Biology and Fertility of Soils

, Volume 54, Issue 2, pp 175–188 | Cite as

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

  • Junhui Chen
  • Xuan Sun
  • Jufeng Zheng
  • Xuhui Zhang
  • Xiaoyu Liu
  • Rongjun Bian
  • Lianqing Li
  • Kun Cheng
  • Jinwei Zheng
  • Genxing Pan
Original Paper


Topsoil samples were collected from plots in a dry cropland in the North China Plain 3 years after a single incorporation of biochar at 20 and 40 t ha−1 and analyzed for abundances and composition of microbial community and for respiration under controlled laboratory conditions at 15, 20, and 25 °C. The addition of biochar generally reduced soil respirations at the three temperatures and the temperature sensitivity (Q10) at 15–20 °C. Biochar amendment significantly increased bacterial 16S rRNA gene abundances and fungal ITS gene diversity and induced clear changes in their community compositions due to improvements in soil chemical properties such as soil organic C (SOC) and available N contents and pH. Illumina Miseq sequencing showed that the relative abundances of Actinobacteria, Gammaproteobacteria, Firmicutes, and Alternaria within Ascomycota, capable of decomposing SOC, were significantly decreased under biochar at 40 t ha−1. The Q10 values at 15–20 °C were significantly correlated with fungal diversity and dehydrogenase activity. Our results suggest that after 3 years a single biochar amendment could induce a shift in microbial community composition and functioning towards a slower organic C turnover and stability to warming, which may potentially reduce soil C loss in dryland under climate warming in the future.


Biochar Soil organic carbon decomposition Temperature sensitivity Pyrosequencing 



This work was funded by the National Science Foundation of China under grant numbers 41401318, 41371300, and 41371298, and the Scientific Research Foundation of Zhejiang A & F University under grant number 2014FR024. 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.

Supplementary material

374_2017_1253_MOESM1_ESM.docx (16 kb)
ESM 1 (DOCX 15 kb)


  1. Alef K, Nannipieri P (1995) Chapter 7-enzyme activities. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic Press, London, pp 311–373Google Scholar
  2. Alexopoulos CJ, Mims CW, Blackwell M (1996) Introductory mycology, Fourth edn. John Wiley & Sons, New YorkGoogle Scholar
  3. Ameloot N, De Neve S, Jegajeevagan K, Yildiz G, Buchan D, Funkuin YN, Prins W, Bouckaert L, Sleutel S (2013) Short-term CO2 and N2O emissions and microbial properties of biochar amended sandy loam soils. Soil Biol Biochem 57:401–410CrossRefGoogle Scholar
  4. 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 78:195–203CrossRefGoogle Scholar
  5. Arfi Y, Marchand C, Wartel M, Record E (2012) Fungal diversity in anoxic-sulfidic sediments in a mangrove soil. Fungal Ecol 5:282–285CrossRefGoogle Scholar
  6. Atkinson CJ, Fitzgerald JD, Hipps NA (2010) Potential mechanisms for achieving agricultural benefits from biochar application to temperate soils: a review. Plant Soil 337:1–18CrossRefGoogle Scholar
  7. Bardgett R, Saggar S (1994) Effects of heavy metal contamination on the short-term decomposition of labelled [14C] glucose in a pasture soil. Soil Biol Biochem 26:727–733CrossRefGoogle Scholar
  8. Bell CW, Fricks BE, Rocca JD, Steinweg JM, McMahon SK, Wallenstein MD (2013) High-throughput fluorometric measurement of potential soil extracellular enzyme activities. J Visual Experi: JoVE 50961Google Scholar
  9. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedPubMedCentralGoogle Scholar
  10. Castaldi S, Riondino M, Baronti S, Esposito FR, Marzaioli R, Rutigliano FA, Vaccari FP, Miglietta F (2011) Impact of biochar application to a Mediterranean wheat crop on soil microbial activity and greenhouse gas fluxes. Chemosphere 85:1464–1471CrossRefPubMedGoogle Scholar
  11. Chen J, Liu X, Zheng J, Zhang B, Lu H, Chi Z, Pan G, Li L, Zheng J, Zhang X, Wang J, Yu X (2013) Biochar soil amendment increased bacterial but decreased fungal gene abundance with shifts in community structure in a slightly acid rice paddy from Southwest China. Appl Soil Ecol 71:33–44CrossRefGoogle Scholar
  12. 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 91:68–79CrossRefGoogle Scholar
  13. 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 67:857–867CrossRefGoogle Scholar
  14. 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 574:24–33CrossRefPubMedGoogle Scholar
  15. Conant RT, Steinweg JM, Haddix ML, Paul EA, Plante AF, Six J (2008) Experimental warming shows that decomposition temperature sensitivity increases with soil organic matter recalcitrance. Ecology 89:2384–2391CrossRefPubMedGoogle Scholar
  16. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173CrossRefPubMedGoogle Scholar
  17. Domene X, Mattana S, Hanley K, Enders A, Lehmann J (2014) Medium-term effects of corn biochar addition on soil biota activities and functions in a temperate soil cropped to corn. Soil Biol Biochem 72:152–162CrossRefGoogle Scholar
  18. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefPubMedPubMedCentralGoogle Scholar
  19. Fang C, Smith P, Moncrieff JB, Smith JU (2005) Similar response of labile and resistant soil organic matter pools to changes in temperature. Nature 433:57–59CrossRefPubMedGoogle Scholar
  20. Fang Y, Singh BP, Singh B (2014) Temperature sensitivity of biochar and native carbon mineralisation in biochar-amended soils. Agric Ecosyst Environ 191:158–167CrossRefGoogle Scholar
  21. Farrell M, Kuhn TK, Macdonald LM, Maddern TM, Murphy DV, Hall PA, Singh BP, Baumann K, Krull ES, Baldock JA (2013) Microbial utilisation of biochar-derived carbon. Sci Total Environ 465:288–297CrossRefPubMedGoogle Scholar
  22. Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120CrossRefPubMedPubMedCentralGoogle Scholar
  23. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364CrossRefPubMedGoogle Scholar
  24. Hartley IP, Ineson P (2008) Substrate quality and the temperature sensitivity of soil organic matter decomposition. Soil Biol Biochem 40:1567–1574CrossRefGoogle Scholar
  25. He X, Du Z, Wang Y, Lu N, Zhang Q (2016) Sensitivity of soil respiration to soil temperature decreased under deep biochar amended soils in temperate croplands. Appl Soil Ecol 108:204–210CrossRefGoogle Scholar
  26. Insam H (2001) Developments in soil microbiology since the mid 1960s. Geoderma 100:389–402CrossRefGoogle Scholar
  27. Jenkins JR, Viger M, Arnold EC, Harris ZM, Ventura M, Miglietta F, Girardin C, Edwards RJ, Rumpel C, Fornasier F, Zavalloni C, Tonon G, Alberti G, Taylor G (2017) Biochar alters the soil microbiome and soil function: results of next-generation amplicon sequencing across Europe. GCB Bioenergy 9:591–612CrossRefGoogle Scholar
  28. 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 52:1–14CrossRefGoogle Scholar
  29. Jin H (2010) Characterization of microbial life colonizing biochar and biochar-amended soils. Dissertation, Cornell UniversityGoogle Scholar
  30. Jones DL, Murphy DV, Khalid M, Ahmad W, Edwards-Jones G, DeLuca TH (2011) Short-term biochar-induced increase in soil CO2 release is both biotically and abiotically mediated. Soil Biol Biochem 43:1723–1731CrossRefGoogle Scholar
  31. Jones DL, Rousk J, Edwards-Jones G, DeLuca TH, Murphy DV (2012) Biochar-mediated changes in soil quality and plant growth in a three year field trial. Soil Biol Biochem 45:113–124CrossRefGoogle Scholar
  32. Keith A, Singh B, Singh BP (2011) Interactive priming of biochar and labile organic matter mineralization in a smectite-rich soil. Environ Sci Technol 45:9611–9618CrossRefPubMedGoogle Scholar
  33. Khodadad CLM, Zimmerman AR, Green SJ, Uthandi S, Foster JS (2011) Taxa-specific changes in soil microbial community composition induced by pyrogenic carbon amendments. Soil Biol Biochem 43:385–392CrossRefGoogle Scholar
  34. 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 27:753–760CrossRefGoogle Scholar
  35. Kramer C, Gleixner G (2008) Soil organic matter in soil depth profiles: distinct carbon preferences of microbial groups during carbon trasformation. Soil Biol Biochem 40:425–433CrossRefGoogle Scholar
  36. Kuzyakov Y, Subbotina I, Chen H, Bogomolova I, Xu X (2009) Black carbon decomposition and incorporation into soil microbial biomass estimated by 14C labeling. Soil Biol Biochem 41:210–219CrossRefGoogle Scholar
  37. Laird D, Fleming P, Wang BQ, Horton R, Karlen D (2010) Biochar impact on nutrient leaching from a Midwestern agricultural soil. Geoderma 158:436–442CrossRefGoogle Scholar
  38. Lal R (2004) Soil carbon sequestration impacts on global climate change and food security. Science 11:1623–1627CrossRefGoogle Scholar
  39. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microb 75:5111–5120CrossRefGoogle Scholar
  40. Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota—a review. Soil Biol Biochem 43:1812–1836CrossRefGoogle Scholar
  41. Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24CrossRefGoogle Scholar
  42. Liski J, Ilvesniemi H, Mäkelä A, Westman CJ (1999) CO2 emissions from soil in response to climatic warming are overestimated: the decomposition of old soil organic matter is tolerant of temperature. Ambio 28:171–174Google Scholar
  43. 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 76:12–21CrossRefGoogle Scholar
  44. Luo Y, Wan S, Hui D, Wallace L (2001) Acclimation of soil respiration to warming in a tall grass prairie. Nature 413:622–625CrossRefPubMedGoogle Scholar
  45. Luo Y, Durenkamp M, De Nobili M, Lin Q, Devonshire BJ, Brookes PC (2013) Microbial biomass growth, following incorporation of biochars produced at 350 °C or 700 °C, in a silty-clay loam soil of high and low pH. Soil Biol Biochem 57:513–523CrossRefGoogle Scholar
  46. Maestrini B, Herrmann AM, Nannipieri P, Schmidt MWI, Abiven S (2014) Ryegrass-derived pyrogenic organic matter changes organic carbon and nitrogen mineralization in a temperate forest soil. Soil Biol Biochem 69:291–301CrossRefGoogle Scholar
  47. Maestrini B, Nannipieri P, Abiven S (2015) A meta-analysis on pyrogenic organic matter induced priming effect. GCB Bioenergy 7:577–590CrossRefGoogle Scholar
  48. Major J, Rondon M, Molina D, Riha SJ, Lehmann J (2012) Nutrient leaching in a Colombian savanna Oxisol amended with biochar. J Environ Qual 41:1076–1086CrossRefPubMedGoogle Scholar
  49. Marschner P, Kandeler E, Marschner B (2003) Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biol Biochem 35:453–461CrossRefGoogle Scholar
  50. Menichetti L, Reyes Ortigoza AL, García N, Giagnoni L, Nannipieri P, Renella G (2015) Thermal sensitivity of enzyme activity in tropical soils assessed by the Q10 and equilibrium model. Biol Fertil Soils 51:299–310CrossRefGoogle Scholar
  51. 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 81:244–254CrossRefGoogle Scholar
  52. Mulvaney RL (1996) Nitrogen-inorganic forms. In: Bigham JM (ed) Methods of soil analysis, part 3 chemical methods, The Soil Science Society of American Book Series no 5. Soil Science Society of American, Inc., American Society of Agronomy, Inc., Madison, WI, pp 1123–1184Google Scholar
  53. Noyce G, Basiliko N, Fulthorpe R, Sackett T, Thomas S (2015) Soil microbial responses over 2 years following biochar addition to a north temperate forest. Biol Fertil Soils 51:649–659CrossRefGoogle Scholar
  54. Omondi MO, Xia X, Nahayo A, Liu X, Korai PK, Pan G (2016) Quantification of biochar effects on soil hydrological properties using meta-analysis of literature data. Geoderma 274:28–34CrossRefGoogle Scholar
  55. Pan G, Smith P, Pan W (2009) The role of soil organic matter in maintaining the productivity and yield stability of cereals in China. Agric Ecosyst Environ 129:344–348CrossRefGoogle Scholar
  56. Pietikäinen J, Kiikkilä O, Fritze H (2000) Charcoal as a habitat for microbes and its effect on the microbial community of the underlying humus. Oikos 89:231–242CrossRefGoogle Scholar
  57. Pronk GJ, Heister K, Ding GC, Smalla K, Kögel-Knabner I (2012) Development of biogeochemical interfaces in an artificial soil incubation experiment; aggregation and formation of organo-mineral associations. Geoderma 189:585–594CrossRefGoogle Scholar
  58. Quilliam RS, Glanville HC, Wade SC, Jones DL (2013) Life in the ‘charosphere’—does biochar in agricultural soil provide a significant habitat for microorganisms? Soil Biol Biochem 65:287–293CrossRefGoogle Scholar
  59. Rousk J, Brookes PC, Bååth E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microb 75:1589–1596CrossRefGoogle Scholar
  60. Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351CrossRefPubMedGoogle Scholar
  61. Rousk J, Dempster DN, Jones DL (2013) Transient biochar effects on decomposer microbial growth rates: evidence from two agricultural case-studies. Eur J Soil Sci 64:770–776CrossRefGoogle Scholar
  62. Schlesinger W, Andrews J (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20CrossRefGoogle Scholar
  63. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kogel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56CrossRefPubMedGoogle Scholar
  64. Schulze ED, Freibauer A (2005) Environmental science: carbon unlocked from soils. Nature 437:205–206CrossRefPubMedGoogle Scholar
  65. Serra-Wittling C, Houot S, Barriuso E (1995) Soil enzymatic response to addition of municipal solid-waste compost. Biol Fertil Soils 20:226–236CrossRefGoogle Scholar
  66. Singh BP, Cowie AL (2014) Long-term influence of biochar on native organic carbon mineralisation in a low-carbon clayey soil. Sci Rep-UK 4:e3687CrossRefGoogle Scholar
  67. Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264CrossRefPubMedGoogle Scholar
  68. Smith P, Marino D, Cai ZC, Gwary D, Janzen H, Kumar P (2008) Greenhouse gas mitigation in agriculture. Philos Trans R Soc B 363:789–813CrossRefGoogle Scholar
  69. Sohi S, Krull E, Lopez-Capel E, Bol R (2010) A review of biochar and its use and function in soil. Adv Agronomy 105:47–82CrossRefGoogle Scholar
  70. Soil Survey Staff (1999) Soil taxonomy, a basic classification for making and interpreting soil surveys. In: Agriculture Handbook 436, 2nd edn. Natural Resources Conservation Service, Washington, pp 869Google Scholar
  71. Song GH, Li LQ, Pan GX, Zhang Q (2005) Topsoil organic carbon storage of China and its loss by cultivation. Biogeochemistry 74:47–62CrossRefGoogle Scholar
  72. Taghizadeh-Toosi A, Clough T, Sherlock R, Condron L (2012) Biochar adsorbed ammonia is bioavailable. Plant Soil 350:57–69CrossRefGoogle Scholar
  73. Thiet RK, Frey SD, Six J (2006) Do growth yield efficiencies differ between soil microbial communities differing in fungal:bacterial ratios? Reality check and methodological issues. Soil Biol Biochem 38:837–844CrossRefGoogle Scholar
  74. von Lützow M, Kögel-Knabner I (2009) Temperature sensitivity of soil organic matter decomposition—what do we know? Biol Fertil Soils 46:1–15CrossRefGoogle Scholar
  75. Warnock D, Lehmann J, Kuyper T, Rillig M (2007) Mycorrhizal responses to biochar in soil—concepts and mechanisms. Plant Soil 300:9–20CrossRefGoogle Scholar
  76. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar
  77. Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass C by fumigation-extraction—an automated procedure. Soil Biol Biochem 22:1167–1169CrossRefGoogle Scholar
  78. Yao Q, Liu J, Yu Z, Li Y, Jin J, Liu X, Wang G (2017a) Changes of bacterial community compositions after three years of biochar application in a black soil of northeast China. Appl Soil Ecol 113:11–21CrossRefGoogle Scholar
  79. Yao Q, Liu J, Yu Z, Li Y, Jin J, Liu X, Wang G (2017b) Three years of biochar amendment alters soil physiochemical properties and fungal community composition in a black soil of northeast China. Soil Biol Biochem 110:56–67CrossRefGoogle Scholar
  80. Zhang A, Liu Y, Pan G, Hussain Q, Li L, Zheng J, Zhang X (2012) Effect of biochar amendment on maize yield and greenhouse gas emissions from a soil organic carbon poor calcareous loamy soil from Central China Plain. Plant Soil 351:263–275CrossRefGoogle Scholar
  81. Zhang K, Chen L, Li Y, Brookes PC, Xu J, Luo Y (2017) The effects of combinations of biochar, lime, and organic fertilizer on nitrification and nitrifiers. Biol Fertil Soils 53:77–87CrossRefGoogle Scholar
  82. Zheng J, Chen J, Pan G, Liu X, Zhang X, Li L, Bian R, Cheng K, Jinwei Z (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 571:206–217CrossRefPubMedGoogle Scholar
  83. Zhou H, Zhang D, Wang P, Liu X, Cheng K, Li L, Zheng J, Zhang X, Zheng J, Crowley D, van Zwieten L, Pan G (2017) Changes in microbial biomass and the metabolic quotient with biochar addition to agricultural soils: a meta-analysis. Agric Ecosyst Environ 239:80–89CrossRefGoogle Scholar
  84. Zhou J, Wu L, Deng Y, Zhi X, Jiang Y-H, Tu Q, Xie J, Van Nostrand JD, He Z, Yang Y (2011) Reproducibility and quantitation of amplicon sequencing-based detection. ISME J 5:1303–1313CrossRefPubMedPubMedCentralGoogle Scholar
  85. Zimmerman AR, Gao B, Ahn M-Y (2011) Positive and negative carbon mineralization priming effects among a variety of biochar-amended soils. Soil Biol Biochem 43:1169–1179CrossRefGoogle Scholar
  86. Zimmermann M, Leifeld J, Conen F, Bird MI, Meir P (2012) Can composition and physical protection of soil organic matter explain soil respiration temperature sensitivity? Biogeochemistry 107:423–436CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Institute of Resource, Ecosystem and Environment of AgricultureNanjing Agricultural UniversityNanjingChina
  2. 2.Zhejiang Provincial Key Laboratory of Carbon Cycling in Forest Ecosystems and Carbon Sequestration, School of Environmental and Resource SciencesZhejiang A & F UniversityHangzhouChina
  3. 3.Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource UtilizationNanjingChina

Personalised recommendations