, Vancov T, Fu S, Fang Y, Ge T, Dong Y, Luo Y, Yu B, Cai Y, White JC, Li Y. Biochar mitigates the suppressive effects of nitrogen deposition on soil methane uptake in a subtropical forest. Agric Ecosyst Environ, 2026, 395 109951

[55] Zhu K, Ye X, Ran H, Zhang P, Wang G. Contrasting effects of straw and biochar on microscale heterogeneity of soil O₂ and pH: implication for N₂O emissions. Soil Biol Biochem, 2022, 166 108564

Funding

National Key Research and Development Program of China(2022YFE0127800)

National Natural Science Foundation of China(32271845)

RIGHTS & PERMISSIONS

The Author(s)