Microbially Driven Iron Cycling Facilitates Organic Carbon Accrual in Decadal Biochar-Amended Soil.

Soil organic carbon (SOC) is pivotal for both agricultural activities and climate change mitigation, and biochar stands as a promising tool for bolstering SOC and curtailing soil carbon dioxide (CO2) emissions. However, the involvement of biochar in SOC dynamics and the underlying interactions among biochar, soil microbes, iron minerals, and fresh organic matter (FOM, such as plant debris) remain largely unknown, especially in agricultural soils after long-term biochar amendment. We therefore introduced FOM to soils with and without a decade-long history of biochar amendment, performed soil microcosm incubations, and evaluated carbon and iron dynamics as well as microbial properties. Biochar amendment resulted in 2-fold SOC accrual over a decade and attenuated FOM-induced CO2 emissions by approximately 11% during a 56-day incubation through diverse pathways. Notably, biochar facilitated microbially driven iron reduction and subsequent Fenton-like reactions, potentially having enhanced microbial extracellular electron transfer and the carbon use efficiency in the long run. Throughout iron cycling processes, physical protection by minerals could contribute to both microbial carbon accumulation and plant debris preservation, alongside direct adsorption and occlusion of SOC by biochar particles. Furthermore, soil slurry experiments, with sterilization and ferrous iron stimulation controls, confirmed the role of microbes in hydroxyl radical generation and biotic carbon sequestration in biochar-amended soils. Overall, our study sheds light on the intricate biotic and abiotic mechanisms governing carbon dynamics in long-term biochar-amended upland soils.

[1]  A. Kappler,et al.  Coupled iron cycling and organic matter transformation across redox interfaces , 2023, Nature Reviews Earth & Environment.

[2]  Bin Chen,et al.  Formation of soil organic carbon pool is regulated by the structure of dissolved organic matter and microbial carbon pump efficacy: A decadal study comparing different carbon management strategies , 2023, Global change biology.

[3]  Guodong Fang,et al.  Pyrogenic carbon accelerates iron cycling and hydroxyl radical production during redox fluctuations of paddy soils , 2023, Biochar.

[4]  S. Basu,et al.  Reactive oxygen species affect the potential for mineralization processes in permeable intertidal flats , 2023, Nature Communications.

[5]  Yong-guan Zhu,et al.  Introducing the soil mineral carbon pump , 2023, Nature Reviews Earth & Environment.

[6]  P. Nico,et al.  Reactive Iron, Not Fungal Community, Drives Organic Carbon Oxidation Potential in Floodplain Soils , 2023, SSRN Electronic Journal.

[7]  Yong-guan Zhu,et al.  Multiple Effects of Humic Components on Microbially Mediated Iron Redox Processes and Production of Hydroxyl Radicals. , 2022, Environmental science & technology.

[8]  Xiuping Zhu,et al.  Sunlight-Induced Interfacial Electron Transfer of Ferrihydrite under Oxic Conditions: Mineral Transformation and Redox Active Species Production. , 2022, Environmental science & technology.

[9]  A. Cowie,et al.  Microspectroscopic visualization of how biochar lifts the soil organic carbon ceiling , 2022, Nature Communications.

[10]  S. Frey,et al.  Clarifying the evidence for microbial‐ and plant‐derived soil organic matter, and the path toward a more quantitative understanding , 2022, Global change biology.

[11]  A. Kappler,et al.  Tide-Triggered Production of Reactive Oxygen Species in Coastal Soils. , 2022, Environmental science & technology.

[12]  R. B. Jackson,et al.  Global stocks and capacity of mineral-associated soil organic carbon , 2022, Nature Communications.

[13]  B. Ma,et al.  Diel Fluctuation of Extracellular Reactive Oxygen Species Production in the Rhizosphere of Rice. , 2022, Environmental science & technology.

[14]  Fei Liu,et al.  Microbial community mediates hydroxyl radical production in soil slurries by iron redox transformation. , 2022, Water research.

[15]  B. Xing,et al.  Biochar stability and impact on soil organic carbon mineralization depend on biochar processing, aging and soil clay content , 2022, Soil Biology and Biochemistry.

[16]  Robert B. Young,et al.  Microbial iron cycling during palsa hillslope collapse promotes greenhouse gas emissions before complete permafrost thaw , 2022, Communications Earth & Environment.

[17]  T. Lundell,et al.  Basidiomycota Fungi and ROS: Genomic Perspective on Key Enzymes Involved in Generation and Mitigation of Reactive Oxygen Species , 2022, Frontiers in Fungal Biology.

[18]  Baoliang Chen,et al.  Enhanced Microbial Ferrihydrite Reduction by Pyrogenic Carbon: Impact of Graphitic Structures. , 2021, Environmental science & technology.

[19]  A. Franks,et al.  Biochar aging alters the bioavailability of cadmium and microbial activity in acid contaminated soils. , 2021, Journal of hazardous materials.

[20]  Dong-mei Zhou,et al.  Active Iron Phases Regulate the Abiotic Transformation of Organic Carbon during Redox Fluctuation Cycles of Paddy Soil. , 2021, Environmental science & technology.

[21]  Xiujun Wang,et al.  Impacts of continuous biochar application on major carbon fractions in soil profile of North China Plain’s cropland: In comparison with straw incorporation , 2021 .

[22]  Paul G Tratnyek,et al.  Fe(II) Redox Chemistry in the Environment. , 2021, Chemical reviews.

[23]  J. Russell,et al.  Organic matter mineralization in modern and ancient ferruginous sediments , 2021, Nature Communications.

[24]  Dong-mei Zhou,et al.  Pyrogenic Carbon Initiated the Generation of Hydroxyl Radicals from the Oxidation of Sulfide. , 2021, Environmental science & technology.

[25]  Guanghui Yu,et al.  Fenton chemistry and reactive oxygen species in soil: Abiotic mechanisms of biotic processes, controls and consequences for carbon and nutrient cycling , 2021 .

[26]  E. Swanner,et al.  An evolving view on biogeochemical cycling of iron , 2021, Nature Reviews Microbiology.

[27]  T. Scholten,et al.  Iron mineral dissolution releases iron and associated organic carbon during permafrost thaw , 2020, Nature Communications.

[28]  Daniel C W Tsang,et al.  Biochar Aging: Mechanisms, Physicochemical Changes, Assessment, And Implications for Field Applications. , 2020, Environmental science & technology.

[29]  Atul K. Jain,et al.  Global Carbon Budget 2020 , 2020, Earth System Science Data.

[30]  Guanghui Yu,et al.  An iron-dependent burst of hydroxyl radicals stimulates straw decomposition and CO2 emission from soil hotspots: Consequences of Fenton or Fenton-like reactions , 2020 .

[31]  C. Liang,et al.  Microbial necromass on the rise: The growing focus on its role in soil organic matter development , 2020 .

[32]  He-ping Zhao,et al.  Role of pyrogenic carbon in parallel microbial reduction of nitrobenzene in the liquid and sorbed phases. , 2020, Environmental science & technology.

[33]  A. Thompson,et al.  Iron-mediated organic matter decomposition in humid soils can counteract protection , 2020, Nature Communications.

[34]  X. Xia,et al.  Biochar’s stability and effect on the content, composition and turnover of soil organic carbon , 2020 .

[35]  F. Besenbacher,et al.  Carbon dots-fed Shewanella oneidensis MR-1 for bioelectricity enhancement , 2020, Nature Communications.

[36]  Jitao Lv,et al.  Pathway for the Production of Hydroxyl Radical during the Microbially Mediated Redox Transformation of Iron (Oxyhydr)oxides. , 2019, Environmental science & technology.

[37]  Caixian Tang,et al.  13C-DNA-SIP Distinguishes the Prokaryotic Community That Metabolizes Soybean Residues Produced Under Different CO2 Concentrations , 2019, Front. Microbiol..

[38]  D. Segrè,et al.  Microbial carbon use efficiency predicted from genome-scale metabolic models , 2019, Nature Communications.

[39]  Guanghui Yu,et al.  Fungus-initiated catalytic reactions at hyphal-mineral interfaces drive iron redox cycling and biomineralization , 2019, Geochimica et Cosmochimica Acta.

[40]  G. Tyson,et al.  Biochar-Mediated Anaerobic Oxidation of Methane. , 2019, Environmental science & technology.

[41]  W. Zhong,et al.  Assessment of abundance and diversity of exoelectrogenic bacteria in soil under different land use types , 2019, CATENA.

[42]  S. Mooney,et al.  Biochar enhances soil hydraulic function but not soil aggregation in a sandy loam , 2018, European Journal of Soil Science.

[43]  J. Lehmann,et al.  Priming mechanisms with additions of pyrogenic organic matter to soil , 2018, Geochimica et Cosmochimica Acta.

[44]  A. Cowie,et al.  Biochar in climate change mitigation , 2018, Nature Geoscience.

[45]  Diego Barcellos,et al.  Influence of pO2 on Iron Redox Cycling and Anaerobic Organic Carbon Mineralization in a Humid Tropical Forest Soil. , 2018, Environmental science & technology.

[46]  Guanghui Yu,et al.  Redox interface-associated organo-mineral interactions: A mechanism for C sequestration under a rice-wheat cropping system , 2018 .

[47]  G. Kling,et al.  The role of iron and reactive oxygen species in the production of CO2 in arctic soil waters , 2018 .

[48]  P. Nico,et al.  Anaerobic microsites have an unaccounted role in soil carbon stabilization , 2017, Nature Communications.

[49]  T. Hengl,et al.  Soil carbon debt of 12,000 years of human land use , 2017, Proceedings of the National Academy of Sciences.

[50]  J. Jastrow,et al.  The importance of anabolism in microbial control over soil carbon storage , 2017, Nature Microbiology.

[51]  Jinsheng He,et al.  Iron-mediated soil carbon response to water-table decline in an alpine wetland , 2017, Nature Communications.

[52]  T. Shahzad,et al.  Corncob-derived biochar decelerates mineralization of native and added organic matter (AOM) in organic matter depleted alkaline soil , 2017 .

[53]  D. Cozzolino,et al.  Biochar built soil carbon over a decade by stabilizing rhizodeposits , 2017 .

[54]  Guiyao Zhou,et al.  Effects of biochar application on soil greenhouse gas fluxes: a meta‐analysis , 2017 .

[55]  L. T. Angenent,et al.  Rapid electron transfer by the carbon matrix in natural pyrogenic carbon , 2017, Nature Communications.

[56]  A. Shade Diversity is the question, not the answer , 2016, The ISME Journal.

[57]  Hanqing Yu,et al.  Extracellular electron transfer mechanisms between microorganisms and minerals , 2016, Nature Reviews Microbiology.

[58]  N. Batjes Harmonized soil property values for broad-scale modelling (WISE30sec) with estimates of global soil carbon stocks , 2016 .

[59]  Y. Kuzyakov,et al.  Biochar stability in soil: meta‐analysis of decomposition and priming effects , 2016 .

[60]  Ling Zhao,et al.  The Interfacial Behavior between Biochar and Soil Minerals and Its Effect on Biochar Stability. , 2016, Environmental science & technology.

[61]  Yan-xin Wang,et al.  Production of Abundant Hydroxyl Radicals from Oxygenation of Subsurface Sediments. , 2016, Environmental science & technology.

[62]  M. Kleber,et al.  The contentious nature of soil organic matter , 2015, Nature.

[63]  Jennifer Pett-Ridge,et al.  Mineral protection of soil carbon counteracted by root exudates , 2015 .

[64]  E. Blagodatskaya,et al.  Microbial hotspots and hot moments in soil: Concept & review , 2015 .

[65]  D. Sparks,et al.  Properties of Fe-organic matter associations via coprecipitation versus adsorption. , 2014, Environmental science & technology.

[66]  A. Kappler,et al.  Biochar as an Electron Shuttle between Bacteria and Fe(III) Minerals , 2014 .

[67]  Julie E. Jones,et al.  Impact of biochar on mineralisation of C and N from soil and willow litter and its relationship with microbial community biomass and structure , 2014, Biology and Fertility of Soils.

[68]  Juan Gao,et al.  Key role of persistent free radicals in hydrogen peroxide activation by biochar: implications to organic contaminant degradation. , 2014, Environmental science & technology.

[69]  G. Kling,et al.  Dark formation of hydroxyl radical in Arctic soil and surface waters. , 2013, Environmental science & technology.

[70]  Davey L. Jones,et al.  Life in the 'charosphere' - Does biochar in agricultural soil provide a significant habitat for microorganisms? , 2013 .

[71]  W. Silver,et al.  Iron oxidation stimulates organic matter decomposition in humid tropical forest soils , 2013, Global change biology.

[72]  B. Voelker,et al.  Widespread Production of Extracellular Superoxide by Heterotrophic Bacteria , 2013, Science.

[73]  Alfonso Mucci,et al.  Preservation of organic matter in sediments promoted by iron , 2012, Nature.

[74]  A. Keith,et al.  Interactive priming of biochar and labile organic matter mineralization in a smectite-rich soil. , 2011, Environmental science & technology.

[75]  Caroline A. Masiello,et al.  Biochar effects on soil biota – A review , 2011 .

[76]  A. Salamov,et al.  The Plant Cell Wall–Decomposing Machinery Underlies the Functional Diversity of Forest Fungi , 2011, Science.

[77]  Y. Kuzyakov Priming effects : interactions between living and dead organic matter , 2010 .

[78]  Julie M Grossman,et al.  Black carbon affects the cycling of non-black carbon in soil , 2010 .

[79]  M. Heimann,et al.  Terrestrial ecosystem carbon dynamics and climate feedbacks , 2008, Nature.

[80]  R. B. Jackson,et al.  Toward an ecological classification of soil bacteria. , 2007, Ecology.

[81]  J. Six,et al.  Bacterial and Fungal Contributions to Carbon Sequestration in Agroecosystems , 2006 .

[82]  R. Lal Soil Carbon Sequestration Impacts on Global Climate Change and Food Security , 2004, Science.

[83]  L. Stookey Ferrozine---a new spectrophotometric reagent for iron , 1970 .

[84]  Jitao Lv,et al.  Dithionite extractable iron responsible for the production of hydroxyl radicals in soils under fluctuating redox conditions , 2022, Geoderma.

[85]  A. Dekas,et al.  Contributions of anoxic microsites to soil carbon protection across soil textures , 2022, Geoderma.

[86]  Jiong Cheng,et al.  Interactions between aged biochar, fresh low molecular weight carbon and soil organic carbon after 3.5 years soil-biochar incubations , 2019, Geoderma.

[87]  Y. Kuzyakov,et al.  Does repeated biochar incorporation induce further soil priming effect? , 2017, Journal of Soils and Sediments.

[88]  P. Brookes,et al.  AN EXTRACTION METHOD FOR MEASURING SOIL MICROBIAL BIOMASS C , 1987 .