Skip to main content
Log in

Response of soil bacterial community to biochar application in a boreal pine forest

  • Original Paper
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

Abstract

Boreal forests commonly suffer from nitrogen deficiency due to low rate of nitrogen mineralization. Biochar may promote soil organic matter decomposition and accelerate nitrogen mineralization. In this study, Illumina NovaSeq sequencing combined with functional annotation of prokaryotic taxa (FAPROTAX) analysis was used to investigate the effect of biochar pyrolysis temperatures, the amount of applied biochar, and the period since the biochar application (2- and 3-year) on soil bacterial communities. The results show that biochar pyrolysis temperatures (500 °C and 650 °C) and the amount of applied biochar (0.5 kg m−2 and 1.0 kg m−2) did not change soil properties. Nevertheless, the interaction of biochar pyrolysis temperature and the amount had significant effects on bacterial species richness and evenness (P < 0.05). The application of biochar produced at 500 °C had a lower abundance of Actinobacteria and Verrucomicrobia, while that produced at 650 °C had a higher abundance of Conexibacter and Phenylobacterium. When biochar produced at 650 °C was applied, applying 0.5 kg m−2 had a higher abundance of Cyanobacteria, Conexibacter, and Phenylobacterium than that of 1.0 kg m−2 (P < 0.05). Functionally, the abundance of the aromatic compound degradation group increased with the extension of application time and increase of pyrolysis temperature. The time since application played an important role in the formation of soil bacterial communities and their functional structure. Long-term studies are necessary to understand the consequence of biochar on bacterial communities in boreal forests.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The datasets generated during and/or analysed during the current study are available in the NCBI Sequence Read Archive (SRA) database (https://www.ncbi.nlm.nih.gov/sra) with the following Accession Number: SRP341147.

References

  • Abujabhah IS, Doyle RB, Bound SA, Bowman JP (2017) Assessment of bacterial community composition, methanotrophic and nitrogen-cycling bacteria in three soils with different biochar application rates. J Soils Sediments 18(1):148–158

    Article  Google Scholar 

  • Adamczyk S, Adamczyk B, Kitunen V, Smolander A (2015) Monoterpenes and higher terpenes may inhibit enzyme activities in boreal forest soil. Soil Biol Biochem 87:59–66

    Article  CAS  Google Scholar 

  • Adamczyk B, Karonen M, Adamczyk S, Engström MT, Laakso T, Saranpää P, Kitunen V, Smolander A, Simon J (2017) Tannins can slow-down but also speed-up soil enzymatic activity in boreal forest. Soil Biol Biochem 107:60–67

    Article  CAS  Google Scholar 

  • Anders E, Watzinger A, Rempt F, Kitzler B, Wimmer B, Zehetner F, Stahr K, Zechmeister-Boltenstern S, Soja G (2013) Biochar affects the structure rather than the total biomass of microbial communities in temperate soils. Agric Food Sci 22(4):404–423

    Article  Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • Barberan A, McGuire KL, Wolf JA, Jones FA, Wright SJ, Turner BL, Essene A, Hubbell SP, Faircloth BC, Fierer N (2015) Relating belowground microbial composition to the taxonomic, phylogenetic, and functional trait distributions of trees in a tropical forest. Ecol Lett 18(12):1397–1405

    Article  PubMed  Google Scholar 

  • Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515(7528):505–511

    Article  CAS  PubMed  Google Scholar 

  • Bruckman VJ, Varol EA, Uzun BB, Liu J (2016) Biochar in the view of climate change mitigation: the FOREBIOM experience. In: Bruckman VJ (ed) Biochar: a regional supply chain approach in view of climate change mitigation, 1st edn. Cambridge University Press, Cambridge, pp 1–22

    Chapter  Google Scholar 

  • Cajander AK (1949) Forest types and their significance. Acta for Fenn 56:71

    Article  Google Scholar 

  • Chao A (1984) Non-parametric estimation of the classes in a population. Scand J Stat 11(4):265–270

    Google Scholar 

  • Clough TJ, Condron LM (2010) Biochar and the nitrogen cycle: introduction. J Environ Qual 39(4):1218–2122

    Article  CAS  PubMed  Google Scholar 

  • Cole EJ, Zandvakili OR, Blanchard J, Xing B, Hashemi M, Etemadi F (2019) Investigating responses of soil bacterial community composition to hardwood biochar amendment using high-throughput PCR sequencing. Appl Soil Ecol 136:80–85

    Article  Google Scholar 

  • 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 72:152–162

    Article  CAS  Google Scholar 

  • Fan S, Zuo J, Dong H (2020) Changes in soil properties and bacterial community composition with biochar amendment after six years. Agronomy 10(5):746

    Article  CAS  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88(6):1354–1364

    Article  PubMed  Google Scholar 

  • Hart S, Luckai N, Brando P (2013) Charcoal function and management in boreal ecosystems. J Appl Ecol 50(5):1197–1206

    Article  CAS  Google Scholar 

  • Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60(4):579–598

    Article  Google Scholar 

  • Haynes RJ, Swift RS (1990) Stability of soil aggregates in relation to organic constituents and soil water content. J Soil Sci 41(1):73–83

    Article  CAS  Google Scholar 

  • He Y, Zhou X, Jiang L, Li M, Du Z, Zhou G, Shao J, Wang X, Xu Z, Hosseini Bai S, Wallace H, Xu C (2017) Effects of biochar application on soil greenhouse gas fluxes: a meta-analysis. GCB Bioenergy 9(4):743–755

    Article  CAS  Google Scholar 

  • Hossain MZ, Bahar MM, Sarkar B, Donne SW, Ok YS, Palansooriya KN, Kirkham MB, Chowdhury S, Bolan N (2020) Biochar and its importance on nutrient dynamics in soil and plant. Biochar 2(4):379–420

    Article  Google Scholar 

  • 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(3):591–612

    Article  CAS  Google Scholar 

  • Jiang X, Denef K, Stewart CE, Cotrufo MF (2015) 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):1–14

    Article  Google Scholar 

  • Kalam S, Basu A, Ahmad I, Sayyed RZ, El-Enshasy HA, Dailin DJ, Suriani NL (2020) Recent understanding of soil Acidobacteria and their ecological significance: a critical review. Front Microbiol. https://doi.org/10.3389/fmicb.2020.580024

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(2):385–392

    Article  CAS  Google Scholar 

  • Kolb SE, Fermanich KJ, Dornbush ME (2009) Effect of charcoal quantity on microbial biomass and activity in temperate soils. Soil Sci Soc Am J 73(4):1173–1181

    Article  CAS  Google Scholar 

  • Kolton M, Meller Harel Y, Pasternak Z, Graber ER, Elad Y, Cytryn E (2011) Impact of biochar application to soil on the root-associated bacterial community structure of fully developed greenhouse pepper plants. Appl Environ Microbiol 77(14):4924–4930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuzyakov Y, Bogomolova I, Glaser B (2014) Biochar stability in soil: decomposition during eight years and transformation as assessed by compound-specific 14C analysis. Soil Biol Biochem 70:229–236

    Article  CAS  Google Scholar 

  • Lehmann J (2007) Bio-energy in the black. Front Ecol Environ 5(7):381–387

    Article  Google Scholar 

  • Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota—a review. Soil Biol Biochem 43(9):1812–1836

    Article  CAS  Google Scholar 

  • Li Y, Hu S, Chen J, Müller K, Li Y, Fu W, Lin Z, Wang H (2017) Effects of biochar application in forest ecosystems on soil properties and greenhouse gas emissions: a review. J Soils Sediments 18(2):546–563

    Article  Google Scholar 

  • Liang B, Lehmann J, Solomon D, Kinyangi J, Grossman J, O’Neill B, Skjemstad JO, Thies J, Luizão FJ, Petersen J, Neves EG (2006) Black carbon increases cation exchange capacity in soils. Soil Sci Soc Am J 70(5):1719–1730

    Article  CAS  Google Scholar 

  • Louca S, Parfrey LW, Doebeli MJS (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353(6305):1272–1277

    Article  CAS  PubMed  Google Scholar 

  • 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 57:513–523

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Moody PW, Yo SA, Aitken RL (1997) Soil organic carbon, permanganate fractions, and the chemical properties of acidic soils. Soil Res 35(6):1301–1308

    Article  CAS  Google Scholar 

  • Needleman SB (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48(3):443–453

    Article  CAS  PubMed  Google Scholar 

  • Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. Methods of soil analysis: part 2 chemical and microbiological properties, vol 9. ASA, Wahington, pp 539–579

    Google Scholar 

  • Nguyen TTN, Wallace HM, Xu CY, Van Zwieten L, Weng ZH, Xu Z, Che R, Tahmasbian I, Hu HW, Bai SH (2018) The effects of short term, long term and reapplication of biochar on soil bacteria. Sci Total Environ 636:142–151

    Article  CAS  PubMed  Google Scholar 

  • Nielsen S, Minchin T, Kimber S, van Zwieten L, Gilbert J, Munroe P, Joseph S, Thomas T (2014) Comparative analysis of the microbial communities in agricultural soil amended with enhanced biochars or traditional fertilisers. Agric Ecosyst Environ 191:73–82

    Article  Google Scholar 

  • Noyce GL, Basiliko N, Fulthorpe R, Sackett TE, Thomas SC (2015) Soil microbial responses over 2 years following biochar addition to a north temperate forest. Biol Fertil Soils 51(6):649–659

    Article  CAS  Google Scholar 

  • Ogawa M, Okimori Y, Takahashi F (2006) Carbon sequestration by carbonization of biomass and forestation: three case studies. Mitig Adapt Strateg Glob Change 11(2):429–444

    Article  Google Scholar 

  • Ohlson M, Dahlberg B, Økland T, Brown KJ, Halvorsen R (2009) The charcoal carbon pool in boreal forest soils. Nat Geosci 2(10):692–695

    Article  CAS  Google Scholar 

  • Palansooriya KN, Wong JTF, Hashimoto Y, Huang L, Rinklebe J, Chang SX, Bolan N, Wang H, Ok YS (2019) Response of microbial communities to biochar-amended soils: a critical review. Biochar 1(1):3–22

    Article  Google Scholar 

  • Palviainen M, Berninger F, Bruckman VJ, Köster K, de Assumpção CRM, Aaltonen H, Makita N, Mishra A, Kulmala L, Adamczyk B, Zhou X, Heinonsalo J, Köster E, Pumpanen J (2018) Effects of biochar on carbon and nitrogen fluxes in boreal forest soil. Plant Soil 425(1):71–85

    Article  CAS  Google Scholar 

  • Prayogo C, Jones JE, Baeyens J, Bending GD (2013) 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(4):695–702

    Article  Google Scholar 

  • Ralebitso-Senior TK, Orr CH (2016) Microbial ecology analysis of biochar-augmented soils: setting the scene. Biochar application. Elsevier, Amsterdam, pp 1–40

    Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512

    Article  Google Scholar 

  • Rutherford PM, McGill WB, Arocena JM, Figueiredo CT (2007) Total nitrogen. Soil Sampl Methods Anal 9:239–241

    Google Scholar 

  • Sackett TE, Basiliko N, Noyce GL, Winsborough C, Schurman J, Ikeda C, Thomas SC (2015) Soil and greenhouse gas responses to biochar additions in a temperate hardwood forest. GCB Bioenergy 7(5):1062–1074

    Article  CAS  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sohi SP, Krull E, Lopez-Capel E, Bol R (2010) A review of biochar and its use and function in soil. Adv Agron 105:47–82

    Article  CAS  Google Scholar 

  • Song Y, Li X, Xu M, Jiao W, Bian Y, Yang X, Gu C, Wang F, Jiang X (2019) Does biochar induce similar successions of microbial community structures among different soils? Bull Environ Contam Toxicol 103(4):642–650

    Article  CAS  PubMed  Google Scholar 

  • Sousa NR, Franco AR, Ramos MA, Oliveira RS, Castro PML (2015) The response of Betula pubescens to inoculation with an ectomycorrhizal fungus and a plant growth promoting bacterium is substrate-dependent. Ecol Eng 81:439–443

    Article  Google Scholar 

  • Sponseller RA, Gundale MJ, Futter M, Ring E, Nordin A, Nasholm T, Laudon H (2016) Nitrogen dynamics in managed boreal forests: recent advances and future research directions. Ambio 45(2):175–187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, Bahram M, Bechem E, Chuyong G, Kõljalg U (2010) 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol 188(1):291–301

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Van Zwieten L, Kimber S, Morris S, Chan KY, Downie A, Rust J, Joseph S, Cowie A (2009) Effects of biochar from slow pyrolysis of papermill waste on agronomic performance and soil fertility. Plant Soil 327(1):235–246

    Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Xiong Z, Kuzyakov Y (2015) Biochar stability in soil: meta-analysis of decomposition and priming effects. GCB Bioenergy 8(3):512–523

    Article  Google Scholar 

  • Xu N, Tan G, Wang H, Gai X (2016) Effect of biochar additions to soil on nitrogen leaching, microbial biomass and bacterial community structure. Eur J Soil Biol 74:1–8

    Article  Google Scholar 

  • Yao Q, Liu J, Yu Z, Li Y, Jin J, Liu X, Wang G (2017) Changes of bacterial community compositions after three years of biochar application in a black soil of northeast China. Appl Soil Ecol 113:11–21

    Article  Google Scholar 

  • Zhang L, Zhang H, Wang Z, Chen G, Wang L (2016) Dynamic changes of the dominant functioning microbial community in the compost of a 90-m3 aerobic solid state fermentor revealed by integrated meta-omics. Bioresour Technol 203:1–10

    Article  CAS  PubMed  Google Scholar 

  • Zhao P, Palviainen M, Köster K, Berninger F, Bruckman VJ, Pumpanen J (2019) Effects of biochar on fluxes and turnover of carbon in boreal forest soils. Soil Sci Soc Am J 83(1):126–136

    Article  CAS  Google Scholar 

  • Zhu X, Zhu T, Pumpanen J, Palviainen M, Zhou X, Kulmala L, Bruckman VJ, Köster E, Köster K, Aaltonen H, Makita N, Wang Y, Berninger F (2020) Short-term effects of biochar on soil CO2 efflux in boreal Scots pine forests. Ann for Sci 77(2):1–15

    Article  Google Scholar 

Download references

Acknowledgements

We thank the staff of the Hyytiälä Forestry Field Station for supporting us in the field work.

Author information

Authors and Affiliations

Authors

Contributions

JP, JH, FB and HS: conceptualization. YG, XlL and HS: methodology and writing—original draft preparation. HS, XZ, YG and XlL: software, formal analysis, and data curation. JP, KK, FB, JH, MP and HS: writing—review and editing. JP, KK, MP and HS: funding acquisition. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Hui Sun.

Ethics declarations

Conflict of interest

We declare that there are no conflict of interest related to this work.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Project funding: This study was funded by The Foundation for Research of Natural Resources in Finland (2016085). The study was also supported by the Academy of Finland (286685, 294600, 307222, 277623) and the FCoE of atmospheric sciences (Center of Excellence (1118615)).

The online version is available at http://www.springerlink.com.

Corresponding editor: Yu Lei.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 123 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ge, Y., Li, Xl., Palviainen, M. et al. Response of soil bacterial community to biochar application in a boreal pine forest. J. For. Res. 34, 749–759 (2023). https://doi.org/10.1007/s11676-022-01509-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11676-022-01509-x

Keywords

Navigation