Abstract
The role of soil organic C (SOC) quality affecting microbial community composition and function under biochar application is poorly understood. We investigated the relationship between the pool size and chemical composition of SOC; composition of main microbial groups; enzyme activities involved in C, N, and P cycling; and soil respiration in a rice paddy amended with biochar for 20 months in a laboratory experiment at 15, 25, and 35 °C. Soil labile and recalcitrant organic C pools were determined by a two-step sulfuric acid (H2SO4) hydrolysis method. The chemical composition of SOC was determined with 13C-nuclear magnetic resonance spectroscopy. The biochar amendment at 20 and 40 t ha−1 significantly decreased the soil labile C pool I (extracted by 5 N H2SO4), alkyl, and carbonyl C contents and increased the recalcitrant C pool (acid-resistant) and aromatic C contents and the aromatic C to O-alkyl C ratio. The phospholipid-fatty acid concentrations and soil enzyme activities were unchanged by biochar application at 10 and 20 t ha−1, but both were increased at 40 t ha−1. Biochar increased the ratio of gram-positive (G+) to gram-negative (G−) bacteria and decreased that of fungi to bacteria. The recalcitrant C pool and aromatic C contents were positively correlated to the G+ bacteria abundance and were important factors in shaping composition of the main microbial groups and improving enzyme activities. Biochar application at 40 t ha−1 lowered soil respiration rates at 15 and 25 °C by decreasing labile C pool and increasing C recalcitrancy while increased temperature sensitivities of soil respiration at 25/15 °C and 35/25 °C by stimulating microbial abundance and enzyme activities. Together, our results suggest that biochar soil amendment shifted microbial community composition and function through influencing the composition of SOC.
Similar content being viewed by others
References
Ameloot N, Sleutel S, Case SDC, Alberti G, McNamara NP, Zavalloni C, Vervisch B, Gd V, De Neve S (2014) C mineralization and microbial activity in four biochar field experiments several years after incorporation. Soil Biol Biochem 78:195–203
Blagodatskaya Е, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol Fertil Soils 45:115–131
Bossio DA, Scow KM (1998) Impact of carbon and flooding on PLFA profiles and substrate utilization patterns of soil microbial communities. Microb Ecol 35:265–278
Bremner JM (1996) Nitrogen total. In: Sparks DL (ed) Methods of soil analysis, part 3 chemical methods, the soil science Society of American Book Series no 5. Soil Science Society of America, Inc., Madison, WI, pp 1085–1122
Brookes PC, Chen Y, Chen L, Qiu G, Luo Y, Xu J (2017) Is the rate of mineralization of soil organic carbon under microbiological control? Soil Biol Biochem 112:127–139
Budai A, Rasse DP, Lagomarsino A, Lerch TZ, Paruch L (2016) Biochar persistence, priming and microbial responses to pyrolysis temperature series. Biol Fertil Soils 52:749–761
Cao XY, Pignatello JJ, Li Y, Lattao C, Chappell MA, Chen N, Miller LF, Mao JD (2012) Characterization of wood chars produced at different temperatures using advanced solid-state 13C NMR spectroscopic techniques. Energ Fuel 26:5983–5991
Chen J, Liu X, Li L, Zheng J, Qu J, Zheng J, Zhang X, Pan G (2015) Consistent increase in abundance and diversity but variable change in community composition of bacteria in topsoil of rice paddy under short term biochar treatment across three sites from South China. Appl Soil Ecol 91:68–79
Chen J, Sun X, Li L, Liu X, Zhang B, Zheng J, Pan G (2016) Change in active microbial community structure, abundance and carbon cycling in an acid rice paddy soil with the addition of biochar. Eur J Soil Sci 67:857–867
Chen J, Li S, Liang C, Xu Q, Li Y, Qin H, Fuhrmann JJ (2017) Response of microbial community structure and function to short-term biochar amendment in an intensively managed bamboo (Phyllostachys praecox) plantation soil: effect of particle size and addition rate. Sci Total Environ 574:24–33
Chen J, Sun X, Zheng J, Zhang X, Liu X, Bian R, Li L, Cheng K, Zheng J, Pan G (2018) Biochar amendment changes temperature sensitivity of soil respiration and composition of microbial communities 3 years after incorporation in an organic carbon-poor dry cropland soil. Biol Fertil Soils 54:175–188
Cheng L, Zhang N, Yuan M, Xiao J, Qin Y, Deng Y, Tu Q, Xue K, Van Nostrand JD, Wu L, He Z, Zhou X, Leigh MB, Konstantinidis KT, Schuur EAG, Luo Y, Tiedje JM, Zhou J (2017) Warming enhances old organic carbon decomposition through altering functional microbial communities. ISME J 11:1825–1835
Conant RT, Ryan MG, Ågren GI, Birge HE, Davidson EA, Eliasson PE, Evans SE, Frey SD, Giardina CP, Hopkins FM, Hyvönen R, Kirschbaum MUF, Lavallee JM, Leifeld J, Parton WJ, Megan Steinweg J, Wallenstein MD, Martin Wetterstedt JÅ, Bradford MA (2011) Temperature and soil organic matter decomposition rates—synthesis of current knowledge and a way forward. Glob Chang Biol 17:3392–3404
Conrad R, Klose M (1999) Anaerobic conversion of carbon dioxide to methane, acetate and propionate on washed rice roots. FEMS Microbiol Ecol 30:147–155
Craine JM, Fierer N, McLauchlan KK (2010) Widespread coupling between the rate and temperature sensitivity of organic matter decay. Nat Geosci 3:854–857
Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173
DeForest JL (2009) 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 41:1180–1186
Dong X, Li G, Lin Q, Zhao X (2017) Quantity and quality changes of biochar aged for 5 years in soil under field conditions. Catena 159:136–143
Fang C, Smith P, Moncrieff JB, Smith JU (2005) Similar response of labile and resistant soil organic matter pools to changes in temperature. Nature 433:57–59
Fang Y, Singh BP, Singh B (2014) Temperature sensitivity of biochar and native carbon mineralisation in biochar-amended soils. Agric Ecosyst Environ 191:158–167
Fang Y, Singh BP, Matta P, Cowie AL, Van Zwieten L (2017) Temperature sensitivity and priming of organic matter with different stabilities in a vertisol with aged biochar. Soil Biol Biochem 115:346–356
Gong ZT, Zhang GL, Chen ZC (2007) Pedogenesis and soil taxonomy. Science Press, Beijing, China
Jiang X, Denef K, Stewart C, Cotrufo MF (2016) Controls and dynamics of biochar decomposition and soil microbial abundance, composition, and carbon use efficiency during long-term biochar-amended soil incubations. Biol Fertil Soils 52:1–14
Karhu K, Auffret MD, Dungait JAJ, Hopkins DW, Prosser JI, Singh BK, Subke J-A, Wookey PA, Agren GI, Sebastia M-T, Gouriveau F, Bergkvist G, Meir P, Nottingham AT, Salinas N, Hartley IP (2014) Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513:81–84
Keiblinger KM, Hall EK, Wanek W, Szukics U, Hämmerle I, Ellersdorfer G, Böck S, Strauss J, Sterflinger K, Richter A, Zechmeister-Boltenstern S (2010) The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency. FEMS Microbiol Ecol 73:430–440
Kirschbaum MUF (1995) The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic carbon storage. Soil Biol Biochem 27:753–760
Kramer C, Gleixner G (2008) Soil organic matter in soil depth profiles: distinct carbon preferences of microbial groups during carbon transformation. Soil Biol Biochem 40:425–433
Lammirato C, Miltner A, Kaestner M (2011) Effects of wood char and activated carbon on the hydrolysis of cellobiose by β-glucosidase from Aspergillus niger. Soil Biol Biochem 43:1936–1942
Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota—a review. Soil Biol Biochem 43:1812–1836
Li Y, Zhang J, Chang SX, Jiang P, Zhou G, Fu S, Yan E, Wu J, Lin L (2013) Long-term intensive management effects on soil organic carbon pools and chemical composition in Moso bamboo (Phyllostachys pubescens) forests in subtropical China. Forest Ecol Manag 303:121–130
Li Y, Li Y, Chang SX, Liang X, Qin H, Chen J, Xu Q (2017) Linking soil fungal community structure and function to soil organic carbon chemical composition in intensively managed subtropical bamboo forests. Soil Biol Biochem 107:19–31
Li Y, Li Y, Chang SX, Yang Y, Fu S, Jiang P, Luo Y, Yang M, Chen Z, Hu S, Zhao M, Liang X, Xu Q, Zhou G, Zhou J (2018) Biochar reduces soil heterotrophic respiration in a subtropical plantation through increasing soil organic carbon recalcitrancy and decreasing carbon-degrading microbial activity. Soil Biol Biochem 122:173–185
Liu X, Zheng J, Zhang D, Cheng K, Zhou H, Zhang A, Li L, Joseph S, Smith P, Crowley D, Kuzyakov Y, Pan G (2016) Biochar has no effect on soil respiration across Chinese agricultural soils. Sci Total Environ 554-555:259–265
Lu W, Ding W, Zhang J, Li Y, Luo J, Bolan N, Xie Z (2014) Biochar suppressed the decomposition of organic carbon in a cultivated sandy loam soil: a negative priming effect. Soil Biol Biochem 76:12–21
Luo Y, Durenkamp M, De Nobili M, Lin Q, Brookes PC (2011) Short term soil priming effects and the mineralisation of biochar following its incorporation to soils of different pH. Soil Biol Biochem 43:2304–2314
Mao JD, Johnson RL, Lehmann J, Olk DC, Neves EG, Thompson ML, Schmidt-Rohr K (2012) Abundant and stable char residues in soils: implications for soil fertility and carbon sequestration. Environ Sci Technol 46:9571–9576
Mitchell PJ, Simpson AJ, Soong R, Simpson MJ (2015) Shifts in microbial community and water-extractable organic matter composition with biochar amendment in a temperate forest soil. Soil Biol Biochem 81:244–254
Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670
Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762
Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19
Nelson DW, Sommers LE (1982) Total carbon, organic carbon and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2 chemical and microbiological properties. American Society of Agronomy, Inc., Soil Science Society of America, Inc., Madison, WI, pp 539–579
Ng EL, Patti AF, Rose MT, Schefe CR, Wilkinson K, Smernik RJ, Cavagnaro TR (2014) Does the chemical nature of soil carbon drive the structure and functioning of soil microbial communities? Soil Biol Biochem 70:54–61
Nguyen TT, Marschner P (2016) Soil respiration, microbial biomass and nutrient availability in soil after repeated addition of low and high C/N plant residues. Biol Fertil Soils 52:165–176
Panettieri M, Knicker H, Murillo JM, Madejón E, Hatcher PG (2014) Soil organic matter degradation in an agricultural chronosequence under different tillage regimes evaluated by organic matter pools, enzymatic activities and CPMAS 13C NMR. Soil Biol Biochem 78:170–181
Paz-Ferreiro J, Gascó G, Gutiérrez B, Méndez A (2012) Soil biochemical activities and the geometric mean of enzyme activities after application of sewage sludge and sewage sludge biochar to soil. Biol Fertil Soils 48:511–517
Pei J, Zhuang S, Cui J, Li J, Li B, Wu J, Fang C (2017) Biochar decreased the temperature sensitivity of soil carbon decomposition in a paddy field. Agric Ecosyst Environ 249:156–164
Prayogo C, Jones J, Baeyens J, Bending G (2014) 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 50:695–702
Rovira P, Vallejo VR (2002) Labile and recalcitrant pools of carbon and nitrogen in organic matter decomposing at different depths in soil: an acid hydrolysis approach. Geoderma 107:109–141
Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315
Schlesinger W, Andrews J (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20
Sihi D, Inglett PW, Inglett KS (2016) Carbon quality and nutrient status drive the temperature sensitivity of organic matter decomposition in subtropical peat soils. Biogeochemistry 131:103–119
Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404
Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24
Smith JL, Collins HP, Bailey VL (2010) The effect of young biochar on soil respiration. Soil Biol Biochem 42:2345–2347
Sun J, Drosos M, Mazzei P, Savy D, Todisco D, Vinci G, Pan G, Piccolo A (2017) The molecular properties of biochar carbon released in dilute acidic solution and its effects on maize seed germination. Sci Total Environ 576:858–867
Tian J, Wang J, Dippold M, Gao Y, Blagodatskaya E, Kuzyakov Y (2016) Biochar affects soil organic matter cycling and microbial functions but does not alter microbial community structure in a paddy soil. Sci Total Environ 556:89–97
Trasar-Cepeda C, Gil-Sotres F, Leirós MC (2007) Thermodynamic parameters of enzymes in grassland soils from Galicia, NW Spain. Soil Biol Biochem 39:311–319
von Lützow M, Kögel-Knabner I (2009) Temperature sensitivity of soil organic matter decomposition—what do we know? Biol Fertil Soils 46:1–15
Wagai R, Kishimoto-Mo AW, Yonemura S, Shirato Y, Hiradate S, Yagasaki Y (2013) Linking temperature sensitivity of soil organic matter decomposition to its molecular structure, accessibility, and microbial physiology. Glob Chang Biol 19:1114–1125
Wallenstein MD, McMahon SK, Schimel JP (2009) Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Glob Chang Biol 15:1631–1639
Wei C, Yu Q, Bai E, Lü X, Li Q, Xia J, Kardol P, Liang W, Wang Z, Han X (2013) Nitrogen deposition weakens plant-microbe interactions in grassland ecosystems. Glob Chang Biol 19:3688–3697
Wu J, Jorgensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass-C by fumigation-extraction-an automated procedure. Soil Biol Biochem 22:1167–1169
Yao H, Thornton B, Paterson E (2012) Incorporation of 13C-labelled rice rhizodeposition carbon into soil microbial communities under different water status. Soil Biol Biochem 53:72–77
Zak DR, Pregitzer KS, Curtis PS, Holmes WE (2000) Atmospheric CO2 and the composition and function of soil microbial communities. Ecol Appl 10:47–59
Zheng J, Chen J, Pan G, Liu X, Zhang X, Li L, Bian R, Cheng K, Zheng J (2016) Biochar decreased microbial metabolic quotient and shifted community composition four years after a single incorporation in a slightly acid rice paddy from Southwest China. Sci Total Environ 571:206–217
Zhou JZ, Xue K, Xie JP, Deng Y, Wu LY, Cheng XL, Fei SF, Deng SP, He ZL, Van Nostrand JD, Luo YQ (2012) Microbial mediation of carbon-cycle feedbacks to climate warming. Nat Clim Chang 2:106–110
Zhou G, Zhou X, Zhang T, Du Z, He Y, Wang X, Shao J, Cao Y, Xue S, Wang H, Xu C (2017) Biochar increased soil respiration in temperate forests but had no effects in subtropical forests. Forest Ecol Manag 405:339–349
Zhu Z, Ge T, Luo Y, Liu S, Xu X, Tong C, Shibistova O, Guggenberger G, Wu J (2018) Microbial stoichiometric flexibility regulates rice straw mineralization and its priming effect in paddy soil. Soil Biol Biochem 121:67–76
Acknowledgements
We thank Dr. Paolo Nannipieri, the Editor-in-Chief, and the anonymous reviewers for their very valuable comments in improving both the language and scientific quality of the manuscript.
Funding
This work was funded by the National Natural Science Foundation of China under grant numbers 41401318, 41371298, and 31470626, and the Natural Science Foundation of Zhejiang Province under grant number LGF18C160001.
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
ESM 1
(DOCX 178 kb)
Rights and permissions
About this article
Cite this article
Chen, J., Chen, D., Xu, Q. et al. Organic carbon quality, composition of main microbial groups, enzyme activities, and temperature sensitivity of soil respiration of an acid paddy soil treated with biochar. Biol Fertil Soils 55, 185–197 (2019). https://doi.org/10.1007/s00374-018-1333-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-018-1333-2