Biochar-induced changes in soil microbial communities: a comparison of two feedstocks and pyrolysis temperatures
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
National Competence Centre BIOCIRCL, project no. TN02000044
Technology Agency of the Czech Republic
Grant No. 24-10238L
Czech Science Foundation
PubMed
39516989
PubMed Central
PMC11549753
DOI
10.1186/s40793-024-00631-z
PII: 10.1186/s40793-024-00631-z
Knihovny.cz E-zdroje
- Klíčová slova
- Biochar, Enzymatic activity, Microbial composition, Organic waste recycling, Soil quality,
- Publikační typ
- časopisecké články MeSH
BACKGROUND: The application of a biochar in agronomical soil offers a dual benefit of improving soil quality and sustainable waste recycling. However, utilizing new organic waste sources requires exploring the biochar's production conditions and application parameters. Woodchips (W) and bone-meat residues (BM) after mechanical deboning from a poultry slaughterhouse were subjected to pyrolysis at 300 °C and 500 °C and applied to cambisol and luvisol soils at ratios of 2% and 5% (w/w). RESULTS: Initially, the impact of these biochar amendments on soil prokaryotes was studied over the course of one year. The influence of biochar variants was further studied on prokaryotes and fungi living in the soil, rhizosphere, and roots of Triticum aestivum L., as well as on soil enzymatic activity. Feedstock type, pyrolysis temperature, application dose, and soil type all played significant roles in shaping both soil and endophytic microbial communities. BM treated at a lower pyrolysis temperature of 300 °C increased the relative abundance of Pseudomonadota while causing a substantial decrease in soil microbial diversity. Conversely, BM prepared at 500 °C favored the growth of microbes known for their involvement in various nutrient cycles. The W biochar, especially when pyrolysed at 500 °C, notably affected microbial communities, particularly in acidic cambisol compared to luvisol. In cambisol, biochar treatments had a significant impact on prokaryotic root endophytes of T. aestivum L. Additionally, variations in prokaryotic community structure of the rhizosphere depended on the increasing distance from the root system (2, 4, and 6 mm). The BM biochar enhanced the activity of acid phosphatase, whereas the W biochar increased the activity of enzymes involved in the carbon cycle (β-glucosidase, β-xylosidase, and β-N-acetylglucosaminidase). CONCLUSIONS: These results collectively suggest, that under appropriate production conditions, biochar can exert a positive influence on soil microorganisms, with their response closely tied to the biochar feedstock composition. Such insights are crucial for optimizing biochar application in agricultural practices to enhance soil health.
Zobrazit více v PubMed
Adam G, Duncan H. Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils. Soil Biol Biochem. 2001;33(7–8):943–51. DOI
Adamczyk M, Perez-Mon C, Gunz S, Frey B. Strong shifts in microbial community structure are associated with increased litter input rather than temperature in High Arctic soils. Soil Biol Biochem. 2020;151:108054. 10.1016/j.soilbio.2020.108054. DOI
Adetunji AT, Lewu FB, Mulidzi R, Ncube B. The biological activities of DOI
Ali A, Guo D, Zhang Y, et al. Using bamboo biochar with compost for the stabilization and phytotoxicity reduction of heavy metals in mine-contaminated soils of China. Sci Rep. 2017;7:2690. 10.1038/s41598-017-03045-9. PubMed DOI PMC
Ali A, Guo D, Arockiam J, et al. Application of wood biochar in polluted soils stabilized the toxic metals and enhanced wheat ( PubMed DOI
Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001;26:32–46.
Anderson MJ, Walsh DCI. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol Monogr. 2013;83:557–74. DOI
Azeem M, Ali A, Arockiam J, et al. Bone-derived biochar improved soil quality and reduced Cd and Zn phytoavailability in a multi-metal contaminated mining soil. Environ Pollut. 2021;277:116800. 10.1016/j.envpol.2021.116800. PubMed DOI
Baetz U, Martinoia E. Root exudates: the hidden part of plant defense. Trends Plant Sci. 2014;19:90–8. 10.1016/j.tplants.2013.11.006. PubMed DOI
Barra PJ, Inostroza NG, Acuña JJ, et al. Formulation of bacterial consortia from avocado DOI
Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Ser B Stat Methodol. 1995;57:289–300. 10.1111/j.2517-6161.1995.tb02031.x. DOI
Bessadok K, Navarro-Torre S, Pajuelo E, et al. The ACC-Deaminase Producing Bacterium PubMed DOI PMC
Bosetto A, Justo PI, Zanardi B, et al. Research Progress Concerning Fungal and Bacterial PubMed DOI
Bruns MA, Byrne LB. Scale Model of a Soil Aggregate and Associated Organisms: A Teaching Tool for Soil Ecology. JNRLSE. 2004;33:85–91. 10.2134/jnrlse.2004.0085. DOI
Buss W, Bogush A, Ignatyev K, Mašek O. Unlocking the Fertilizer Potential of Waste-Derived Biochar. ACS Sustainable Chem Eng. 2020;8:12295–303. 10.1021/acssuschemeng.0c04336. DOI
Callahan BJ. (2018) Silva taxonomic training data formatted for DADA2 (Silva version 132) [Data set]. Zenodo. 10.5281/zenodo.1172783. DOI
Callahan BJ, McMurdie PJ, Rosen MJ, et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016a;13:581–3. 10.1038/nmeth.3869. PubMed DOI PMC
Callahan BJ, Sankaran K, Fukuyama JA, et al. Bioconductor workflow for microbiome data analysis: from raw reads to community analyses. F1000Res. 2016b;5:1492. 10.12688/f1000research.8986.1. PubMed DOI PMC
Chen S, Qi G, Ma G, Zhao X. Biochar amendment controlled bacterial wilt through changing soil chemical properties and microbial community. Microbiol Res. 2020;231:126373. 10.1016/j.micres.2019.126373. PubMed DOI
Coombs JT, Franco CMM. Isolation and Identification of Actinobacteria from Surface-Sterilized Wheat Roots. Appl Environ Microbiol. 2003;69:5603–8. 10.1128/AEM.69.9.5603-5608.2003. PubMed DOI PMC
Cruz-Paredes C, Bang-Andreasen T, Christensen S, et al. Bacteria Respond Stronger Than Fungi Across a Steep Wood Ash-Driven pH Gradient. Front Glob Change. 2021;4:781844. 10.3389/ffgc.2021.781844. DOI
DeForest JL. The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and l-DOPA. Soil Biol Biochem. 2009;41:1180–6. 10.1016/j.soilbio.2009.02.029. DOI
Ding Y, Liu Y, Liu S et al. (2016) Biochar to improve soil fertility. A review. ASD 36:. 10.1007/s13593-016-0372-z
Divan Baldani VL, Baldani JI, Döbereiner J. Inoculation of rice plants with the endophytic diazotrophs DOI
Ekenler M, Tabatabai MA. DOI
Elzobair KA, Stromberger ME, Ippolito JA. Stabilizing effect of biochar on soil extracellular enzymes after a denaturing stress. Chemosphere. 2016;142:114–9. 10.1016/j.chemosphere.2015.03.018. PubMed DOI
Estrada GA, Baldani VLD, de Oliveira DM, et al. Selection of phosphate-solubilizing diazotrophic DOI
Fang K, Bao Z-S-N, Chen L, et al. Growth-promoting characteristics of potential nitrogen-fixing bacteria in the root of an invasive plant PubMed DOI PMC
Fierer N, Bradford MA, Jackson RB. Toward an ecological classification of soil bacteria. Ecology. 2007;88:1354–64. 10.1890/05-1839. PubMed DOI
Fitz WJ, Wenzel WW, Wieshammer G, Istenic B. Microtome sectioning causes artifacts in rhizobox experiments. Plant Soil. 2003;256:455–62. DOI
Foster EJ, Hansen N, Wallenstein M, Cotrufo MF. Biochar and manure amendments impact soil nutrients and microbial enzymatic activities in a semi-arid irrigated maize cropping system. Agric Ecosyst Environ. 2016;233:404–14. 10.1016/j.agee.2016.09.029. DOI
Frank A, Saldierna Guzmán J, Shay J. Transmission of Bacterial Endophytes. Microorganisms. 2017;5:70. 10.3390/microorganisms5040070. PubMed DOI PMC
Fraraccio S, Strejcek M, Dolinova I, et al. Secondary compound hypothesis revisited: Selected plant secondary metabolites promote bacterial degradation of cis-1,2-dichloroethylene (cDCE). Sci Rep. 2017;7. 10.1038/s41598-017-07760-1. PubMed PMC
Gaiero JR, McCall CA, Thompson KA, et al. Inside the root microbiome: Bacterial root endophytes and plant growth promotion. Am J Bot. 2013;100:1738–50. 10.3732/ajb.1200572. PubMed DOI
Geisseler D, Horwath WR. Relationship between carbon and nitrogen availability and extracellular enzyme activities in soil. Pedobiologia. 2009;53:87–98. 10.1016/j.pedobi.2009.06.002. DOI
Ghani WAWAK, Mohd A, da Silva G, et al. Biochar production from waste rubber-wood-sawdust and its potential use in C sequestration: Chemical and physical characterization. Ind Crops Prod. 2013;44:18–24. 10.1016/j.indcrop.2012.10.017. DOI
Glæsner N, Hansen HCB, Hu Y, et al. Low crystalline apatite in bone char produced at low temperature ameliorates phosphorus-deficient soils. Chemosphere. 2019;223:723–30. 10.1016/j.chemosphere.2019.02.048. PubMed DOI
Glaser B, Lehr V-I. Biochar effects on phosphorus availability in agricultural soils: A meta-analysis. Sci Rep. 2019;9:9338. 10.1038/s41598-019-45693-z. PubMed DOI PMC
Haack FS, Poehlein A, Kröger C et al. (2016) Molecular Keys to the PubMed PMC
Haegeman B, Hamelin J, Moriarty J, et al. Robust estimation of microbial diversity in theory and in practice. ISME J. 2013;7:1092–101. 10.1038/ismej.2013.10. PubMed DOI PMC
Ibarra-Galeana JA, Castro-Martínez C, Fierro-Coronado RA, et al. Characterization of phosphate-solubilizing bacteria exhibiting the potential for growth promotion and phosphorus nutrition improvement in maize ( DOI
Ishii S, Ashida N, Ohno H, et al. PubMed DOI
Ives AR, Carpenter SR. Stability and Diversity of Ecosystems. Science. 2007;317:58–62. 10.1126/science.1133258. PubMed DOI
Ji M, Wang X, Usman M, et al. Effects of different feedstocks-based biochar on soil remediation: A review. Environ Pollut. 2022;294:118655. 10.1016/j.envpol.2021.118655. PubMed DOI
Jia Y, Siebers N, Panten K, Kruse J. Fate and availability of phosphorus from bone char with and without sulfur modification in soil size fractions after five-year field fertilizations. Soil Tillage Res. 2023;231:105720. 10.1016/j.still.2023.105720. DOI
Jiang S, Huang J, Lu H, et al. Optimisation for assay of fluorescein diacetate hydrolytic activity as a sensitive tool to evaluate impacts of pollutants and nutrients on microbial activity in coastal sediments. Mar Pollut Bull. 2016;110:424–31. 10.1016/j.marpolbul.2016.06.031. PubMed DOI
Jin Y, Liang X, He M, et al. Manure biochar influence upon soil properties, phosphorus distribution and phosphatase activities: A microcosm incubation study. Chemosphere. 2016;142:128–35. 10.1016/j.chemosphere.2015.07.015. PubMed DOI
Kandel S, Joubert P, Doty S. Bacterial Endophyte Colonization and Distribution within Plants. Microorganisms. 2017;5:77. 10.3390/microorganisms5040077. PubMed DOI PMC
Karimi B, Maron PA, Chemidlin-Prevost Boure N, et al. Microbial diversity and ecological networks as indicators of environmental quality. Environ Chem Lett. 2017;15:265–81. 10.1007/s10311-017-0614-6. DOI
Kennedy AC, Smith KL. Soil microbial diversity and the sustainability of agricultural soils. Plant Soil. 1995;170:75–86. 10.1007/BF02183056.
Khan AA, Jilani G, Akhtar MS, et al. Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. J Agric Biol Sci. 2009;1:48–58.
Kracmarova M, Karpiskova J, Uhlik O, et al. Microbial Communities in Soils and Endosphere of PubMed DOI PMC
Kracmarova M, Kratochvilova H, Uhlik O, et al. Response of Soil Microbes and Soil Enzymatic Activity to 20 Years of Fertilization. Agronomy. 2020b;10:1542. 10.3390/agronomy10101542. DOI
Kuźniar A, Włodarczyk K, Grządziel J, et al. Culture-independent analysis of an endophytic core microbiome in two species of wheat: PubMed DOI
Latini A, Bacci G, Teodoro M, et al. The Impact of Soil-Applied Biochars From Different Vegetal Feedstocks on Durum Wheat Plant Performance and Rhizospheric Bacterial Microbiota in Low Metal-Contaminated Soil. Front Microbiol. 2019;10. 10.3389/fmicb.2019.02694. PubMed PMC
Lehmann J, Joseph S. Biochar for Environmental Management: Science and Technology. Oxfordshire: Routledge; 2012.
Li T, Zhou Q. The key role of PubMed DOI
Li X, Wang T, Chang SX, et al. Biochar increases soil microbial biomass but has variable effects on microbial diversity: A meta-analysis. Sci Total Environ. 2020;749:141593. 10.1016/j.scitotenv.2020.141593. PubMed DOI
Liu J, Liu M, Wu M, et al. Soil pH rather than nutrients drive changes in microbial community following long-term fertilization in acidic Ultisols of southern China. J Soils Sediments. 2018;18:1853–64. 10.1007/s11368-018-1934-2. DOI
Lopes ÉMG, Reis MM, Frazão LA, et al. Biochar increases enzyme activity and total microbial quality of soil grown with sugarcane. Environ Technol Innov. 2021;21:101270. 10.1016/j.eti.2020.101270. DOI
Lopez-Echartea E, Strejcek M, Mukherjee S, et al. Bacterial succession in oil-contaminated soil under phytoremediation with poplars. Chemosphere. 2020;243:125242. 10.1016/j.chemosphere.2019.125242. PubMed DOI
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. 10.1186/s13059-014-0550-8. PubMed DOI PMC
Luo Y, Dungait JAJ, Zhao X, et al. Pyrolysis temperature during biochar production alters its subsequent utilization by microorganisms in an acid arable soil. Land Degrad Dev. 2018;29:2183–8. 10.1002/ldr.2846. DOI
McMurdie PJ, Holmes S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE. 2013;8:e61217. 10.1371/journal.pone.0061217. PubMed DOI PMC
Miliute I, Buzaite O, Baniulis D, Stanys V. Bacterial endophytes in agricultural crops and their role in stress tolerance: a review. Zemdirbyste. 2015;102:465–78. 10.13080/z-a.2015.102.060. DOI
Nilsson RH, Ryberg M, Abarenkov K, et al. The ITS region as a target for characterization of fungal communities using emerging sequencing technologies. FEMS Microbiol Lett. 2009;296:97–101. 10.1111/j.1574-6968.2009.01618.x. PubMed DOI
Oksanen J, Blanchet FG, Kindt R et al. (2019) vegan: Community Ecology Package. R package version 2.5-6.
Oni BA, Oziegbe O, Olawole OO. Significance of biochar application to the environment and economy. Ann Agric Sci. 2019;64:222–36. 10.1016/j.aoas.2019.12.006. DOI
Pan S-Y, Dong C-D, Su J-F, et al. The Role of Biochar in Regulating the Carbon, Phosphorus, and Nitrogen Cycles Exemplified by Soil Systems. Sustainability. 2021;13:5612. 10.3390/su13105612. DOI
Pande A, Pandey P, Mehra S, et al. Phenotypic and genotypic characterization of phosphate solubilizing bacteria and their efficiency on the growth of maize. JGEB. 2017;15:379–91. 10.1016/j.jgeb.2017.06.005. PubMed DOI PMC
Pedrinho A, Mendes LW, de Araujo Pereira AP, et al. Soil microbial diversity plays an important role in resisting and restoring degraded ecosystems. Plant Soil. 2024;500:325–49. 10.1007/s11104-024-06489-x. DOI
Penn CJ, Camberato JJ. A Critical Review on Soil Chemical Processes that Control How Soil pH Affects Phosphorus Availability to Plants. Agriculture. 2019;9:120. 10.3390/agriculture9060120. DOI
Perazzolli M, Vicelli B, Antonielli L, et al. Simulated global warming affects endophytic bacterial and fungal communities of Antarctic pearlwort leaves and some bacterial isolates support plant growth at low temperatures. Sci Rep. 2022;12:18839. 10.1038/s41598-022-23582-2. PubMed DOI PMC
R Core Team. R: A language and environment for statistical computing in. R Foundation for Statistical Computing; 2017.
Rodriguez H, Gonzalez T, Goire I, Bashan Y. Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium PubMed DOI
Schmalenberger A, Fox A. Bacterial Mobilization of Nutrients From Biochar-Amended Soils. Advances in Applied Microbiology. Elsevier; 2016. pp. 109–59. PubMed
Sharma SK, Ramesh A, Sharma MP, et al. Microbial Community Structure and Diversity as Indicators for Evaluating Soil Quality. In: Lichtfouse E, editor. Biodiversity, Biofuels, Agroforestry and Conservation Agriculture. Dordrecht: Springer Netherlands; 2010. pp. 317–58.
Sharma S, Kumar V, Tripathi RB. Isolation of Phosphate Solubilizing Microorganism (PSMs) From Soil. JMB. 2011;2:90–5.
Sharma M, Khurana H, Singh DN, Negi RK. The genus PubMed DOI
Shaw LJ, Nicol GW, Smith Z, et al. PubMed DOI
Stiborova H, Kronusova O, Kastanek P, et al. Waste products from the poultry industry: a source of high-value dietary supplements. J Chem Technol Biotechnol. 2020;95:985–92. 10.1002/jctb.6131. DOI
Stott DE, Andrews SS, Liebig MA, et al. Evaluation of DOI
Száková J, Stiborová H, Mercl F, et al. Woodchips biochar
Tang L, Shen Z, Duan X, et al. Evaluating the potential of charred bone as P hotspot assisted by phosphate-solubilizing bacteria. Sci Total Environ. 2019;696:133965. 10.1016/j.scitotenv.2019.133965. PubMed DOI
Taylor DL, Walters WA, Lennon NJ, et al. Accurate Estimation of Fungal Diversity and Abundance through Improved Lineage-Specific Primers Optimized for Illumina Amplicon Sequencing. AEM. 2016;82:7217–26. 10.1128/AEM.02576-16. PubMed DOI PMC
Thiruvengadam S, Ramki R, Rohini S, et al. Isolation, Screening and Evaluation of Multifunctional Strains of High Efficient Phosphate Solubilizing Microbes from Rhizosphere Soil. Rese Jour Pharm Technol. 2020;13:1825. 10.5958/0974-360X.2020.00328.5. DOI
Tomczyk A, Sokołowska Z, Boguta P. Biochar physicochemical properties: pyrolysis temperature and feedstock kind effects. Rev Environ Sci Biotechnol. 2020;19:191–215. 10.1007/s11157-020-09523-3. DOI
Van den Brink PJ, Braak CJF. Ecological and statistical evaluation of effects of pesticides in freshwater model ecosystems. Environ Toxicol Chem. 1999;18:138–48.
van den Brink PJ, den Besten PJ, bij, de Vaate A, ter Braak CJF. (2009) Principal response curves technique for the analysis of multivariate biomonitoring time series. Environ Monit Assess 152:271–281. 10.1007/s10661-008-0314-6 PubMed
Vassilev N, Martos E, Mendes G, et al. Biochar of animal origin: a sustainable solution to the global problem of high-grade rock phosphate scarcity? Animal biochar solubilisation. J Sci Food Agric. 2013;93:1799–804. 10.1002/jsfa.6130. PubMed DOI
Vaughn SF, Kenar JA, Thompson AR, Peterson SC. Comparison of biochars derived from wood pellets and pelletized wheat straw as replacements for peat in potting substrates. Ind Crops Prod. 2013;51:437–43. 10.1016/j.indcrop.2013.10.010. DOI
Wall DH, Nielsen UN, Six J. Soil biodiversity and human health. Nature. 2015;528:69–76. 10.1038/nature15744. PubMed DOI
Wang J. Preparation, modification and environmental application of biochar: A review. J Clean Prod. 2019;227:1002–22. DOI
Wang X, Zhou W, Liang G, et al. Characteristics of maize biochar with different pyrolysis temperatures and its effects on organic carbon, nitrogen and enzymatic activities after addition to fluvo-aquic soil. Sci Total Environ. 2015;538:137–44. 10.1016/j.scitotenv.2015.08.026. PubMed DOI
Warnock DD, Lehmann J, Kuyper TW, Rillig MC. Mycorrhizal responses to biochar in soil – concepts and mechanisms. Plant Soil. 2007;300:9–20. 10.1007/s11104-007-9391-5. DOI
Wenzel WW, Wieshammer G, Fitz WJ, Puschenreiter M. Novel rhizobox design to assess rhizosphere characteristics at high spatial resolution. Plant Soil. 2001;237:37–45. DOI
White JF, Kingsley KL, Zhang Q, et al. Review: Endophytic microbes and their potential applications in crop management. Pest Manag Sci. 2019;75:2558–65. 10.1002/ps.5527. PubMed DOI PMC
Wickham H. ggplot2 - Elegant Graphics for Data Analysis (2nd Edition). J Stat Soft. 2017;77. 10.18637/jss.v077.b02.
Wittmann C, Kähkönen MA, Ilvesniemi H, et al. Areal activities and stratification of hydrolytic enzymes involved in the biochemical cycles of carbon, nitrogen, sulphur and phosphorus in podsolized boreal forest soils. Soil Biol Biochem. 2004;36:425–33. 10.1016/j.soilbio.2003.10.019. DOI
Woolet J, Whitman T. Pyrogenic organic matter effects on soil bacterial community composition. Soil Biol Biochem. 2020;141:107678. 10.1016/j.soilbio.2019.107678. DOI
Xun W, Liu Y, Li W, et al. Specialized metabolic functions of keystone taxa sustain soil microbiome stability. Microbiome. 2021;9:35. 10.1186/s40168-020-00985-9. PubMed DOI PMC
Yao F, Yang S, Wang Z, et al. Microbial Taxa Distribution Is Associated with Ecological Trophic Cascades along an Elevation Gradient. Front Microbiol. 2017;8:2071. 10.3389/fmicb.2017.02071. PubMed DOI PMC
Zhang J, Kim Y-J, Hoang V-A, et al. PubMed DOI
Zhang L, Jing Y, Xiang Y, et al. Responses of soil microbial community structure changes and activities to biochar addition: A meta-analysis. Sci Total Environ. 2018;643:926–35. 10.1016/j.scitotenv.2018.06.231. PubMed DOI
Zhang M, Riaz M, Zhang L, et al. Biochar Induces Changes to Basic Soil Properties and Bacterial Communities of Different Soils to Varying Degrees at 25 mm Rainfall: More Effective on Acidic Soils. Front Microbiol. 2019;10:1321. 10.3389/fmicb.2019.01321. PubMed DOI PMC
Zhao L, Cao X, Mašek O, Zimmerman A. Heterogeneity of biochar properties as a function of feedstock sources and production temperatures. J Hazard Mater. 2013;256–257:1–9. 10.1016/j.jhazmat.2013.04.015. PubMed DOI
Zhao S-X, Ta N, Wang X-D. Effect of Temperature on the Structural and Physicochemical Properties of Biochar with Apple Tree Branches as Feedstock Material. Energies. 2017;10:1293. 10.3390/en10091293. DOI
Zheng H, Liu D, Liao X, et al. Field-aged biochar enhances soil organic carbon by increasing recalcitrant organic carbon fractions and making microbial communities more conducive to carbon sequestration. Agric Ecosyst Environ. 2022;340:108177. 10.1016/j.agee.2022.108177. DOI
Zhou X, Guo Z, Chen C, Jia Z. Soil microbial community structure and diversity are largely influenced by soil pH and nutrient quality in 78-year-old tree plantations. Biogeosciences. 2017;14:2101–11. 10.5194/bg-14-2101-2017. DOI
Zhou C, Heal K, Tigabu M, et al. Biochar addition to forest plantation soil enhances phosphorus availability and soil bacterial community diversity. Ecol Manag. 2020;455:117635. 10.1016/j.foreco.2019.117635. DOI
Zwetsloot MJ, Lehmann J, Bauerle T, et al. Phosphorus availability from bone char in a P-fixing soil influenced by root-mycorrhizae-biochar interactions. Plant Soil. 2016;408:95–105. 10.1007/s11104-016-2905-2. DOI