Environmental Chemistry Environmental Chemistry Society
Environmental problems - Chemical approaches
RESEARCH ARTICLE

Biochar amendment altered the molecular-level composition of native soil organic matter in a temperate forest soil

Perry J. Mitchell A B , André J. Simpson A B , Ronald Soong B and Myrna J. Simpson A B C

A Department of Chemistry, University of Toronto, 80 St. George Street, Toronto, ON, M5S 3H6, Canada.

B Environmental NMR Centre and Department of Physical and Environmental Sciences, University of Toronto Scarborough, 1265 Military Trail, Toronto, ON, M1C 1A4, Canada.

C Corresponding author. Email: myrna.simpson@utoronto.ca

Environmental Chemistry - http://dx.doi.org/10.1071/EN16001
Submitted: 2 January 2016  Accepted: 3 May 2016   Published online: 8 June 2016

Environmental context. Biochar amendment in soil can sequester carbon but may also stimulate microbial activity, potentially enhancing soil organic matter degradation. We incubated biochar in a temperate forest soil and characterised the soil organic matter composition using molecular-level biomarker and nuclear magnetic resonance techniques. Biochar amendment altered the native soil organic matter composition and decreased the concentration of easily degradable soil organic matter components.

Abstract. Biochar amendment in soil can sequester carbon and improve soil water and nutrient retention, fertility and plant productivity. However, biochar may stimulate microbial activity, leading to priming or accelerated soil organic matter (OM) degradation, which could alter the native soil OM molecular composition. To investigate this, we amended sugar maple wood biochar (pyrolysed at 500 °C) at four concentrations (0, 5, 10 and 20 metric tons per hectare) in a temperate forest soil for 32 weeks. Solvent extraction and CuO oxidation were used to characterise free compounds and lignin-derived phenols respectively at 8 week intervals, while base hydrolysis was used to examine plant wax, cutin and suberin components at the end of the incubation. Stimulated soil microbial activity following an adaptation period (16 weeks) resulted in increased inputs of microbial- and plant-derived soil OM components including solvent-extractable short-chain n-alkanols and n-alkanoic acids, long-chain n-alkanes and n-alkanols, and sugars. Degradation parameters for base-hydrolysable cutin- and suberin-derived compounds did not show any significant degradation of these plant biopolymers. Analysis of lignin-derived phenols revealed lower concentrations of extractable phenols and progressive oxidation of syringyl and vanillyl phenols at higher biochar application rates over time. Solution-state 1H nuclear magnetic resonance analysis of base-extractable soil OM after 32 weeks showed a decrease in the proportion of labile OM components such as carbohydrates and peptides and a relative increase in more recalcitrant polymethylene OM constituents in the amended soils. The biochar-mediated shifts in soil OM composition and reduction in labile carbon may reduce soil fertility in biochar-amended systems with long-term amendment.

Additional keywords: biomarker, cutin, lignin, nuclear magnetic resonance, suberin.


References

[1]  S. A. McCormack, N. Ostle, R. D. Bardgett, D. W. Hopkins, A. J. Vanbergen, Biochar in bioenergy cropping systems: impacts on soil faunal communities and linked ecosystem processes. GCB Bioenergy 2013, 5, 81.
Biochar in bioenergy cropping systems: impacts on soil faunal communities and linked ecosystem processes.CrossRef | 1:CAS:528:DC%2BC3sXmsVCku7k%3D&md5=d0bc155d5325b6a4cd5339ce4a150e46CAS | open url image1

[2]  J. Lehmann, S. Joseph, Biochar for environmental management: an introduction, in Biochar for Environmental Management: Science and Technology (Eds J. Lehmann, S. Joseph) 2009, pp. 1–12 (Earthscan: London, UK). 10.4324/9781849770552

[3]  C. I. Kammann, H. P. Schmidt, N. Messerschmidt, S. Linsel, D. Steffens, C. Müller, H. W. Koyro, P. Conte, S. Joseph, Plant growth improvement mediated by nitrate capture in co-composted biochar. Sci. Rep. 2015, 5, 11080.
Plant growth improvement mediated by nitrate capture in co-composted biochar.CrossRef | 26057083PubMed | open url image1

[4]  H. P. Schmidt, B. H. Pandit, V. Martinsen, G. Cornelissen, P. Conte, C. I. Kammann, Fourfold increase in pumpkin yield in response to low-dosage root zone application of urine-enhanced biochar to a fertile tropical soil. Agriculture 2015, 5, 723.
Fourfold increase in pumpkin yield in response to low-dosage root zone application of urine-enhanced biochar to a fertile tropical soil.CrossRef | open url image1

[5]  J. Lehmann, M. C. Rillig, J. Thies, C. A. Masiello, W. C. Hockaday, D. Crowley, Biochar effects on soil biota – a review. Soil Biol. Biochem. 2011, 43, 1812.
Biochar effects on soil biota – a review.CrossRef | 1:CAS:528:DC%2BC3MXhtVWrt7fI&md5=c11a501e8964c1f13c988d23f1425669CAS | open url image1

[6]  G. Cimò, J. Kucerik, A. E. Berns, G. E. Schaumann, G. Alonzo, P. Conte, Effect of heating time and temperature on the chemical characteristics of biochar from poultry manure. J. Agric. Food Chem. 2014, 62, 1912.
Effect of heating time and temperature on the chemical characteristics of biochar from poultry manure.CrossRef | 24506474PubMed | open url image1

[7]  C. L. M. Khodadad, A. R. Zimmerman, S. J. Green, S. Uthandi, J. S. Foster, Taxa-specific changes in soil microbial community composition induced by pyrogenic carbon amendments. Soil Biol. Biochem. 2011, 43, 385.
Taxa-specific changes in soil microbial community composition induced by pyrogenic carbon amendments.CrossRef | 1:CAS:528:DC%2BC3MXhtlGmtA%3D%3D&md5=57568056fec860ca14e1dbaec53a34e2CAS | open url image1

[8]  C. Prayogo, J. E. Jones, J. Baeyens, G. D. Bending, Impact of biochar on mineralisation of C and N from soil and willow litter and its relationship with microbial community biomass and structure. Biol. Fertil. Soils 2014, 50, 695.
Impact of biochar on mineralisation of C and N from soil and willow litter and its relationship with microbial community biomass and structure.CrossRef | 1:CAS:528:DC%2BC2cXmvFCmsbc%3D&md5=1758c197cc8bb7a2822991f62fe44a3bCAS | open url image1

[9]  A. Watzinger, S. Feichtmair, B. Kitzler, F. Zehetner, S. Kloss, B. Wimmer, S. Zechmeister-Boltenstern, G. Soja, Soil microbial communities responded to biochar application in temperate soils and slowly metabolized 13C-labelled biochar as revealed by 13C PLFA analyses: results from a short-term incubation and pot experiment. Eur. J. Soil Sci. 2014, 65, 40.
Soil microbial communities responded to biochar application in temperate soils and slowly metabolized 13C-labelled biochar as revealed by 13C PLFA analyses: results from a short-term incubation and pot experiment.CrossRef | 1:CAS:528:DC%2BC2cXnt1egug%3D%3D&md5=7fb1551c0e5e139f4658d581f56714a5CAS | open url image1

[10]  J. D. Gomez, K. Denef, C. E. Stewart, J. Zheng, M. F. Cotrufo, Biochar addition rate influences soil microbial abundance and activity in temperate soils. Eur. J. Soil Sci. 2014, 65, 28.
Biochar addition rate influences soil microbial abundance and activity in temperate soils.CrossRef | 1:CAS:528:DC%2BC2cXnt1ensg%3D%3D&md5=270f36b45ba0789c9b73d00cfc848459CAS | open url image1

[11]  S. Steinbeiss, G. Gleixner, M. Antonietti, Effect of biochar amendment on soil carbon balance and soil microbial activity. Soil Biol. Biochem. 2009, 41, 1301.
Effect of biochar amendment on soil carbon balance and soil microbial activity.CrossRef | 1:CAS:528:DC%2BD1MXmtVGkurc%3D&md5=4e9392941b1edf5e1d49c13cc8cd89d4CAS | open url image1

[12]  G. Baiamonte, C. De Pasquale, V. Marsala, G. Cimò, G. Alonzo, G. Crescimanno, P. Conte, Structure alteration of a sandy-clay soil by biochar amendments. J. Soils Sediments 2015, 15, 816.
Structure alteration of a sandy-clay soil by biochar amendments.CrossRef | 1:CAS:528:DC%2BC2cXhsVSisbjP&md5=611b28865706a431679af3dfd704ba99CAS | open url image1

[13]  A. S. Basso, F. E. Miguez, D. A. Laird, R. Horton, M. Westgate, Assessing potential of biochar for increasing water-holding capacity of sandy soils. GCB Bioenergy 2013, 5, 132.
Assessing potential of biochar for increasing water-holding capacity of sandy soils.CrossRef | 1:CAS:528:DC%2BC3sXmsVCrsrg%3D&md5=8b60568bcbb28b2a7369ee50050a0c2fCAS | open url image1

[14]  X. Domene, S. Mattana, K. Hanley, A. Enders, J. Lehmann, Medium-term effects of corn biochar addition on soil biota activities and functions in a temperate soil cropped to corn. Soil Biol. Biochem. 2014, 72, 152.
Medium-term effects of corn biochar addition on soil biota activities and functions in a temperate soil cropped to corn.CrossRef | 1:CAS:528:DC%2BC2cXkslKjsro%3D&md5=307e723874d1672cb0aa21dfb36e1401CAS | open url image1

[15]  Y. Kuzyakov, J. K. Friedel, K. Stahr, Review of mechanisms and quantification of priming effects. Soil Biol. Biochem. 2000, 32, 1485.
Review of mechanisms and quantification of priming effects.CrossRef | 1:CAS:528:DC%2BD3cXntFSmu78%3D&md5=bfcc42bebff97532bf0b83c36dc9bc3eCAS | open url image1

[16]  Y. Kuzyakov, Priming effects: interactions between living and dead organic matter. Soil Biol. Biochem. 2010, 42, 1363.
Priming effects: interactions between living and dead organic matter.CrossRef | 1:CAS:528:DC%2BC3cXptlCrtbc%3D&md5=3c4a05f86210d3bb428c3204d424a7f6CAS | open url image1

[17]  A. Cross, S. P. Sohi, The priming potential of biochar products in relation to labile carbon contents and soil organic matter status. Soil Biol. Biochem. 2011, 43, 2127.
The priming potential of biochar products in relation to labile carbon contents and soil organic matter status.CrossRef | 1:CAS:528:DC%2BC3MXhtVWku7%2FN&md5=7be274d043fbb489474b4d0029ee36f8CAS | open url image1

[18]  A. Keith, B. Singh, B. P. Singh, Interactive priming of biochar and labile organic matter mineralization in a smectite-rich soil. Environ. Sci. Technol. 2011, 45, 9611.
Interactive priming of biochar and labile organic matter mineralization in a smectite-rich soil.CrossRef | 1:CAS:528:DC%2BC3MXhtlCiurbN&md5=196088ec4be04f3e8e84ce5498a10875CAS | 21950729PubMed | open url image1

[19]  D. N. Dempster, D. B. Gleeson, Z. M. Solaiman, D. L. Jones, D. V. Murphy, Decreased soil microbial biomass and nitrogen mineralisation with Eucalyptus biochar addition to a coarse textured soil. Plant Soil 2012, 354, 311.
Decreased soil microbial biomass and nitrogen mineralisation with Eucalyptus biochar addition to a coarse textured soil.CrossRef | 1:CAS:528:DC%2BC38XlvFWgtbc%3D&md5=9e208bdd877c19920d0b690b906a037aCAS | open url image1

[20]  D. L. Jones, J. Rousk, G. Edwards-Jones, T. H. DeLuca, D. V. Murphy, Biochar-mediated changes in soil quality and plant growth in a three-year field trial. Soil Biol. Biochem. 2012, 45, 113.
Biochar-mediated changes in soil quality and plant growth in a three-year field trial.CrossRef | 1:CAS:528:DC%2BC3MXhs1CrtL3P&md5=4ef163384fd76abf00870131d61a23d6CAS | open url image1

[21]  N. Ameloot, S. Sleutel, S. D. C. Case, G. Alberti, N. P. McNamara, C. Zavalloni, B. Vervisch, G. delle Vedove, S. De Neve, C mineralization and microbial activity in four biochar field experiments several years after incorporation. Soil Biol. Biochem. 2014, 78, 195.
C mineralization and microbial activity in four biochar field experiments several years after incorporation.CrossRef | 1:CAS:528:DC%2BC2cXhsVSqtrvO&md5=f9428ae5fcea0f603ee3ca6013e1ab91CAS | open url image1

[22]  T. Whitman, Z. Zhu, J. Lehmann, Carbon mineralizability determines interactive effects on mineralization of pyrogenic organic matter and soil organic carbon. Environ. Sci. Technol. 2014, 48, 13727.
Carbon mineralizability determines interactive effects on mineralization of pyrogenic organic matter and soil organic carbon.CrossRef | 1:CAS:528:DC%2BC2cXhvVelurjL&md5=62cf809b74df2fd4ec1494b9279ac9a6CAS | 25361379PubMed | open url image1

[23]  M. Zimmermann, M. I. Bird, C. Wurster, G. Saiz, I. Goodrick, J. Barta, P. Capek, H. Santruckova, R. Smernik, Rapid degradation of pyrogenic carbon. Glob. Change Biol. 2012, 18, 3306.
Rapid degradation of pyrogenic carbon.CrossRef | open url image1

[24]  N. Ameloot, S. De Neve, K. Jegajeevagan, G. Yildiz, D. Buchan, Y. N. Funkuin, W. Prins, L. Bouckaert, S. Sleutel, Short-term CO2 and N2O emissions and microbial properties of biochar-amended sandy loam soils. Soil Biol. Biochem. 2013, 57, 401.
Short-term CO2 and N2O emissions and microbial properties of biochar-amended sandy loam soils.CrossRef | 1:CAS:528:DC%2BC3sXitVGntLk%3D&md5=331749abf21047981963234abbafca7cCAS | open url image1

[25]  A. Otto, M. J. Simpson, Degradation and preservation of vascular plant-derived biomarkers in grassland and forest soils from western Canada. Biogeochemistry 2005, 74, 377.
Degradation and preservation of vascular plant-derived biomarkers in grassland and forest soils from western Canada.CrossRef | 1:CAS:528:DC%2BD2MXhtFGlt7vL&md5=cba0d09422b99162ef4455aae71477ccCAS | open url image1

[26]  C. R. Anderson, L. M. Condron, T. J. Clough, M. Fiers, A. Stewart, R. A. Hill, R. R. Sherlock, Biochar-induced soil microbial community change: implications for biogeochemical cycling of carbon, nitrogen and phosphorus. Pedobiologia 2011, 54, 309.
Biochar-induced soil microbial community change: implications for biogeochemical cycling of carbon, nitrogen and phosphorus.CrossRef | 1:CAS:528:DC%2BC3MXht1ymsrfJ&md5=87e4717995d8d0185bae5f2ce67f9134CAS | open url image1

[27]  S. E. Ziegler, S. A. Billings, C. S. Lane, J. Li, M. L. Fogel, Warming alters routing of labile and slower-turnover carbon through distinct microbial groups in boreal forest organic soils. Soil Biol. Biochem. 2013, 60, 23.
Warming alters routing of labile and slower-turnover carbon through distinct microbial groups in boreal forest organic soils.CrossRef | 1:CAS:528:DC%2BC3sXktlKnu74%3D&md5=925750cf7c6d59dc4e9c77b6378fc32aCAS | open url image1

[28]  M. V. Lützow, I. Kögel-Knabner, K. Ekschmitt, E. Matzner, G. Guggenberger, B. Marschner, H. Flessa, Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions – a review. Eur. J. Soil Sci. 2006, 57, 426.
Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions – a review.CrossRef | open url image1

[29]  I. Kögel-Knabner, The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol. Biochem. 2002, 34, 139.
The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter.CrossRef | open url image1

[30]  J. Lehmann, A handful of carbon. Nature 2007, 447, 143.
A handful of carbon.CrossRef | 1:CAS:528:DC%2BD2sXltVGktbc%3D&md5=43c9b8a213770b12e8d414e936d76b70CAS | 17495905PubMed | open url image1

[31]  P. J. Mitchell, A. J. Simpson, R. Soong, M. J. Simpson, Shifts in microbial community and water-extractable organic matter composition with biochar amendment in a temperate forest soil. Soil Biol. Biochem. 2015, 81, 244.
Shifts in microbial community and water-extractable organic matter composition with biochar amendment in a temperate forest soil.CrossRef | 1:CAS:528:DC%2BC2cXitVWkt7jJ&md5=cec93aa306717055d219c9c32399505dCAS | open url image1

[32]  X. Feng, M. J. Simpson, Molecular-level methods for monitoring soil organic matter responses to global climate change. J. Environ. Monit. 2011, 13, 1246.
Molecular-level methods for monitoring soil organic matter responses to global climate change.CrossRef | 1:CAS:528:DC%2BC3MXlsFSgsrc%3D&md5=19ff98baf363fbeb3b98ee71e5d69b44CAS | 21416081PubMed | open url image1

[33]  M. J. Simpson, A. J. Simpson, The chemical ecology of soil organic matter molecular constituents. J. Chem. Ecol. 2012, 38, 768.
The chemical ecology of soil organic matter molecular constituents.CrossRef | 1:CAS:528:DC%2BC38Xptl2ltbs%3D&md5=f82c559562e8c09226881b524e883858CAS | 22549555PubMed | open url image1

[34]  J. I. Hedges, J. R. Ertel, Characterization of lignin by gas capillary chromatography of cupric oxide oxidation products. Anal. Chem. 1982, 54, 174.
Characterization of lignin by gas capillary chromatography of cupric oxide oxidation products.CrossRef | 1:CAS:528:DyaL38XjslWitQ%3D%3D&md5=73fe6d8a63921e8e8507db8bbf342e09CAS | open url image1

[35]  A. Otto, M. J. Simpson, Evaluation of CuO oxidation parameters for determining the source and stage of lignin degradation in soil. Biogeochemistry 2006, 80, 121.
Evaluation of CuO oxidation parameters for determining the source and stage of lignin degradation in soil.CrossRef | 1:CAS:528:DC%2BD28XhtVWhsr%2FI&md5=be74a6326423ca7ff811412a3135ee9cCAS | open url image1

[36]  A. Otto, M. J. Simpson, Sources and composition of hydrolysable aliphatic lipids and phenols in soils from western Canada. Org. Geochem. 2006, 37, 385.
Sources and composition of hydrolysable aliphatic lipids and phenols in soils from western Canada.CrossRef | 1:CAS:528:DC%2BD28Xit1ajtLY%3D&md5=4de7600216edbdf1271a1affe0a45657CAS | open url image1

[37]  F. A. Hansel, C. T. Aoki, C. M. B. F. Maia, A. Cunha, R. A. Dedecek, Comparison of two alkaline treatments in the extraction of organic compounds associated with water repellency in soil under Pinus taeda. Geoderma 2008, 148, 167.
Comparison of two alkaline treatments in the extraction of organic compounds associated with water repellency in soil under Pinus taeda.CrossRef | 1:CAS:528:DC%2BD1cXhsVWhtb7K&md5=d18f63115868dfdd3b7ef14d3bfd17c3CAS | open url image1

[38]  J. S. Clemente, E. G. Gregorich, A. J. Simpson, R. Kumar, D. Courtier-Murias, M. J. Simpson, Comparison of nuclear magnetic resonance methods for the analysis of organic matter composition from soil density and particle fractions. Environ. Chem. 2012, 9, 97.
Comparison of nuclear magnetic resonance methods for the analysis of organic matter composition from soil density and particle fractions.CrossRef | 1:CAS:528:DC%2BC38Xis1amtbk%3D&md5=432d700a92eec808d870b83b9148ea5bCAS | open url image1

[39]  T. Gradowski, S. C. Thomas, Phosphorus limitation of sugar maple growth in central Ontario. For. Ecol. Manage. 2006, 226, 104.
Phosphorus limitation of sugar maple growth in central Ontario.CrossRef | open url image1

[40]  G. L. Noyce, N. Basiliko, R. Fulthorpe, T. E. Sackett, S. C. Thomas, Soil microbial responses over 2 years following biochar addition to a north temperate forest. Biol. Fertil. Soils 2015, 51, 649.
Soil microbial responses over 2 years following biochar addition to a north temperate forest.CrossRef | 1:CAS:528:DC%2BC2MXmsFyms7o%3D&md5=9e95e49d575f453941e04296a695b164CAS | open url image1

[41]  T. E. Sackett, N. Basiliko, G. L. Noyce, C. Winsborough, J. Schurman, C. Ikeda, S. C. Thomas, Soil and greenhouse gas responses to biochar additions in a temperate hardwood forest. GCB Bioenergy 2015, 7, 1062.
Soil and greenhouse gas responses to biochar additions in a temperate hardwood forest.CrossRef | 1:CAS:528:DC%2BC2MXhtlSmtrzP&md5=1e40ed1c297e0630b07a723b482a9404CAS | open url image1

[42]  Soil Classification Working Group The Canadian System of Soil Classification 1998 (NRC Research Press: Ottawa, ON).

[43]  R. Calvelo Pereira, J. Kaal, M. Camps Arbestain, R. Pardo Lorenzo, W. Aitkenhead, M. Hedley, F. Macías, J. Hindmarsh, J. A. Maciá-Agulló, Contribution to characterisation of biochar to estimate the labile fraction of carbon. Org. Geochem. 2011, 42, 1331.
Contribution to characterisation of biochar to estimate the labile fraction of carbon.CrossRef | 1:CAS:528:DC%2BC3MXhsVWktrzL&md5=24745c768f828334f8c0fced6e2245e7CAS | open url image1

[44]  N. Ameloot, S. Sleutel, K. C. Das, J. Kanagaratnam, S. De Neve, Biochar amendment to soils with contrasting organic matter level: effects on N mineralization and biological soil properties. GCB Bioenergy 2015, 7, 135.
Biochar amendment to soils with contrasting organic matter level: effects on N mineralization and biological soil properties.CrossRef | 1:CAS:528:DC%2BC2cXitFGku7nE&md5=8868ac223319fbbb67a54d02988bea3dCAS | open url image1

[45]  A. Otto, M. J. Simpson, Analysis of soil organic matter biomarkers by sequential chemical degradation and gas chromatography–mass spectrometry. J. Sep. Sci. 2007, 30, 272.
Analysis of soil organic matter biomarkers by sequential chemical degradation and gas chromatography–mass spectrometry.CrossRef | 1:CAS:528:DC%2BD2sXisVyrtb0%3D&md5=8830c5c0d282a5375ae675c43e20d08dCAS | 17390623PubMed | open url image1

[46]  A. Otto, B. R. T. Simoneit, Chemosystematics and diagenesis of terpenoids in fossil conifer species and sediment from the Eocene Zeitz formation, Saxony, Germany. Geochim. Cosmochim. Acta 2001, 65, 3505.
Chemosystematics and diagenesis of terpenoids in fossil conifer species and sediment from the Eocene Zeitz formation, Saxony, Germany.CrossRef | 1:CAS:528:DC%2BD3MXotVOrurc%3D&md5=625952a725135e4ade8a60eab474522fCAS | open url image1

[47]  M. A. Goñi, J. I. Hedges, Lignin dimers: structures, distribution, and potential geochemical applications. Geochim. Cosmochim. Acta 1992, 56, 4025.
Lignin dimers: structures, distribution, and potential geochemical applications.CrossRef | open url image1

[48]  D. H. Hunneman, G. Eglinton, The constituent acids of gymnosperm cutins. Phytochemistry 1972, 11, 1989.
The constituent acids of gymnosperm cutins.CrossRef | 1:CAS:528:DyaE38XksVGmsr4%3D&md5=27095e416a7a133fac0b9ad134533a85CAS | open url image1

[49]  C. Rumpel, N. Rabia, S. Derenne, K. Quenea, K. Eusterhues, I. Kögel-Knabner, A. Mariotti, Alteration of soil organic matter following treatment with hydrofluoric acid (HF). Org. Geochem. 2006, 37, 1437.
Alteration of soil organic matter following treatment with hydrofluoric acid (HF).CrossRef | 1:CAS:528:DC%2BD28XhtFylurnK&md5=019b80da091570a7d8690d5416c0fe71CAS | open url image1

[50]  C. N. Gonçalves, R. S. D. Dalmolin, D. P. Dick, H. Knicker, E. Klamt, I. Kögel-Knabner, The effect of 10 % HF treatment on the resolution of CPMAS 13C NMR spectra and on the quality of organic matter in Ferralsols. Geoderma 2003, 116, 373.
The effect of 10 % HF treatment on the resolution of CPMAS 13C NMR spectra and on the quality of organic matter in Ferralsols.CrossRef | open url image1

[51]  W. T. Dixon, J. Schaefer, M. D. Sefcik, E. O. Stejskal, R. A. McKay, Total suppression of sidebands in CPMAS C-13 NMR. J. Magn. Reson. 1982, 49, 341.
Total suppression of sidebands in CPMAS C-13 NMR.CrossRef | 1:CAS:528:DyaL38XlsFGiu7Y%3D&md5=696fd2dd62849b2672882ff140fd6c79CAS | open url image1

[52]  A. J. Simpson, M. J. Simpson, E. Smith, B. P. Kelleher, Microbially derived inputs to soil organic matter: are current estimates too low? Environ. Sci. Technol. 2007, 41, 8070.
Microbially derived inputs to soil organic matter: are current estimates too low?CrossRef | 1:CAS:528:DC%2BD2sXhtFGnsLvP&md5=d8ab6d2f567b30a75a0531b7c6ec0c14CAS | 18186339PubMed | open url image1

[53]  É. Lichtfouse, G. Berthier, S. Houot, E. Barriuso, V. Bergheaud, T. Vallaeys, Stable carbon isotope evidence for the microbial origin of C14–C18 n-alkanoic acids in soils. Org. Geochem. 1995, 23, 849.
Stable carbon isotope evidence for the microbial origin of C14–C18 n-alkanoic acids in soils.CrossRef | 1:CAS:528:DyaK28Xjs1Whtg%3D%3D&md5=f248b960b8a8ef55e9bba2f223741122CAS | open url image1

[54]  J. L. Harwood, N. J. Russell, Lipids in Plants and Microbes 1984 (George Allen and Unwin: London, UK). 10.1007/978-94-011-5989-0

[55]  O. Pisani, K. M. Hills, D. Courtier-Murias, A. J. Simpson, N. J. Mellor, E. A. Paul, S. J. Morris, M. J. Simpson, Molecular-level analysis of long-term vegetative shifts and relationships to soil organic matter composition. Org. Geochem. 2013, 62, 7.
Molecular-level analysis of long-term vegetative shifts and relationships to soil organic matter composition.CrossRef | 1:CAS:528:DC%2BC3sXhtlekt7nK&md5=e5a6287a7b051e1fd511d4a3c8873836CAS | open url image1

[56]  A. Frostegård, E. Bååth, The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol. Fertil. Soils 1996, 22, 59.
The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil.CrossRef | open url image1

[57]  K. A. Spokas, J. M. Novak, C. E. Stewart, K. B. Cantrell, M. Uchimiya, M. G. DuSaire, K. S. Ro, Qualitative analysis of volatile organic compounds on biochar. Chemosphere 2011, 85, 869.
Qualitative analysis of volatile organic compounds on biochar.CrossRef | 1:CAS:528:DC%2BC3MXhsVehsbbM&md5=b557b1ede2a385b502d7a17a509dec15CAS | 21788060PubMed | open url image1

[58]  J. L. Deenik, T. McClellan, G. Uehara, M. J. Antal, S. Campbell, Charcoal volatile matter content influences plant growth and soil nitrogen transformations. Soil Sci. Soc. Am. J. 2010, 74, 1259.
Charcoal volatile matter content influences plant growth and soil nitrogen transformations.CrossRef | 1:CAS:528:DC%2BC3cXovVOjurk%3D&md5=fc68ebbf50f6f9e478c6bb0af95a56e0CAS | open url image1

[59]  B. Maestrini, A. M. Herrmann, P. Nannipieri, M. W. I. Schmidt, S. Abiven, Ryegrass-derived pyrogenic organic matter changes organic carbon and nitrogen mineralization in a temperate forest soil. Soil Biol. Biochem. 2014, 69, 291.
Ryegrass-derived pyrogenic organic matter changes organic carbon and nitrogen mineralization in a temperate forest soil.CrossRef | 1:CAS:528:DC%2BC2cXisVKktg%3D%3D&md5=0c8406f14e5ee4926f10423ed9ff9a17CAS | open url image1

[60]  A. W. West, W. D. Grant, G. P. Sparling, Use of ergosterol, diaminopimelic acid and glucosamine contents of soils to monitor changes in microbial populations. Soil Biol. Biochem. 1987, 19, 607.
Use of ergosterol, diaminopimelic acid and glucosamine contents of soils to monitor changes in microbial populations.CrossRef | 1:CAS:528:DyaL2sXlsFegur0%3D&md5=5c84690d3c73cbae54612b4625ad2a72CAS | open url image1

[61]  S. E. Hale, J. Lehmann, D. Rutherford, A. R. Zimmerman, R. T. Bachmann, V. Shitumbanuma, A. O’Toole, K. L. Sundqvist, H. P. H. Arp, G. Cornelissen, Quantifying the total and bioavailable polycyclic aromatic hydrocarbons and dioxins in biochars. Environ. Sci. Technol. 2012, 46, 2830.
Quantifying the total and bioavailable polycyclic aromatic hydrocarbons and dioxins in biochars.CrossRef | 1:CAS:528:DC%2BC38XitVSntLo%3D&md5=4654a60b3fb14a7c3299714656a0ec0aCAS | 22321025PubMed | open url image1

[62]  J. E. Thies, M. C. Rillig, Characteristics of biochar: biological properties, in Biochar for Environmental Management: Science and Technology (Eds J. Lehmann, S. Joseph) 2009, pp. 85–105 (Earthscan: London, UK). 10.4324/9781849770552

[63]  R. S. Quilliam, S. Rangecroft, B. A. Emmett, T. H. Deluca, D. L. Jones, Is biochar a source or sink for polycyclic aromatic hydrocarbon (PAH) compounds in agricultural soils? GCB Bioenergy 2013, 5, 96.
Is biochar a source or sink for polycyclic aromatic hydrocarbon (PAH) compounds in agricultural soils?CrossRef | 1:CAS:528:DC%2BC3sXmsVCku7c%3D&md5=39bda40e9e5625b4877b65e59188a868CAS | open url image1

[64]  E. C. Hammer, Z. Balogh-Brunstad, I. Jakobsen, P. A. Olsson, S. L. S. Stipp, M. C. Rillig, A mycorrhizal fungus grows on biochar and captures phosphorus from its surfaces. Soil Biol. Biochem. 2014, 77, 252.
A mycorrhizal fungus grows on biochar and captures phosphorus from its surfaces.CrossRef | 1:CAS:528:DC%2BC2cXht12ntL%2FI&md5=99da322fab5dc02b3614cb989cd7e4dfCAS | open url image1

[65]  W. C. Hockaday, A. M. Grannas, S. Kim, P. G. Hatcher, Direct molecular evidence for the degradation and mobility of black carbon in soils from ultrahigh-resolution mass spectral analysis of dissolved organic matter from a fire-impacted forest soil. Org. Geochem. 2006, 37, 501.
Direct molecular evidence for the degradation and mobility of black carbon in soils from ultrahigh-resolution mass spectral analysis of dissolved organic matter from a fire-impacted forest soil.CrossRef | 1:CAS:528:DC%2BD28Xit1ajtbs%3D&md5=d329d17984ba54dd2ba1a2b869355024CAS | open url image1

[66]  M. Wengel, E. Kothe, C. M. Schmidt, K. Heide, G. Gleixner, Degradation of organic matter from black shales and charcoal by the wood-rotting fungus Schizophyllum commune and release of DOC and heavy metals in the aqueous phase. Sci. Total Environ. 2006, 367, 383.
Degradation of organic matter from black shales and charcoal by the wood-rotting fungus Schizophyllum commune and release of DOC and heavy metals in the aqueous phase.CrossRef | 1:CAS:528:DC%2BD28Xnt1yhtbg%3D&md5=f4643475ac63511e9e8d8bfe06f237d4CAS | 16483638PubMed | open url image1

[67]  P. L. Ascough, C. J. Sturrock, M. I. Bird, Investigation of growth responses in saprophytic fungi to charred biomass. Isotopes Environ. Health Stud. 2010, 46, 64.
Investigation of growth responses in saprophytic fungi to charred biomass.CrossRef | 1:CAS:528:DC%2BC3cXjt1Wjsrk%3D&md5=a74d8d27c105e8db9f7e90dbcc31ca48CAS | 20229385PubMed | open url image1

[68]  A. Otto, C. Shunthirasingham, M. J. Simpson, A comparison of plant and microbial biomarkers in grassland soils from the Prairie Ecozone of Canada. Org. Geochem. 2005, 36, 425.
A comparison of plant and microbial biomarkers in grassland soils from the Prairie Ecozone of Canada.CrossRef | 1:CAS:528:DC%2BD2MXhtFejurs%3D&md5=b4b79e5b8b6cbfb9e4f151222812359bCAS | open url image1

[69]  P. E. Kolattukudy, K. E. Espelie, Chemistry, biochemistry and function of suberin and associated waxes, in Natural Products of Woody Plants (Ed. J. W. Rowe) 1989, pp. 304–367 (Springer: Berlin, Germany). 10.1007/978-3-642-74075-6

[70]  M. Riederer, K. Matzke, F. Ziegler, I. Kögel-Knabner, Occurrence, distribution and fate of the lipid plant biopolymers cutin and suberin in temperate forest soils. Org. Geochem. 1993, 20, 1063.
Occurrence, distribution and fate of the lipid plant biopolymers cutin and suberin in temperate forest soils.CrossRef | 1:CAS:528:DyaK2cXlvFSjsQ%3D%3D&md5=ec06cb2fc9d867d52477417f1861d608CAS | open url image1

[71]  M. A. Goñi, J. I. Hedges, Potential applications of cutin-derived CuO reaction products for discriminating vascular plant sources in natural environments. Geochim. Cosmochim. Acta 1990, 54, 3073.
Potential applications of cutin-derived CuO reaction products for discriminating vascular plant sources in natural environments.CrossRef | open url image1

[72]  K. Lorenz, R. Lal, C. M. Preston, K. G. J. Nierop, Strengthening the soil organic carbon pool by increasing contributions from recalcitrant aliphatic bio(macro)molecules. Geoderma 2007, 142, 1.
Strengthening the soil organic carbon pool by increasing contributions from recalcitrant aliphatic bio(macro)molecules.CrossRef | 1:CAS:528:DC%2BD2sXhtFels7%2FE&md5=ba38bc99aba501799ee797cd0adaa22fCAS | open url image1

[73]  Y. Olshansky, T. Polubesova, B. Chefetz, Reconstitution of cutin monomers on smectite surfaces: adsorption and esterification. Geoderma 2014, 232–234, 406.
Reconstitution of cutin monomers on smectite surfaces: adsorption and esterification.CrossRef | open url image1

[74]  S. Derenne, C. Largeau, A review of some important families of refractory macromolecules: composition, origin, and fate in soils and sediments. Soil Sci. 2001, 166, 833.
A review of some important families of refractory macromolecules: composition, origin, and fate in soils and sediments.CrossRef | 1:CAS:528:DC%2BD3MXovVertrY%3D&md5=033986367e2caeded571dba000f7db5eCAS | open url image1

[75]  M. Thevenot, M. Dignac, C. Rumpel, Fate of lignins in soils: a review. Soil Biol. Biochem. 2010, 42, 1200.
Fate of lignins in soils: a review.CrossRef | 1:CAS:528:DC%2BC3cXntVektLk%3D&md5=f047eee751c12f1dd11a44e7eb625909CAS | open url image1

[76]  J. R. Ertel, J. I. Hedges, The lignin component of humic substances: distribution among soil and sedimentary humic, fulvic, and base-insoluble fractions. Geochim. Cosmochim. Acta 1984, 48, 2065.
The lignin component of humic substances: distribution among soil and sedimentary humic, fulvic, and base-insoluble fractions.CrossRef | 1:CAS:528:DyaL2cXmtlemsLg%3D&md5=107ab5cb8d5d74aa4aea0872678b82cfCAS | open url image1

[77]  S. Opsahl, R. Benner, Early diagenesis of vascular plant tissues: lignin and cutin decomposition and biogeochemical implications. Geochim. Cosmochim. Acta 1995, 59, 4889.
Early diagenesis of vascular plant tissues: lignin and cutin decomposition and biogeochemical implications.CrossRef | 1:CAS:528:DyaK2MXpvV2msrk%3D&md5=52cacd5a166217003c5e7c8586a58cb2CAS | open url image1

[78]  T. Riedel, S. Iden, J. Geilich, K. Wiedner, W. Durner, H. Biester, Changes in the molecular composition of organic matter leached from an agricultural topsoil following addition of biomass-derived black carbon (biochar). Org. Geochem. 2014, 69, 52.
Changes in the molecular composition of organic matter leached from an agricultural topsoil following addition of biomass-derived black carbon (biochar).CrossRef | 1:CAS:528:DC%2BC2cXksFyrsro%3D&md5=e67ab61bc6b80cea5167e4ab4c3b085bCAS | open url image1

[79]  Y. Kuzyakov, I. Bogomolova, B. Glaser, Biochar stability in soil: decomposition during eight years and transformation as assessed by compound-specific 14C analysis. Soil Biol. Biochem. 2014, 70, 229.
Biochar stability in soil: decomposition during eight years and transformation as assessed by compound-specific 14C analysis.CrossRef | 1:CAS:528:DC%2BC2cXitlCjt7k%3D&md5=2523652b64e8a3f03f41aa26c7e88374CAS | open url image1

[80]  S. Abiven, M. W. I. Schmidt, J. Lehmann, Biochar by design. Nat. Geosci. 2014, 7, 326.
Biochar by design.CrossRef | 1:CAS:528:DC%2BC2cXntVSnsbg%3D&md5=6d93c74499c6f6392a8f7382b82cf042CAS | open url image1



Supplementary MaterialSupplementary Material (892 KB) Export Citation Cited By (1)