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.
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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
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
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
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
Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth
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
Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515(7528):505–511
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
Cajander AK (1949) Forest types and their significance. Acta for Fenn 56:71
Chao A (1984) Non-parametric estimation of the classes in a population. Scand J Stat 11(4):265–270
Clough TJ, Condron LM (2010) Biochar and the nitrogen cycle: introduction. J Environ Qual 39(4):1218–2122
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
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
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
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88(6):1354–1364
Hart S, Luckai N, Brando P (2013) Charcoal function and management in boreal ecosystems. J Appl Ecol 50(5):1197–1206
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
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
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
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
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
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
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
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
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
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
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
Lehmann J (2007) Bio-energy in the black. Front Ecol Environ 5(7):381–387
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
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
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
Louca S, Parfrey LW, Doebeli MJS (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353(6305):1272–1277
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
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
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
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
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
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
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
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
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
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
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
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
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
Ralebitso-Senior TK, Orr CH (2016) Microbial ecology analysis of biochar-augmented soils: setting the scene. Biochar application. Elsevier, Amsterdam, pp 1–40
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
Rutherford PM, McGill WB, Arocena JM, Figueiredo CT (2007) Total nitrogen. Soil Sampl Methods Anal 9:239–241
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
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
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
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
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
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
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
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
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
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
Wang J, Xiong Z, Kuzyakov Y (2015) Biochar stability in soil: meta-analysis of decomposition and priming effects. GCB Bioenergy 8(3):512–523
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
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
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
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
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
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We thank the staff of the Hyytiälä Forestry Field Station for supporting us in the field work.
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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.
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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)).
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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
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DOI: https://doi.org/10.1007/s11676-022-01509-x