Decoupled fungal and bacterial functional responses to biochar amendment drive rhizosphere priming effect on soil organic carbon mineralization

Abstract

•	Biochar application altered rhizosphere priming effects by − 116.96% to + 171.59% during maize growth.
•	Biochar application increased total soil organic carbon and boosted bacterial abundance.
•	Biochar-plant interactions accelerated soil carbon mineralization and accumulation.

References

[1] AbrolV, Ben-HurM, VerheijenFGA, KeizerJJ, MartinsMAS, TenawH, TchehanskyL, GraberER. Biochar effects on soil water infiltration and erosion under seal formation conditions: rainfall simulation experiment. J Soils Sediments, 2016, 16(12): 2709-2719

[2] AmelootN, GraberER, VerheijenFGA, De NeveS. Interactions between biochar stability and soil organisms: review and research needs. Eur J Soil Sci, 2013, 64(4): 379-390

[3] BarabásiA-L, GulbahceN, LoscalzoJ. Network medicine: a network-based approach to human disease. Nat Rev Genet, 2010, 12(1): 56-68

[4] BarberánA, BatesST, CasamayorEO, FiererN. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J, 2012, 6(2): 343-351

[5] Barbosa de SousaÁM, Soares SantosRR, GehringC. Charcoal in Amazonian paddy soil—nutrient availability, rice growth and methane emissions. J Plant Nutr Soil Sci, 2014, 177(1): 39-47

[6] BarnettSE, YoungblutND, BuckleyDH. Bacterial community dynamics explain carbon mineralization and assimilation in soils of different land-use history. Environ Microbiol, 2022, 24(11): 5230-5247

[7] BastianM, HeymannS, JacomyM. Gephi: an open source software for exploring and manipulating networks. Proc Int AAAI Confer Web Social Media, 2009, 3(1): 361-362

[8] BastidaF, EldridgeDJ, GarciaC, Kenny PngG, BardgettRD, Delgado-BaquerizoM. Soil microbial diversity-biomass relationships are driven by soil carbon content across global biomes. ISME J, 2021, 15(7): 2081-2091

[9] BiddleJF, Fitz-GibbonS, SchusterSC, BrenchleyJE, HouseCH. Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. P Natl Acad Sci USA, 2008, 105(30): 10583-10588

[10] BokulichNA, KaehlerBD, RideoutJR, DillonM, BolyenE, KnightR, HuttleyGA, Gregory CaporasoJ. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2's q2-feature-classifier plugin. Microbiome, 2018, 6(1): 90

[11] BolyenE, RideoutJR, DillonMR, BokulichNA, AbnetCC, Al-GhalithGA, AlexanderH, AlmEJ, ArumugamM, AsnicarF, BaiY, BisanzJE, BittingerK, BrejnrodA, BrislawnCJ, BrownCT, CallahanBJ, Caraballo-RodriguezAM, ChaseJ, CopeEK, Da SilvaR, DienerC, DorresteinPC, DouglasGM, DurallDM, DuvalletC, EdwardsonCF, ErnstM, EstakiM, FouquierJ, GauglitzJM, GibbonsSM, GibsonDL, GonzalezA, GorlickK, GuoJ, HillmannB, HolmesS, HolsteH, HuttenhowerC, HuttleyGA, JanssenS, JarmuschAK, JiangL, KaehlerBD, KangKB, KeefeCR, KeimP, KelleyST, KnightsD, KoesterI, KosciolekT, KrepsJ, LangilleMGI, LeeJ, LeyR, LiuYX, LoftfieldE, LozuponeC, MaherM, MarotzC, MartinBD, McDonaldD, McIverLJ, MelnikAV, MetcalfJL, MorganSC, MortonJT, NaimeyAT, Navas-MolinaJA, NothiasLF, OrchanianSB, PearsonT, PeoplesSL, PetrasD, PreussML, PruesseE, RasmussenLB, RiversA, RobesonMS2nd, RosenthalP, SegataN, ShafferM, ShifferA, SinhaR, SongSJ, SpearJR, SwaffordAD, ThompsonLR, TorresPJ, TrinhP, TripathiA, TurnbaughPJ, Ul-HasanS, van der HooftJJJ, VargasF, Vazquez-BaezaY, VogtmannE, von HippelM, WaltersW, WanY, WangM, WarrenJ, WeberKC, WilliamsonCHD, WillisAD, XuZZ, ZaneveldJR, ZhangY, ZhuQ, KnightR, CaporasoJG. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol, 2019, 37(8): 852-857

[12] BruunEW, AmbusP, EgsgaardH, Hauggaard-NielsenH. Effects of slow and fast pyrolysis biochar on soil C and N turnover dynamics. Soil Biol Biochem, 2012, 46: 73-79

[13] CalabreseS, MohantyBP, MalikAA. Soil microorganisms regulate extracellular enzyme production to maximize their growth rate. Biogeochemistry, 2022, 158(3): 303-312

[14] CarusoT, De VriesFT, BardgettRD, LehmannJ. Soil organic carbon dynamics matching ecological equilibrium theory. Ecol Evol, 2018, 8(22): 11169-11178

[15] ChenL, LiuL, MaoC, QinS, WangJ, LiuF, BlagodatskyS, YangG, ZhangQ, ZhangD, YuJ, YangY. Nitrogen availability regulates topsoil carbon dynamics after permafrost thaw by altering microbial metabolic efficiency. Nat Commun, 2018, 9: 3951

[16] ChenQL, DingJ, LiCY, YanZZ, HeJZ, HuHW. Microbial functional attributes, rather than taxonomic attributes, drive top soil respiration, nitrification and denitrification processes. Sci Total Environ, 2020, 734

[17] ChenP, LiuY, MoC, JiangZ, YangJ, LinJ. Microbial mechanism of biochar addition on nitrogen leaching and retention in tea soils from different plantation ages. Sci Total Environ, 2021, 757

[18] ChenP, MoC, HeC, CuiH, LinJ, YangJ. Shift of microbial turnover time and metabolic efficiency strongly regulates rhizosphere priming effect under nitrogen fertilization in paddy soil. Sci Total Environ, 2021, 800

[19] ChenT, LiuYX, HuangL. ImageGP: an easy-to-use data visualization web server for scientific researchers. iMeta, 2022, 1(1)

[20] ChenY, SunK, YangY, GaoB, ZhengH. Effects of biochar on the accumulation of necromass-derived carbon, the physical protection and microbial mineralization of soil organic carbon. Crit Rev Environ Sci Technol, 2023

[21] ChengW. Rhizosphere priming effect: its functional relationships with microbial turnover, evapotranspiration, and C-N budgets. Soil Biol Biochem, 2009, 41(9): 1795-1801

[22] CrossA, SohiSP. The priming potential of biochar products in relation to labile carbon contents and soil organic matter status. Soil Biol Biochem, 2011, 43(10): 2127-2134

[23] Delgado-BaquerizoM, OliverioAM, BrewerTE, Benavent-GonzalezA, EldridgeDJ, BardgettRD, MaestreFT, SinghBK, FiererN. A global atlas of the dominant bacteria found in soil. Science, 2018, 359(6373): 320-325

[24] DharmakeerthiRS, HanleyK, WhitmanT, WoolfD, LehmannJ. Organic carbon dynamics in soils with pyrogenic organic matter that received plant residue additions over seven years. Soil Biol Biochem, 2015, 88: 268-274

[25] DijkstraFA, CarrilloY, PendallE, MorganJA. Rhizosphere priming: a nutrient perspective. Front Microbiol, 2013, 4: 00216

[26] DijkstraFA, ZhuB, ChengW. Root effects on soil organic carbon: a double-edged sword. New Phytol, 2021, 230(1): 60-65

[27] FanK, WeisenhornP, GilbertJA, ShiY, BaiY, ChuH. Soil pH correlates with the co-occurrence and assemblage process of diazotrophic communities in rhizosphere and bulk soils of wheat fields. Soil Biol Biochem, 2018, 121: 185-192

[28] FaninN, GundaleMJ, FarrellM, CiobanuM, BaldockJA, NilssonMC, KardolP, WardleDA. Consistent effects of biodiversity loss on multifunctionality across contrasting ecosystems. Nat Ecol Evol, 2018, 2(2): 269-278

[29] FiererN, BradfordMA, JacksonRB. Toward an ecological classification of soil bacteria. Ecology, 2007, 88(6): 1354-1364

[30] GadeL, ScheelCM, PhamCD, LindsleyMD, IqbalN, ClevelandAA, WhitneyAM, LockhartSR, BrandtME, LitvintsevaAP. Detection of fungal DNA in human body fluids and tissues during a multistate outbreak of fungal meningitis and other infections. Eukaryot Cell, 2013, 12(5): 677-683

[31] GalyV, Peucker-EhrenbrinkB, EglintonT. Global carbon export from the terrestrial biosphere controlled by erosion. Nature, 2015, 521(7551): 204-207

[32] GoodaleCL. Multiyear fate of a ¹⁵N tracer in a mixed deciduous forest: retention, redistribution, and differences by mycorrhizal association. Glob Change Biol, 2017, 23(2): 867-880

[33] HarindintwaliJD, HeC, WenX, LiuY, WangM, FuY, XiangL, JiangJ, JiangX, WangF. A comparative evaluation of biochar and Paenarthrobacter sp. AT5 for reducing atrazine risks to soybeans and bacterial communities in black soil. Environ Res, 2024, 252

[34] HeC, HarindintwaliJD, CuiH, CuiY, ChenP, MoC, ZhuQ, ZhengW, AlessiDS, WangF, JiangZ, YangJ. Deciphering the dual role of bacterial communities in stabilizing rhizosphere priming effect under intra-annual change of growing seasons. Sci Total Environ, 2023, 903

[35] HestrinR, HammerEC, MuellerCW, LehmannJ. Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition. Commun Biol, 2019, 2(1): 233

[36] HuG, FeeleyKJ, WuJ, XuG, YuM. Determinants of plant species richness and patterns of nestedness in fragmented landscapes: evidence from land-bridge islands. Landsc Ecol, 2011, 26(10): 1405-1417

[37] HuoC, LuoY, ChengW. Rhizosphere priming effect: a meta-analysis. Soil Biol Biochem, 2017, 111: 78-84

[38] JiangZ, LiuY, YangJ, BrookesPC, GuninaA. Rhizosphere priming regulates soil organic carbon and nitrogen mineralization: the significance of abiotic mechanisms. Geoderma, 2021, 385

[39] JiaoS, XuY, ZhangJ, HaoX, LuY. Core microbiota in agricultural soils and their potential associations with nutrient cycling. mSystems, 2019, 4(2): e00313-00318

[40] JiaoS, YangY, XuY, ZhangJ, LuY. Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across eastern China. ISME J, 2020, 14(1): 202-216

[41] JiaoS, LuY, WeiG. Soil multitrophic network complexity enhances the link between biodiversity and multifunctionality in agricultural systems. Glob Change Biol, 2021, 28(1): 140-153

[42] JosephS, CowieAL, Van ZwietenL, BolanN, BudaiA, BussW, CayuelaML, GraberER, IppolitoJA, KuzyakovY, LuoY, OkYS, PalansooriyaKN, ShepherdJ, StephensS, WengZ, LehmannJ. How biochar works, and when it doesn't: a review of mechanisms controlling soil and plant responses to biochar. GCB Bioenergy, 2021, 13(11): 1731-1764

[43] KaiserC, FranklinO, DieckmannU, RichterA. Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecol Lett, 2014, 17(6): 680-690

[44] KaiserC, FranklinO, RichterA, DieckmannU. Social dynamics within decomposer communities lead to nitrogen retention and organic matter build-up in soils. Nat Commun, 2015, 6: 8960

[45] KatohK, MisawaK, KumaK, MiyataT. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res, 2002, 30(14): 3059-3066

[46] KeithA, SinghB, SinghBP. Interactive priming of biochar and labile organic matter mineralization in a smectite-rich soil. Environ Sci Technol, 2011, 45(22): 9611-9618

[47] KeithA, SinghB, DijkstraFA. Biochar reduces the rhizosphere priming effect on soil organic carbon. Soil Biol Biochem, 2015, 88: 372-379

[48] KuzyakovY. Review: factors affecting rhizosphere priming effects. J Plant Nutr Soil Sci, 2002, 165(4): 382-396

[49] KuzyakovY, FriedelJK, StahrK. Review of mechanisms and quantification of priming effects. Soil Biol Biochem, 2000, 32(11–12): 1485-1498

[50] KuzyakovY, HillPW, JonesDL. Root exudate components change litter decomposition in a simulated rhizosphere depending on temperature. Plant Soil, 2007, 290(1–2): 293-305

[51] LabouyrieM, BallabioC, RomeroF, PanagosP, JonesA, SchmidMW, MikryukovV, DulyaO, TedersooL, BahramM, LugatoE, van der HeijdenMGA, OrgiazziA. Patterns in soil microbial diversity across Europe. Nat Commun, 2023, 14: 3311

[52] LehmannJ, KleberM. The contentious nature of soil organic matter. Nature, 2015, 528(7580): 60-68

[53] LehmannJ, CowieA, MasielloCA, KammannC, WoolfD, AmonetteJE, CayuelaML, Camps-ArbestainM, WhitmanT. Biochar in climate change mitigation. Nat Geosci, 2021, 14(12): 883-892

[54] LiSP, WangP, ChenY, WilsonMC, YangX, MaC, LuJ, ChenXY, WuJ, ShuWS, JiangL. Island biogeography of soil bacteria and fungi: similar patterns, but different mechanisms. ISME J, 2020, 14(7): 1886-1896

[55] LiZ, TongD, NieX, XiaoH, JiaoP, JiangJ, LiQ, LiaoW. New insight into soil carbon fixation rate: the intensive co-occurrence network of autotrophic bacteria increases the carbon fixation rate in depositional sites. Agr Ecosyst Environ, 2021, 320

[56] LiZ, ZengZ, SongZ, WangF, TianD, MiW, HuangX, WangJ, SongL, YangZ, WangJ, FengH, JiangL, ChenY, LuoY, NiuS. Vital roles of soil microbes in driving terrestrial nitrogen immobilization. Global Change Biol, 2021, 27(9): 1848-1858

[57] LiC, GillingsMR, ZhangC, ChenQ, ZhuD, WangJ, ZhaoK, XuQ, LeungPH, LiX, LiuJ, JinL. Ecology and risks of the global plastisphere as a newly expanding microbial habitat. Innovation, 2024

[58] LiuJJ, GuoYP, GuHD, LiuZX, HuXJ, YuZH, LiYS, LiLJ, SuiYY, JinJ, LiuXB, AdamsJM, WangGH. Conversion of steppe to cropland increases spatial heterogeneity of soil functional genes. ISME J, 2023, 17(11): 1872-1883

[59] LiuZ, ZhangW, MaR, LiS, SongK, ZhengJ, WangY, BianR, ZhangX, PanG. Biochar-plant interactions enhance nonbiochar carbon sequestration in a rice paddy soil. Commun Earth Environ, 2023, 4(1): 494

[60] LoucaS, ParfreyLW, DoebeliM. Decoupling function and taxonomy in the global ocean microbiome. Science, 2016, 353(6305): 1272-1277

[61] LuoL, WangJ, LvJ, LiuZ, SunT, YangY, ZhuYG. Carbon sequestration strategies in soil using biochar: advances, challenges, and opportunities. Environ Sci Technol, 2023, 57(31): 11357-11372

[62] MaB, WangH, DsouzaM, LouJ, HeY, DaiZ, BrookesPC, XuJ, GilbertJA. Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China. ISME J, 2016, 10(8): 1891-1901

[63] MaestreFT, QueroJL, GotelliNJ, EscuderoA, OchoaV, Delgado-BaquerizoM, Garcia-GomezM, BowkerMA, SoliveresS, EscolarC, Garcia-PalaciosP, BerdugoM, ValenciaE, GozaloB, GallardoA, AguileraL, ArredondoT, BlonesJ, BoekenB, BranD, ConceicaoAA, CabreraO, ChaiebM, DerakM, EldridgeDJ, EspinosaCI, FlorentinoA, GaitanJ, GaticaMG, GhiloufiW, Gomez-GonzalezS, GutierrezJR, HernandezRM, HuangX, Huber-SannwaldE, JankjuM, MiritiM, MonerrisJ, MauRL, MoriciE, NaseriK, OspinaA, PoloV, PrinaA, PuchetaE, Ramirez-CollantesDA, RomaoR, TigheM, Torres-DiazC, ValJ, VeigaJP, WangD, ZaadyE. Plant species richness and ecosystem multifunctionality in global drylands. Science, 2012, 335(6065): 214-218

[64] MasonARG, SalomonMJ, LoweAJ, CavagnaroTR. Microbial solutions to soil carbon sequestration. J Clean Prod, 2023, 417

[65] McDonaldD, JiangY, BalabanM, CantrellK, ZhuQ, GonzalezA, MortonJT, NicolaouG, ParksDH, KarstSM, AlbertsenM, HugenholtzP, DeSantisT, SongSJ, BartkoA, HavulinnaAS, JousilahtiP, ChengS, InouyeM, NiiranenT, JainM, SalomaaV, LahtiL, MirarabS, KnightR. Greengenes2 unifies microbial data in a single reference tree. Nat Biotechnol, 2023, 42(5): 715-718

[66] McMurdiePJ, HolmesS. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE, 2013, 8(4)

[67] MeierIC, FinziAC, PhillipsRP. Root exudates increase N availability by stimulating microbial turnover of fast-cycling N pools. Soil Biol Biochem, 2017, 106: 119-128

[68] MoinetGYK, HijbeekR, van VuurenDP, GillerKE. Carbon for soils, not soils for carbon. Glob Change Biol, 2023, 29(9): 2384-2398

[69] MoorheadDL, SinsabaughRL, HillBH, WeintraubMN. Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biol Biochem, 2016, 93: 1-7

[70] NatashaN, ShahidM, KhalidS, BibiI, NaeemMA, NiaziNK, TackFMG, IppolitoJA, RinklebeJ. Influence of biochar on trace element uptake, toxicity and detoxification in plants and associated health risks: a critical review. Crit Rev Environ Sci Technol, 2021, 52(16): 2803-2843

[71] NguyenNH, SongZ, BatesST, BrancoS, TedersooL, MenkeJ, SchillingJS, KennedyPG. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol, 2016, 20: 241-248

[72] NilssonRH, LarssonKH, TaylorAFS, Bengtsson-PalmeJ, JeppesenTS, SchigelD, KennedyP, PicardK, GlöcknerFO, TedersooL, SaarI, KõljalgU, AbarenkovK. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res, 2019, 47(D1): D259-D264

[73] PauschJ, ZhuB, KuzyakovY, ChengW. Plant inter-species effects on rhizosphere priming of soil organic matter decomposition. Soil Biol Biochem, 2013, 57: 91-99

[74] PeiJ, DijkstraFA, LiJ, FangC, SuJ, ZhaoJ, NieM, WuJ. Biochar-induced reductions in the rhizosphere priming effect are weaker under elevated CO₂. Soil Biol Biochem, 2020, 142

[75] Peres-NetoPR, JacksonDA. How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia, 2001, 129(2): 169-178

[76] PietikäinenJ, KiikkiläO, FritzeH. Charcoal as a habitat for microbes and its effect on the microbial community of the underlying humus. Oikos, 2000, 89(2): 231-242

[77] QiuLP, ZhangQ, ZhuHS, ReichPB, BanerjeeS, van der HeijdenMGA, SadowskyMJ, IshiiS, JiaXX, ShaoMG, LiuBY, JiaoH, LiHQ, WeiXR. Erosion reduces soil microbial diversity, network complexity and multifunctionality. ISME J, 2021, 15(8): 2474-2489

[78] ReineltL, WhitakerJ, KazakouE, BonnalL, BastianelliD, BullockJM, OstleNJ. Drought effects on root and shoot traits and their decomposability. Funct Ecol, 2023, 37(4): 1044-1054

[79] SinsabaughRL, Follstad ShahJJ. Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol S, 2012, 43(1): 313-343

[80] SpohnM, ChodakM. Microbial respiration per unit biomass increases with carbon-to-nutrient ratios in forest soils. Soil Biol Biochem, 2015, 81: 128-133

[81] StegenJC, LinX, KonopkaAE, FredricksonJK. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J, 2012, 6(9): 1653-1664

[82] TedersooL, BahramM, PolmeS, KoljalgU, YorouNS, WijesunderaR, Villarreal RuizL, Vasco-PalaciosAM, ThuPQ, SuijaA, SmithME, SharpC, SaluveerE, SaittaA, RosasM, RiitT, RatkowskyD, PritschK, PoldmaaK, PiepenbringM, PhosriC, PetersonM, PartsK, PartelK, OtsingE, NouhraE, NjouonkouAL, NilssonRH, MorgadoLN, MayorJ, MayTW, MajuakimL, LodgeDJ, LeeSS, LarssonKH, KohoutP, HosakaK, HiiesaluI, HenkelTW, HarendH, GuoLD, GreslebinA, GreletG, GemlJ, GatesG, DunstanW, DunkC, DrenkhanR, DearnaleyJ, De KeselA, DangT, ChenX, BueggerF, BrearleyFQ, BonitoG, AnslanS, AbellS, AbarenkovK. Fungal biogeography. Global diversity and geography of soil fungi. Science, 2014, 346(6213): 1256688

[83] ThiesJE, RilligMC. LehmannJ, JosephS. Characteristics of biochar: biological properties. Biochar for environmental management, 2009LondonRoutledge85-106

[84] TrivediP, LeachJE, TringeSG, SaT, SinghBK. Plant-microbiome interactions: from community assembly to plant health. Nat Rev Microbiol, 2020, 18(11): 607-621

[85] WangC, ChenD, ShenJ, YuanQ, FanF, WeiW, LiY, WuJ. Biochar alters soil microbial communities and potential functions 3–4 years after amendment in a double rice cropping system. Agr Ecosyst Environ, 2021, 311

[86] WangF, HarindintwaliJD, YuanZ, WangM, WangF, LiS, YinZ, HuangL, FuY, LiL, ChangSX, ZhangL, RinklebeJ, YuanZ, ZhuQ, XiangL, TsangDCW, XuL, JiangX, LiuJ, WeiN, KästnerM, ZouY, OkYS, ShenJ, PengD, ZhangW, BarceloD, ZhouY, BaiZ, LiB, ZhangB, WeiK, CaoH, TanZ, ZhaoL-b, HeX, ZhengJ, BolanN, LiuX, HuangC, DietmannS, LuoM, SunN, GongJ, GongY, BrahushiF, ZhangT, XiaoC, LiX, ChenW, JiaoN, LehmannJ, ZhuY-G, JinH, SchaefferA, TiedjeJM, ChenJM. Technologies and perspectives for achieving carbon neutrality. Innovation, 2021, 2(4)

[87] WangS, SunP, ZhangG, GrayN, DolfingJ, Esquivel-ElizondoS, PenuelasJ, WuY. Contribution of periphytic biofilm of paddy soils to carbon dioxide fixation and methane emissions. Innovation, 2022, 3(1)

[88] WangF, HarindintwaliJD, WeiK, ShanY, MiZ, CostelloMJ, GrunwaldS, FengZ, WangF, GuoY, WuX, KumarP, KästnerM, FengX, KangS, LiuZ, FuY, ZhaoW, OuyangC, ShenJ, WangH, ChangSX, EvansDL, WangR, ZhuC, XiangL, RinklebeJ, DuM, HuangL, BaiZ, LiS, LalR, ElsnerM, WigneronJ-P, FlorindoF, JiangX, ShaheenSM, ZhongX, BolR, VasquesGM, LiX, PfautschS, WangM, HeX, AgathokleousE, DuH, YanH, KengaraFO, BrahushiF, LongX-E, PereiraP, OkYS, RilligMC, JeppesenE, BarcelóD, YanX, JiaoN, HanB, SchäfferA, ChenJM, ZhuY, ChengH, AmelungW, SpötlC, ZhuJ, TiedjeJM. Climate change: strategies for mitigation and adaptation. Innov Geosci, 2023, 1(1)

[89] WangX, LiS, ZhuB, HomyakPM, ChenG, YaoX, WuD, YangZ, LyuM, YangY. Long-term nitrogen deposition inhibits soil priming effects by enhancing phosphorus limitation in a subtropical forest. Global Change Biol, 2023, 29(14): 4081-4093

[90] WardleDA, BardgettRD, KlironomosJN, SetalaH, van der PuttenWH, WallDH. Ecological linkages between aboveground and belowground biota. Science, 2004, 304(5677): 1629-1633

[91] WardleDA, NilssonMC, ZackrissonO. Fire-derived charcoal causes loss of forest humus. Science, 2008, 320(5876): 629

[92] WengZH, Van ZwietenL, SinghBP, KimberS, MorrisS, CowieA, MacdonaldLM. Plant-biochar interactions drive the negative priming of soil organic carbon in an annual ryegrass field system. Soil Biol Biochem, 2015, 90: 111-121

[93] WengZH, Van ZwietenL, SinghBP, TavakkoliE, JosephS, MacdonaldLM, RoseTJ, RoseMT, KimberSWL, MorrisS, CozzolinoD, AraujoJR, ArchanjoBS, CowieA. Biochar built soil carbon over a decade by stabilizing rhizodeposits. Nat Clim Change, 2017, 7(5): 371-379

[94] WengZH, Van ZwietenL, TavakkoliE, RoseMT, SinghBP, JosephS, MacdonaldLM, KimberS, MorrisS, RoseTJ, ArchanjoBS, TangC, FranksAE, DiaoH, SchweizerS, TobinMJ, KleinAR, VongsvivutJ, ChangSLY, KopittkePM, CowieA. Microspectroscopic visualization of how biochar lifts the soil organic carbon ceiling. Nat Commun, 2022, 13(1): 5177

[95] WerthM, KuzyakovY. ¹³C fractionation at the root-microorganisms-soil interface: a review and outlook for partitioning studies. Soil Biol Biochem, 2010, 42(9): 1372-1384

[96] WhitmanT, EndersA, LehmannJ. Pyrogenic carbon additions to soil counteract positive priming of soil carbon mineralization by plants. Soil Biol Biochem, 2014, 73: 33-41

[97] WickhamH. ggplot2: elegant graphics for data analysis, 20162New YorkSpringer Cham

[98] WoolfD, LehmannJ. Modelling the long-term response to positive and negative priming of soil organic carbon by black carbon. Biogeochemistry, 2012, 111(1–3): 83-95

[99] WuP, Ata-Ul-KarimST, SinghBP, WangHL, WuTL, LiuC, FangGD, ZhouDM, WangYJ, ChenWF. A scientometric review of biochar research in the past 20 years (1998–2018). Biochar, 2019, 1(1): 23-43

[100] XueP, MinasnyB, McBratneyA, PinoV, FajardoM, LuoY. Distribution of soil bacteria involved in C cycling across extensive environmental and pedogenic gradients. Eur J Soil Sci, 2023, 74(1)

[101] YuanX, NiuD, GherardiLA, LiuY, WangY, ElserJJ, FuH. Linkages of stoichiometric imbalances to soil microbial respiration with increasing nitrogen addition: evidence from a long-term grassland experiment. Soil Biol Biochem, 2019, 138

[102] ZhangL, MaB, TangC, YuH, LvX, Mazza RodriguesJL, DahlgrenRA, XuJ. Habitat heterogeneity induced by pyrogenic organic matter in wildfire-perturbed soils mediates bacterial community assembly processes. ISME J, 2021, 15(7): 1943-1955

[103] ZhangY, CaiT, RenZ, LiuY, YuanM, CaiY, YuC, ShuR, HeS, LiJ, WongACN, WanH. Decline in symbiont-dependent host detoxification metabolism contributes to increased insecticide susceptibility of insects under high temperature. ISME J, 2021, 15(12): 3693-3703

[104] ZhangY, DangY, WangJ, HuangQ, WangX, YaoL, VinayN, YuK, WenX, XiongY, LiaoY, HanJ, MoF. A synthesis of soil organic carbon mineralization in response to biochar amendment. Soil Biol Biochem, 2022, 175

[105] ZhengB, ZhuY, SardansJ, PenuelasJ, SuJ. 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

[106] ZimmermanAR, GaoB, AhnM-Y. Positive and negative carbon mineralization priming effects among a variety of biochar-amended soils. Soil Biol Biochem, 2011, 43(6): 1169-1179

Funding

National Natural Science Foundation of China(31870419)

National Key Research and Development Program of China(2016YFD0300203-4)