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Decomposition of substrates with recalcitrance gradient, primed CO2, and its relations with soil microbial diversity in post-fire forest soils

  • Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
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A Correction to this article was published on 27 July 2021

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Abstract

Purpose

Fire-induced changes in soil properties exert influence on soil processes, e.g., soil organic carbon (SOC) mineralization. The mineralization of organic substrates and soil priming effects in post-fire soils and the mechanisms involved remain elusive. This study aimed to investigate substrate mineralization with chemical recalcitrance gradient (sucrose, maize flour, and maize straw) and induced priming effects on forest soils after the fire.

Methods

Fire-burned forest soils (unburned as control) after 8 years were collected, and the physicochemical and biotic properties using high-throughput Illumina sequencing) were analyzed. Incubation of 42 days was conducted to investigate substrate decomposition and soil priming effects using the natural abundance 13C technique.

Results

The bacterial community in soil after the fire event had high diversity and was dominated by the phyla of Actinobacteria, Proteobacteria, and Acidobacteria. The addition of substrate to the burned soil had larger mineralization and caused higher soil priming effects than the control soil. Positive priming of SOC by substrate was most likely attributed to “co-metabolism,” indicated by the positive correlation between soil priming and sucrose mineralization.

Conclusion

The intensity of substrate mineralization and soil priming effects in the burned soil depended on fire shifting microbial community and substrate quality itself.

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References

  • Aoyama M, Angers D, N’’dayegamiye A, Bissonnette N (2000) Metabolism of 13C-labeled glucose in aggregates from soils with manure application. Soil Biol Biochem 32:295–300

    Article  CAS  Google Scholar 

  • Bååth E, Frostegård Å, Pennanen T, Fritze H (1995) Microbial community structure and pH response in relation to soil organic matter quality in wood-ash fertilized, clear-cut or burned coniferous forest soils. Soil Biol Biochem 27:229–240

    Article  Google Scholar 

  • Bárcenas-Moreno G, García-Orenes F, Mataix-Solera J, Mataix-Beneyto J, Bååth E (2011) Soil microbial recolonisation after a fire in a Mediterranean forest. Biol Fert Soils 47:261–272

    Article  Google Scholar 

  • Bell JM, Smith JL, Bailey VL, Bolton H (2003) Priming effect and C storage in semi-arid no-till spring crop rotations. Biol Fert Soils 37:237–244

    Article  CAS  Google Scholar 

  • Bird MI, Wynn JG, Saiz G, Wurster CM, McBeath A (2015) The pyrogenic carbon cycle. Annual Rev Earth Planetary Sci 43:273–298

    Article  CAS  Google Scholar 

  • Blagodatskaya E, Blagodatsky SA, Anderson T-H, Kuzyakov Y (2007) Priming effects in chernozem induced by glucose and N in relation to microbial growth strategies. Applied Soil Ecol 37:95–105

    Article  Google Scholar 

  • Brewer CA, Chuang VJ, Masiello CA, Gonnermann H, Gao X, Dugan B, Driver LE, Panzacchi P, Zygourakis K, Davies CA (2014) New approaches to measuring biochar density and porosity. Biomass Bioenergy 66:176–185

    Article  CAS  Google Scholar 

  • Chen D, Wang Y, Lan Z, Li J, Xing W, Hu S, Bai Y (2015) Biotic community shifts explain the contrasting responses of microbial and root respiration to experimental soil acidification. Soil Biol Biochem 90:139–147

    Article  CAS  Google Scholar 

  • Chen L, Jiang Y, Liang C, Luo Y, Xu Q, Han C, Zhao Q, Sun B (2019) Competitive interaction with keystone taxa induced negative priming under biochar amendments. Microbiome 7:1–18

    Google Scholar 

  • Cheng W (2009) Rhizosphere priming effect: its functional relationships with microbial turnover, evapotranspiration, and C-N budgets. Soil Biol Biochem 41:1795–1801

    Article  CAS  Google Scholar 

  • Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Global Change Biol 19:988–995

    Article  Google Scholar 

  • Coyne MS (1999) Soil microbiology: an exploratory approach. Delmar Publishers, Albany, NY, p 462

    Google Scholar 

  • Docherty KM, Balser TC, Bohannan BJM, Gutknecht JLM (2012) Soil microbial responses to fire and interacting global change factors in a California annual grassland. Biogeochemistry 109(1–3):63–83

    Article  CAS  Google Scholar 

  • Fan F, Yin C, Tang Y, Li Z, Song A, Wakelin SA, Zou J, Liang Y (2014) Probing potential microbial coupling of carbon and nitrogen cycling during decomposition of maize residue by 13C-DNA-SIP. Soil Bioland Biochem 70:12–21

    Article  CAS  Google Scholar 

  • Fang Y, Singh B, Singh B, Krull E (2014) Biochar carbon stability in four contrasting soils. European J Soil Sci 65:60–71

    Article  CAS  Google Scholar 

  • 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 465:288–297

    Article  CAS  Google Scholar 

  • Fontaine S, Barot S, Barré P, Bdioui N, Mary B, Rumpel C (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280

    Article  CAS  Google Scholar 

  • Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA, Treseder KK, Wallenstein MD, Brodie EL (2011) Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front Microbiol 2(94):94

    Google Scholar 

  • Graaff MAD, Classen AT, Castro HF, Schadt CW (2010) Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol 188:1055–1064

    Article  CAS  Google Scholar 

  • Guenet B, Danger M, Abbadie L, Lacroix G (2010) Priming effect: bridging the gap between terrestrial and aquatic ecology. Ecol 91:2850–2861

    Article  Google Scholar 

  • Güsewell S, Gessner MO (2009) N : P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct Ecol 23:211–219

    Article  Google Scholar 

  • Herath H, Camps-Arbestain M, Hedley M (2013) Effect of biochar on soil physical properties in two contrasting soils: an Alfisol and an Andisol. Geoderma 209:188–197

    Article  CAS  Google Scholar 

  • Hernandez-Soriano MC, Kerré B, Goos P, Hardy B, Dufey J, Smolders E (2016) Long-term effect of biochar on the stabilization of recent carbon: soils with historical inputs of charcoal. GCB Bioenergy 8:371–381

    Article  CAS  Google Scholar 

  • Hu L, Cao L, Zhang R (2014) Bacterial and fungal taxon changes in soil microbial community composition induced by short-term biochar amendment in red oxidized loam soil. World J Microbiol Biotechnol 30:1085–1092

    Article  CAS  Google Scholar 

  • Jagadamma S, Mayes MA, Steinweg JM, Schaeffer SM (2014) Substrate quality alters the microbial mineralization of added substrate and soil organic carbon. Biogeosciences 11:665–4678

    Article  CAS  Google Scholar 

  • Jien S-H, Wang C-S (2013) Effects of biochar on soil properties and erosion potential in a highly weathered soil. CATENA 110:225–233

    Article  CAS  Google Scholar 

  • Khodadad CL, 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 43:385–392

    Article  CAS  Google Scholar 

  • Kim JS, Sparovek G, Longo RM, De Melo WJ, Crowley D (2007) Bacterial diversity of terra preta and pristine forest soil from the Western Amazon. Soil Biol Biochem 39:684–690

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Schneckenberger K (2004) Review of estimation of plant rhizodeposition and their contribution to soil organic matter formation. Arch Agron Soil Sci 50:115–132

    Article  Google Scholar 

  • 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 41:210–219

    Article  CAS  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 43:1812–1836

    Article  CAS  Google Scholar 

  • Lei Z, Li Q, Song X, Wang W, Zhang Z, Peng C, Tian L (2018) Biochar mitigates dissolved organic carbon loss but does not affect dissolved organic nitrogen leaching loss caused by nitrogen deposition in Moso bamboo plantations. Global Ecol Conserv 16:e00494

  • Liu Z, Dugan B, Masiello CA, Gonnermann HM (2017) Biochar particle size, shape, and porosity act together to influence soil water properties. PLOS One 12(6):e0179079

  • Luo X, Wang L, Liu G, Wang X, Wang Z, Zheng H (2016) Effects of biochar on carbon mineralization of coastal wetland soils in the Yellow River Delta, China. Ecol Eng 94:329–336

    Article  Google Scholar 

  • Luo Y, Durenkamp M, De Nobili M, Lin Q, Brookes P (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

    Article  CAS  Google Scholar 

  • Luo Y, Durenkamp M, De Nobili M, Lin Q, Devonshire B, Brookes P (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 

  • Luo Y, Zang H, Yu Z, Chen Z, Gunina A, Kuzyakov Y, Xu J, Zhang K, Brookes PC (2017) Priming effects in biochar enriched soils using a three-source-partitioning approach: 14C labelling and 13C natural abundance. Soil Biol Biochem 106:28–35

    Article  CAS  Google Scholar 

  • Maestrini B, Nannipieri P, Abiven S (2015) A meta-analysis on pyrogenic organic matter induced priming effect. GCB Bioenergy 7:577–590

    Article  CAS  Google Scholar 

  • Mikutta R, Kleber M, Torn MS, Jahn R (2006) Stabilization of soil organic matter: association with minerals or chemical recalcitrance? Biogeochemistry 77:25–56

    Article  CAS  Google Scholar 

  • Mukherjee A, Zimmerman A, Hamdan R, Cooper W (2014) Physicochemical changes in pyrogenic organic matter (biochar) after 15 months of field aging. Solid Earth 5:693–704

    Article  Google Scholar 

  • Naisse C, Girardin C, Lefevre R, Pozzi A, Maas R, Stark A, Rumpel C (2015) Effect of physical weathering on the carbon sequestration potential of biochars and hydrochars in soil. GCB Bioenergy 7:488–496

    Article  CAS  Google Scholar 

  • Neff J, Reynolds R, Belnap J, Lamothe P (2005) Multi-decadal impacts of grazing on soil physical and biogeochemical properties in southeast Utah. Ecol Appl 15:87–95

    Article  Google Scholar 

  • Nottingham AT, Whitaker J, Turner BL, Salinas N, Zimmermann M, Malhi Y, Meir P (2015) Climate warming and soil carbon in tropical forests: insights from an elevation gradient in the Peruvian Andes. Bioscience 65:906–921

    Article  Google Scholar 

  • Noyce GL, Winsborough C, Fulthorpe R, Basiliko N (2016) The microbiomes and metagenomes of forest biochars. Rep 6(1):26425

    CAS  Google Scholar 

  • O’’neill B, Grossman J, Tsai MT, Gomes JE, Lehmann J, Peterson J, Neves E, Thies JE (2009) Bacterial community composition in Brazilian Anthrosols and adjacent soils characterized using culturing and molecular identification. Microbial Ecol 58:23–35

    Article  CAS  Google Scholar 

  • Pausch J, Kuzyakov Y (2018) Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale. Global Change Biol 24:1–12

    Article  Google Scholar 

  • Pauvert C, Buée M, Laval V, Edel-Hermann V, Fauchery L, Gautier A, Lesur I, Vallance J, Vacher C (2019) Bioinformatics matters: the accuracy of plant and soil fungal community data is highly dependent on the metabarcoding pipeline. Fungal Ecol 41:23–33

    Article  Google Scholar 

  • Pereira eSMC, Semenov AV, Schmitt H, van Elsas JD, Salles JF (2013) Microbe-mediated processes as indicators to establish the normal operating range of soil functioning. Soil Biol Biochem 57:995–1002

    Article  CAS  Google Scholar 

  • Pérez-Valera E, Verdú M, Navarro-Cano J, Goberna M (2020) Soil microbiome drives the recovery of ecosystem functions after fire. Soil Biol Biochem 149:107948

  • Pluchon N, Vincent AG, Gundale MJ, Nilsson MC, Kardol P, Wardle DA (2016) The impact of charcoal and soil mixtures on decomposition and soil microbial communities in boreal forest. Applied Soil Ecol 99:40–50

    Article  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590-D 596

  • Quin PR, Cowie AL, Flavel RJ, Keen BP, Macdonald LM, Morris SG, Singh BP, Young IM, Van Zwieten L (2014) Oil mallee biochar improves soil structural properties—a study with x-ray micro-CT. Agric Ecosyst Environ 191:142–149

    Article  CAS  Google Scholar 

  • Randerson JT, Chen Y, van der Werf GR, Rogers BM, Morton DC (2012) Global burned area and biomass burning emissions from small fires. J Geophys Res-Biogeo 117:G04012

    Article  CAS  Google Scholar 

  • 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 4:1340–1351

    Article  Google Scholar 

  • Rumpel C, Leifeld J, Santin C, Doerr S (2015) Movement of biochar in the environment. Biochar for environmental management. Sci Technol Implementat 283–300

  • Santín C, Doerr SH, Preston CM, González-Rodríguez G (2015) Pyrogenic organic matter production from wildfires: a missing sink in the global carbon cycle. Glob Chang Biol 21:1621–1633

    Article  Google Scholar 

  • Santos F, Torn MS, Bird JA (2012) Biological degradation of pyrogenic organic matter in temperate forest soils. Soil Biol Biochem 51:115–124

    Article  CAS  Google Scholar 

  • Singh BP, Cowie AL (2014) Long-term influence of biochar on native organic carbon mineralisation in a low-carbon clayey soil. Sci Rep 4:3687

    Article  CAS  Google Scholar 

  • Sun DL, Jiang X, Wu QL, Zhou NY (2013) Intragenomic heterogeneity of 16S rRNA genes causes overestimation of prokaryotic diversitY. Appl Environ Microb 79:5962–5969

    Article  CAS  Google Scholar 

  • Tamura M, Tharayil N (2014) Plant litter chemistry and microbial priming regulate the accrual, composition and stability of soil carbon in invaded ecosystems. New Phytol 203:110–124

    Article  CAS  Google Scholar 

  • Tarkalson DD, Kachman SD, Knops JMN, Thies JE, Wortmann CS (2008) Decomposition of Bt and non-Bt corn hybrid residues in the field. Nutr Cyc Agroecosys 80:211–222

    Article  CAS  Google Scholar 

  • Thies JE, Rillig MC (2009) Characteristics of biochar: biological properties. Biochar for Environmental Management: Sci Technol 1:85–105

    Google Scholar 

  • Tinsley J, Taylor T, Moore J (1951) The determination of carbon dioxide derived from carbonates in agricultural and biological materials. Analyst 76:300–310

    Article  CAS  Google Scholar 

  • Van der Werf GR, Randerson JT, Giglio L, Collatz GJ, Mu M, Kasibhatla PS, DeFries MDC, RS. Jin Y, van Leeuwen TT (2010) Global fire emissions and the contribution of deforestation, savanna. forest, agricultural. and peat fires (1997–2009). Atmos Chem Phye 10:11707–11735

    Article  CAS  Google Scholar 

  • Ventura M, Alberti G, Viger M, Jenkins JR, Girardin C, Baronti S, Zaldei A, Taylor G, Rumpel C, Miglietta F (2015) Biochar mineralization and priming effect on SOM decomposition in two European short rotation coppices. GCB Bioenergy 7:1150–1160

    Article  CAS  Google Scholar 

  • Wang J, Xiong Z, Kuzyakov Y (2016) Biochar stability in soil: meta-analysis of decomposition and priming effects. GCB Bioenergy 8:512–523

    Article  CAS  Google Scholar 

  • Wang X, Butterly CR, Baldock JA, Tang C (2017) Long-term stabilization of crop residues and soil organic carbon affected by residue quality and initial soil pH. Sci the Total Environ 587:502–509

    Article  CAS  Google Scholar 

  • Wang XS (2010) Black carbon in urban topsoils of Xuzhou (China): environmental implication and magnetic proxy. Environ Monit Assess 163:41–47

    Article  CAS  Google Scholar 

  • Watzinger A, Feichtmair S, Kitzler B, Zehetner F, Kloss S, Wimmer B, Zechmeister-Boltenstern S, Soja G (2014) 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 65:40–51

    Article  CAS  Google Scholar 

  • Weng ZH, Van Zwieten L, Singh BP, Tavakkoli E, Joseph S, Macdonald LM, Rose TJ, Rose MT, Kimber SW, Morris S (2017) Biochar built soil carbon over a decade by stabilizing rhizodeposits. Nat Clim Chang 7:371–376

    Article  CAS  Google Scholar 

  • Wetterstedt JÅM, Persson T, ÅGren GI, (2010) Temperature sensitivity and substrate quality in soil organic matter decomposition: results of an incubation study with three substrates. Global Change Biol 16:1806–1819

    Article  Google Scholar 

  • Whitman T, Pepe-Ranney C, Enders A, Koechli C, Campbell A, Buckley DH, Lehmann J (2016) Dynamics of microbial community composition and soil organic carbon mineralization in soil following addition of pyrogenic and fresh organic matter. ISME J 10:2918–2930

    Article  CAS  Google Scholar 

  • Wu JJRG, 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(8):1167-1169

  • Yu Z, Chen L, Pan S, Li Y, Kuzyakov Y, Xu J, Brookes P, Luo Y (2018) Feedstock determines biochar-induced soil priming effects by stimulating the activity of specific microorganisms. Eur J Soil Sci 69:521–534

    Article  CAS  Google Scholar 

  • Zhang K, Chen L, Li Y, Brookes PC, Xu J, Luo Y (2020) Interactive effects of soil pH and substrate quality on microbial utilization. Eur J Soil Biol 96: 103151

  • Zheng H, Wang X, Luo X, Wang Z, Xing B (2018) Biochar-induced negative carbon mineralization priming effects in a coastal wetland soil: roles of soil aggregation and microbial modulation. Sci Total Environ 610:951–960

    Article  CAS  Google Scholar 

  • Zimmerman AR, Gao B, Ahn MY (2011) Positive and negative carbon mineralization priming effects among a variety of biochar-amended soils. Soil Biol Biochem 43:169–1179

    Article  CAS  Google Scholar 

  • Zimmerman AR, Ouyang L (2019) Priming of pyrogenic C (biochar) mineralization by dissolved organic matter and vice versa. Soil Biol Biochem 130:105–112

    Article  CAS  Google Scholar 

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Funding

This study was supported by the National Natural Science Foundation of China (41761134095, 41671233).

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Authors and Affiliations

  1. Institute of Soil and Water Resources and Environmental Science, Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Zhejiang University, Hangzhou, 310058, China

    Jie Zhang, Lu Ling, Yu Luo, Peduruhewa H. Jeewani & Jianming Xu

  2. School of Environmental and Rural Science, University of New England, Armidale, NSW, 2351, Australia

    Bhupinder Pal Singh

  3. NSW Department of Primary Industries, Elizabeth Macarthur Agricultural Institute, Menangle, NSW, 2568, Australia

    Bhupinder Pal Singh

  4. Department of Agriculture, Southern Province, Labuduwa, Galle, 80000, Sri Lanka

    Peduruhewa H. Jeewani

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  1. Jie Zhang
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  2. Lu Ling
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  4. Yu Luo
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  5. Peduruhewa H. Jeewani
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Correspondence to Peduruhewa H. Jeewani.

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The original online version of this article was revised: In the original version of this article, the name of the 5th and 6th authors were incorrectly captured and should be changed to Peduruhewa H. Jeewani and Jianming Xu.

The original online version of this article was revised: In the original version of this article, the name of the 5th and 6th authors were incorrectly captured and should be changed to Peduruhewa H. Jeewani and Jianming Xu. 

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11368_2021_3003_MOESM1_ESM.docx

Supplementary file1 Fig. S1 Cumulative Total CO2 (a), cumulative Substate derived CO2 (b) and Cumulative Primed soil CO2 (c) with the addition of three substrates during 42 days of incubation. B: burned soil, UB: unburned soil; S1: sucrose, S2: maize powder; S3: maize straw (DOCX 387 KB)

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Zhang, J., Ling, L., Singh, B.P. et al. Decomposition of substrates with recalcitrance gradient, primed CO2, and its relations with soil microbial diversity in post-fire forest soils. J Soils Sediments 21, 3007–3017 (2021). https://doi.org/10.1007/s11368-021-03003-z

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