Biochar and organic fertilizer applications enhance soil functional microbial abundance and agroecosystem multifunctionality

Abstract

Biochar and organic fertilizer are widely supported to maintain crop production and sustainable development of agroecosystems. However, it is unclear how biochar and organic fertilizer alone or in combination regulate soil functional microbiomes and their relationships to ecosystem multifunctionality (EMF). Herein, a long-term (started in 2013) field experiment, containing five fertilization treatments, was employed to explore the effects of biochar and organic fertilizer applications on the EMF (based on 18 functional indicators of crop productivity, soil nutrient supply, element cycling, and microbial biomass) and the functional microbiomes of bulk soil and rhizosphere soil [normalizing the abundances of 64 genes related to carbon (C), nitrogen (N), phosphorus (P), and sulphur (S) cycles]. Compared with single-chemical fertilization, biochar and organic fertilizer inputs significantly enhanced most ecosystem-single functions and, in particular, the EMF significantly increased by 18.7–30.1%; biochar and organic fertilizer applications significantly increased the abundances of soil microbial functional taxa related to C-N-P-S cycles to varying degree. The combined application of biochar and organic fertilizer showed a better improvement in these indicators compared to using them individually. Most functional microbial populations in the soil, especially the taxa involved in C degradation, nitrification, nitrate-reduction, organic P mineralization, and S cycling showed significantly positive associations with the EMF at different threshold levels, which ultimately was regulated by soil pH and nutrient availability. These results highlight the strong links between soil microbiomes and agroecosystem functions, as well as providing scientific support for inclusion of biochar in agricultural production and services with organic amendments.

Highlights

1.	8-year field evidence revealed impacts of biochar and pig manure on soil functional microbiome and ecosystem functions.
2.	Biochar and pig manure inputs notably enhanced most ecosystem-single functions and the EMF increased by 18.7–30.1%.
3.	Biochar and pig manure inputs notably enriched soil functional microbes related to C-N-P-S cycles to varying degree.
4.	Increase in EMF was related to microbe-driven soil processes such as C degradation, nitrification, and Po mineralization.
5.	Inclusion of biochar in crop production with organic amendments could enhance agro-ecosystem functions and services.

Keywords

Biochar / Organic fertilizer / Functional microbiome / Ecosystem functions / Multifunctionality

References

[] Aasfar A, Bargaz A, Yaakoubi K, Hilali A, Bennis I, Zeroual Y, Meftah Kadmiri I. Nitrogen fixing Azotobacter species as potential soil biological enhancers for crop nutrition and yield stability. Front Microbiol, 2021, 12: 628379,

[] Alori ET, Glick BR, Babalola OO. Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front Microbiol, 2017, 8: 971,

[] Anantharaman K, Hausmann B, Jungbluth SP, Kantor RS, Lavy A, Warren LA, Rappé MS, Pester M, Loy A, Thomas BC, Banfield JF. Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle. ISME J, 2018, 12(7): 1715-1728, coi: 1:CAS:528:DC%2BC1cXktVGquro%3D

[] Azeem M, Hayat R, Hussain Q, Tahir MI, Imran M, Abbas Z, Sajid M, Latif A, Irfan M. Effects of biochar and NPK on soil microbial biomass and enzyme activity during 2 years of application in the arid region. Arab J Geosci, 2019, 12: 1-13, coi: 1:CAS:528:DC%2BC1MXptFGktbg%3D

[] Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Subramanian S, Smith DL. Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci, 2018, 9: 1473,

[] Bai SH, Omidvar N, Gallart M, Kämper W, Tahmasbian I, Farrar MB, Singh K, Zhou G, Muqadass B, Xu CY, Koech R, Li Y, Nguyen TTN, van Zwieten L. Combined effects of biochar and fertilizer applications on yield: a review and meta-analysis. Sci Total Environ, 2022, 808: 152073, coi: 1:CAS:528:DC%2BB3MXis12ltrbE

[] Bao SD (2000) Soil and Agro-Chemistry Analysis, 3rd ed. China Agric. Press, Beijing

[] Basile-Doelsch I, Balesdent J, Pellerin S. Reviews and syntheses: the mechanisms underlying carbon storage in soil. Biogeosciences, 2020, 17(21): 5223-5242, coi: 1:CAS:528:DC%2BB3MXisVegu74%3D

[] Biederman LA, Harpole WS. Biochar and its effects on plant productivity and nutrient cycling: a meta-analysis. GCB Bioenergy, 2013, 5(2): 202-214, coi: 1:CAS:528:DC%2BC3sXmsVCrs70%3D

[] Breiman L. Random forest. Mach Learn, 2001, 45: 5-32,

[] Brtnicky M, Dokulilova T, Holatko J, Pecina V, Kintl A, Latal O, Vyhnanek T, Prichystalova J, Datta R. Long-term effects of biochar-based organic amendments on soil microbial parameters. Agronomy, 2019, 9(11): 747, coi: 1:CAS:528:DC%2BB3cXpsFWnu7k%3D

[] Cao H, Ning L, Xun M, Feng F, Li P, Yue S, Song J, Zhang W, Yang H. Biochar can increase nitrogen use efficiency of Malus hupehensis by modulating nitrate reduction of soil and root. Appl Soil Ecol, 2019, 135: 25-32,

[] Chen W, Wang J, Chen X, Meng Z, Xu R, Duoji D, Zhang J, He J, Wang Z, Chen J, Liu K, Hu T, Zhang Y. Soil microbial network complexity predicts ecosystem function along elevation gradients on the Tibetan Plateau. Soil Biol Biochem, 2022, 172: 108766, coi: 1:CAS:528:DC%2BB38Xhs1CrsL7P

[] Dai Z, Yu M, Chen H, Zhao H, Huang Y, Su W, Xia F, Chang SX, Brookes PC, Dahlgren RA, Xu J. Elevated temperature shifts soil N cycling from microbial immobilization to enhanced mineralization, nitrification and denitrification across global terrestrial ecosystems. Global Change Biol, 2020, 26(9): 5267-5276,

[] Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, Gaitan JJ, Encinar D, Berdugo M, Campbell CD, Singh BK. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun, 2016, 7(1): 10541, coi: 1:CAS:528:DC%2BC28XhslOntb0%3D

[] Delgado-Baquerizo M, Reich PB, Trivedi C, Eldridge DJ, Abades S, Alfaro FD, Bastida F, Berhe AA, Cutler NA, Gallardo A, García-Velázquez L, Hart CC, Hayes PE, He JZ, Hseu ZY, Hu HW, Kirchmair M, Neuhauser S, Pérez CA, Reed SC, Santos F, Sullivan BW, Trivedi P, Wang JT, Weber-Grullon L, Williams MA, Singh BK. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nat Ecol Evol, 2020, 4: 210-220,

[] Dominchin MF, Verdenelli RA, Berger MG, Aoki A, Meriles JM. Impact of N-fertilization and peanut shell biochar on soil microbial community structure and enzyme activities in a Typic Haplustoll under different management practices. Eur J Soil Biol, 2021, 104: 103298, coi: 1:CAS:528:DC%2BB3MXhtV2hsLjI

[] Dotaniya ML, Aparna K, Dotaniya CK, Singh M, Regar KL. Kuddus M. Role of soil enzymes in sustainable crop production. Enzymes in food biotechnology, 2019 Cambridge Academic Press 569-589,

[] Doyle A, Weintraub MN, Schimel JP. Persulfate digestion and simultaneous colorimetric analysis of carbon and nitrogen in soil extracts. Soil Sci Soc Am J, 2004, 68: 669-676, coi: 1:CAS:528:DC%2BD2cXitV2nurw%3D

[] Galhardo CX, Masini JC. Spectrophotometric determination of phosphate and silicate by sequential injection using molybdenum blue chemistry. Anal Chim Acta, 2000, 417: 191-200, coi: 1:CAS:528:DC%2BD3cXkslWlsbg%3D

[] Gao Y, Liang A, Zhang Y, Huang D, McLaughlin N, Zhang Y, Wang Y, Chen X, Zhang S. Effect of tillage practices on soil CO₂ emissions, microbial C-fixation, and C-degradation functional gene abundance in Northeast China. J Soil Sediment, 2023, 23(1): 446-458, coi: 1:CAS:528:DC%2BB38XisFersLvE

[] Garland G, Banerjee S, Edlinger A, Miranda Oliveira E, Herzog C, Wittwer R, Philippot L, Maestre FT, van Der Heijden MG. A closer look at the functions behind ecosystem multifunctionality: a review. J Ecol, 2021, 109(2): 600-613,

[] Giles M, Morley N, Baggs EM, Daniell TJ. Soil nitrate reducing processes–drivers, mechanisms for spatial variation, and significance for nitrous oxide production. Front Microbiol, 2012, 3: 407, coi: 1:CAS:528:DC%2BC3sXhtFSltLnO

[] Gong H, Li J, Liu Z, Zhang Y, Hou R, Zhu O. Mitigated greenhouse gas emissions in cropping systems by organic fertilizer and tillage management. Land, 2022, 11(7): 1026,

[] Guo Z, Han J, Li J, Xu Y, Wang X. Effects of long-term fertilization on soil organic carbon mineralization and microbial community structure. PLoS ONE, 2019, 14(1): e0211163, coi: 1:CAS:528:DC%2BC1MXmtFCmtr4%3D

[] Han Z, Xu P, Li Z, Lin H, Zhu C, Wang J, Zou J. Microbial diversity and the abundance of keystone species drive the response of soil multifunctionality to organic substitution and biochar amendment in a tea plantation. GCB Bioenergy, 2022, 14(4): 481-495, coi: 1:CAS:528:DC%2BB38XntFaqtbo%3D

[] Hossain ME, Shahrukh S, Hossain SA. Chemical fertilizers and pesticides: impacts on soil degradation, groundwater, and human health in Bangladesh. Environmental degradation: challenges and strategies for mitigation, 2022 Cham Springer International Publishing 63-92,

[] Hu W, Ran J, Dong L, Du Q, Ji M, Yao S, Sun Y, Gong C, Hou Q, Gong H, Chen R, Lu J, Xie S, Wang Z, Huang H, Li X, Xiong J, Xia R, Wei M, Zhao D, Zhang Y, Li J, Yang H, Wang X, Deng Y, Sun Y, Li H, Zhang L, Chu Q, Li X, Aqeel M, Manan A, Akram MA, Liu X, Li R, Li F, Hou C, Liu J, He JS, An L, Bardgett RD, Schmid B, Deng J. Aridity-driven shift in biodiversity–soil multifunctionality relationships. Nat Commun, 2021, 12(1): 5350, coi: 1:CAS:528:DC%2BB3MXitVSkurjP

[] Hu W, Zhang Y, Rong X, Fei J, Peng J, Luo G. Coupling amendment of biochar and organic fertilizers increases maize yield and phosphorus uptake by regulating soil phosphatase activity and phosphorus-acquiring microbiota. Agr Ecosyst Environ, 2023, 355: 108582, coi: 1:CAS:528:DC%2BB3sXhtFSjtLfK

[] Huang X, Wang C, Liu Q, Zhu Z, Lynn TM, Shen J, Whiteley AS, Kumaresan D, Tida GE, Wu J. Abundance of microbial CO₂-fixing genes during the late rice season in a long-term management paddy field amended with straw and straw-derived biochar. Can J Soil Sci, 2018, 98(2): 306-316, coi: 1:CAS:528:DC%2BC1cXotlyhurk%3D

[] Ibrahim MM, Zhang H, Guo L, Chen Y, Heiling M, Zhou B, Mao Y. Biochar interaction with chemical fertilizer regulates soil organic carbon mineralization and the abundance of key C-cycling-related bacteria in rhizosphere soil. Eur J Soil Biol, 2021, 106: 103350, coi: 1:CAS:528:DC%2BB3MXisVClsLjJ

[] Jarvie HP, Withers PJA, Neal C. Review of robust measurement of phosphorus in river water: sampling, storage, fractionation and sensitivity. Hydrol Earth Syst Sci, 2002, 6: 113-131,

[] Jia R, Zhou J, Chu J, Shahbaz M, Yang Y, Jones DL, Zang H, Razavi BS, Zeng Z. Insights into the associations between soil quality and ecosystem multifunctionality driven by fertilization management: a case study from the North China Plain. J Cleaner Prod, 2022, 362: 132265, coi: 1:CAS:528:DC%2BB38XhvFeqtbjL

[] Kätterer T, Roobroeck D, Andrén O, Kimutai G, Karltun E, Kirchmann H, Nybery G, Vanlauwe B, de Nowina KR. Biochar addition persistently increased soil fertility and yields in maize-soybean rotations over 10 years in sub-humid regions of Kenya. Field Crop Res, 2019, 235: 18-26,

[] Lazcano C, Zhu-Barker X, Decock C. Effects of organic fertilizers on the soil microorganisms responsible for N₂O emissions: a review. Microorganisms, 2021, 9(5): 983, coi: 1:CAS:528:DC%2BB3MXis1Ghs7jP

[] Li Y, Chapman SJ, Nicol GW, Yao H. Nitrification and nitrifiers in acidic soils. Soil Biol Biochem, 2018, 116: 290-301, coi: 1:CAS:528:DC%2BC2sXhslOntLnF

[] Li S, Wang S, Fan M, Wu Y, Shangguan Z. Interactions between biochar and nitrogen impact soil carbon mineralization and the microbial community. Soil Tillage Res, 2020, 196: 104437,

[] Li M, Guo J, Ren T, Luo G, Shen Q, Lu J, Guo S, Ling N. Crop rotation history constrains soil biodiversity and multifunctionality relationships. Agr Ecosyst Environ, 2021, 319: 107550,

[] Li QM, Zhang D, Zhang JZ, Zhou ZJ, Pan Y, Yang ZH, Zhu JH, Liu YH, Zhang LF. Crop rotations increased soil ecosystem multifunctionality by improving keystone taxa and soil properties in potatoes. Front Microbiol, 2023, 14: 1034761,

[] Liu Y, Wang C, He N, Wen X, Gao Y, Li S, Niu S, Butterbach-Bahl K, Luo Y, Yu G. A global synthesis of the rate and temperature sensitivity of soil nitrogen mineralization: latitudinal patterns and mechanisms. Global Change Biol, 2017, 23(1): 455-464,

[] Liu H, Yang X, Liang C, Li Y, Qiao L, Ai Z, Xue S, Liu G. Interactive effects of microplastics and glyphosate on the dynamics of soil dissolved organic matter in a Chinese loess soil. CATENA, 2019, 182: 104177, coi: 1:CAS:528:DC%2BC1MXhsVajtr3O

[] Liu T, Chen X, Gong X, Lubbers IM, Jiang Y, Feng W, Li X, Whalen JK, Bonkowski M, Griffiths BS, Hu F, Liu M. Earthworms coordinate soil biota to improve multiple ecosystem functions. Curr Biol, 2019, 29(20): 3420-3429, coi: 1:CAS:528:DC%2BC1MXhvFersr%2FN

[] Liu H, Du X, Li Y, Han X, Li B, Zhang X, Li Q, Liang W. Organic substitutions improve soil quality and maize yield through increasing soil microbial diversity. J Cleaner Prod, 2022, 347: 131323, coi: 1:CAS:528:DC%2BB38XhtFyrsrjI

[] Liu M, Linna C, Ma S, Ma Q, Song W, Shen M, Song L, Cui K, Zhou Y, Wang L. Biochar combined with organic and inorganic fertilizers promoted the rapeseed nutrient uptake and improved the purple soil quality. Front Nutr, 2022, 9: 997151,

[] Liu Q, Meki K, Zheng H, Yuan Y, Shao M, Luo X, Li X, Jiang Z, Li F, Xing B. Biochar application in remediating salt-affected soil to achieve carbon neutrality and abate climate change. Biochar, 2023, 5(1): 45, coi: 1:CAS:528:DC%2BB3sXhsF2iu7vE

[] Luo G, Rensing C, Chen H, Liu M, Wang M, Guo S, Ling N, Shen Q. Deciphering the associations between soil microbial diversity and ecosystem multifunctionality driven by long-term fertilization management. Funct Ecol, 2018, 32(4): 1103-1116,

[] Luo G, Wang T, Li K, Li L, Zhang J, Guo S, Ling N, Shen Q. Historical nitrogen deposition and straw addition facilitate the resistance of soil multifunctionality to drying-wetting cycles. Appl Environ Microb, 2019, 85(8): e02251-e2318, coi: 1:CAS:528:DC%2BC1MXps1yqsL8%3D

[] Luo G, Xue C, Jiang Q, Xiao Y, Zhang F, Guo S. Soil carbon, nitrogen, and phosphorus cycling microbial populations and their resistance to global change depend on soil C:N: P stoichiometry. mSystems, 2020, 5(3): e00162-20, coi: 1:CAS:528:DC%2BB3cXitlyjtL7J

[] Maron PA, Sarr A, Kaisermann A, Lévêque J, Mathieu O, Guigue J, Karimi B, Bernard L, Dequiedt S, Terrat S, Chabbi A, Ranjard L. High microbial diversity promotes soil ecosystem functioning. Appl Environ Microb, 2018, 84(9): e02738-e2817, coi: 1:CAS:528:DC%2BC1cXhslGksL7P

[] Neina D. The role of soil pH in plant nutrition and soil remediation. Appl Environ Soil Sci, 2019, 2019: 1-9,

[] Ren T, Liao J, Jin L, Delgado-Baquerizo M, Ruan H. Application of biogas-slurry and biochar improves soil multifunctionality in a poplar plantation during afforestation processes. Plant Soil, 2023,

[] Saha B, Saha S, Roy PD, Padhan D, Pati S, Hazra GC. Meena VS. Microbial transformation of sulphur: an approach to combat the sulphur deficiencies in agricultural soils. Role of rhizospheric microbes in soil: Volume 2: nutrient management and crop improvement, 2018 Berlin Springer 77-97,

[] Saifullah DS, Naeem A, Rengel Z, Naidu R. Biochar application for the remediation of salt-affected soils: challenges and opportunities. Sci Total Environ, 2018, 625: 320-335, coi: 1:CAS:528:DC%2BC1cXhtlGntQ%3D%3D

[] Singh VK, Rai S, Singh D, Upadhyay RS. Dubey SK, Verma SK. Application of soil microorganisms for agricultural and environmental sustainability: a review. Plant, soil and microbes in tropical ecosystems, 2021 Berlin Springer 151-175,

[] Sun R, Guo X, Wang D, Chu H. Effects of long-term application of chemical and organic fertilizers on the abundance of microbial communities involved in the nitrogen cycle. Appl Soil Ecol, 2015, 95: 171-178,

[] Wan W, Tan J, Wang Y, Qin Y, He H, Wu H, Zuo W, He D. Responses of the rhizosphere bacterial community in acidic crop soil to pH: changes in diversity, composition, interaction, and function. Sci Total Environ, 2020, 700: 134418, coi: 1:CAS:528:DC%2BC1MXhvFOqtL7K

[] Wang J, Xie J, Li L, Luo Z, Zhang R, Wang L, Jiang Y. The impact of fertilizer amendments on soil autotrophic bacteria and carbon emissions in maize field on the semiarid Loess Plateau. Front Microb, 2021, 12: 664120,

[] Wang T, Duan Y, Liu G, Shang X, Liu L, Zhang K, Li J, Zou Z, Zhu X, Fang W. Tea plantation intercropping green manure enhances soil functional microbial abundance and multifunctionality resistance to drying-rewetting cycles. Sci Total Environ, 2022, 810: 151282, coi: 1:CAS:528:DC%2BB3MXisVyrsr%2FF

[] Wang X, Ge H, Fang Y, Liu C, Eltohamy KM, Wang Z, Liang X. Biochar reduces colloidal phosphorus in leachate by regulating phoD- and phoC-harboring microbial communities during drying/rewetting cycles. Biochar, 2023, 5(1): 1-15,

[] Waqas MA, Li Y, Smith P, Wang X, Ashraf MN, Noor MA, Amou M, Shi S, Zhu Y, Li J, Wan Y, Qin X, Gao Q, Liu S. The influence of nutrient management on soil organic carbon storage, crop production, and yield stability varies under different climates. J Clean Prod, 2020, 268: 121922, coi: 1:CAS:528:DC%2BB3cXhtVaiu7jM

[] Wu J, Sha C, Wang M, Ye C, Li P, Huang S. Effect of organic fertilizer on soil bacteria in maize fields. Land, 2021, 10(3): 328,

[] Xiao Y, Peng Y, Peng F, Zhang Y, Yu W, Sun M, Gao X. Effects of concentrated application of soil conditioners on soil–air permeability and absorption of nitrogen by young peach trees. Soil Sci Plant Nutr, 2018, 64(3): 423-432, coi: 1:CAS:528:DC%2BC1cXjslOjs7k%3D

[] Yan B, Zhang Y, Wang Y, Rong X, Peng J, Fei J, Luo G. Biochar amendments combined with organic fertilizer improve maize productivity and mitigate nutrient loss by regulating the C–N–P stoichiometry of soil, microbiome, and enzymes. Chemosphere, 2023, 324: 138293, coi: 1:CAS:528:DC%2BB3sXltV2nu7w%3D

[] Yuan Z, Ali A, Ruiz-Benito P, Jucker T, Mori AS, Wang S, Zhang X, Li H, Hao Z, Wang X, Loreau M. Above-and below-ground biodiversity jointly regulate temperate forest multifunctionality along a local-scale environmental gradient. J Ecol, 2020, 108(5): 2012-2024,

[] Zabala JA, Martínez-Paz JM, Alcon F. A comprehensive approach for agroecosystem services and disservices valuation. Sci Total Environ, 2021, 768: 144859, coi: 1:CAS:528:DC%2BB3MXhsVChurw%3D

[] Zak D, Stutter M, Jensen HS, Egemose S, Carstensen MV, Audet J, Strand JA, Feuerbach P, Hoffmann CC, Christen B, Knudsen M, Stockan J, Watson H, Heckrath G, Kronvang B. An assessment of the multifunctionality of integrated buffer zones in Northwestern Europe. J Environ Qual, 2019, 48(2): 362-375, coi: 1:CAS:528:DC%2BC1MXps1Ojt74%3D

[] Zhang Y, Wang F, Zhang J, Zhu T, Lin C, Müller C, Cai Z. Cattle manure and straw have contrasting effects on organic nitrogen mineralization pathways in a subtropical paddy soil. Acta Agr Scand B-S P, 2015, 65(7): 619-628

[] Zhang Y, Yan J, Rong X, Han Y, Yang Z, Hou K, Zhao H, Hu W. Responses of maize yield, nitrogen and phosphorus runoff losses and soil properties to biochar and organic fertilizer application in a light-loamy fluvo-aquic soil. Agr Ecosyst Environ, 2021, 314: 107433, coi: 1:CAS:528:DC%2BB3MXhtlKrsLvO

[] Zhang YJ, Gao W, Luan HA, Tang JW, Li RN, Li MY, Zhang HZ, Huang SW. Effects of a decade of organic fertilizer substitution on vegetable yield and soil phosphorus pools, phosphatase activities, and the microbial community in a greenhouse vegetable production system. J Integr Agr, 2022, 21(7): 2119-2133, coi: 1:CAS:528:DC%2BB38XisFKnsbzL

[] Zhao Q, Wang Y, Xu Z, Yun J, Yu Z. Unravelling how biochar and dung amendments determine the functional structure and community assembly related to methane metabolisms in grassland soils. Biochar, 2022, 4(1): 49, coi: 1:CAS:528:DC%2BB38XitF2kurfP

[] Zhao Y, Wang X, Yao G, Lin Z, Xu L, Jiang Y, Jin Z, Shan S, Ping L. Advances in the effects of biochar on microbial ecological function in soil and crop quality. Sustainability, 2022, 14: 10411, coi: 1:CAS:528:DC%2BB38XitlWrsrbF

[] Zheng B, Zhu Y, Sardans J, Peñuelas J, Su J. QMEC: a tool for high-throughput quantitative assessment of microbial functional potential in C, N, P, and S biogeochemical cycling. Sci China Life Sci, 2018, 61(12): 1451-1462, coi: 1:CAS:528:DC%2BC1cXhsFOgsL7P

[] Zheng B, Zhang D, Wang Y, Hao X, Wadaan MAM, Hozzein WN, Peñuelas J, Zhu Y, Yang X. Responses to soil pH gradients of inorganic phosphate solubilizing bacteria community. Sci Rep, 2019, 9(1): 25,

[] Zhou W, He P, Li S, Lin B. Mineralization of organic sulfur in paddy soils under flooded conditions and its availability to plants. Geoderma, 2005, 125(1–2): 85-93, coi: 1:CAS:528:DC%2BD2MXks1Oh

[] Zhou G, Gao S, Lu Y, Liao Y, Nie J, Cao W. Co-incorporation of green manure and rice straw improves rice production, soil chemical, biochemical and microbiological properties in a typical paddy field in southern China. Soil Tillage Res, 2020, 197: 104499,

Funding

National Natural Science Foundation of China(42107262); Key Field Research and Development Program of Hunan Province(2023NK2028)