Abstract
Background and Aims
Biochar amendment to soil is a promising practice of enhancing productivity of agricultural systems. The positive effects on crop are often attributed to a promotion of beneficial soil microorganisms while suppressing pathogens e.g. This study aims to determine the influence of biochar feedstock on (i) spontaneous and fungi inoculated microbial colonisation of biochar particles and (ii) physical pore space characteristics of native and fungi colonised biochar particles which impact microbial habitat quality.
Methods
Pyrolytic biochars from mixed woods and Miscanthus were investigated towards spontaneous colonisation by classical microbiological isolation, phylogenetic identification of bacterial and fungal strains, and microbial respiration analysis. Physical pore space characteristics of biochar particles were determined by X-ray μ-CT. Subsequent 3D image analysis included porosity, surface area, connectivities, and pore size distribution.
Results
Microorganisms isolated from Wood biochar were more abundant and proliferated faster than those from the Miscanthus biochar. All isolated bacteria belonged to gram-positive bacteria and were feedstock specific. Respiration analysis revealed higher microbial activity for Wood biochar after water and substrate amendment while basal respiration was on the same low level for both biochars. Differences in porosity and physical surface area were detected only in interaction with biochar-specific colonisation. Miscanthus biochar was shown to have higher connectivity values in surface, volume and transmission than Wood biochars as well as larger pores as observed by pore size distribution. Differences in physical properties between colonised and non-colonised particles were larger in Miscanthus biochar than in Wood biochar.
Conclusions
Vigorous colonisation was found on Wood biochar compared to Miscanthus biochar. This is contrasted by our findings from physical pore space analysis which suggests better habitat quality in Miscanthus biochar than in Wood biochar. We conclude that (i) the selected feedstocks display large differences in microbial habitat quality as well as physical pore space characteristics and (ii) physical description of biochars alone does not suffice for the reliable prediction of microbial habitat quality and recommend that physical and surface chemical data should be linked for this purpose.
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References
Abiven S, Menasseri S, Angers DA, Leterme P (2007) Dynamics of aggregate stability and biological binding agents during decomposition of organic materials. Eur J Soil Sci 58(1):239–247
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Ameloot N, De Neve S, Jegajeevagan K, Yildiz G, Buchan D, Funkuin YN, Nkwain Fukuin Y, 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 57:401–410
Ascough PL, Sturrock CJ, Bird MI (2010) Investigation of growth responses in saprophytic fungi to charred biomass. Isot Environ Health Stud 46:64–77
Baveye PC (2014) The biochar dilemma. Soil Sci Soc Am J 52(3):217
Baveye PC, Laba M, Otten W, Bouckaert L, Dello Sterpaio P, Goswami RR, Grinev D, Houston A, Hu Y, Liu J, Mooney S, Pajor R, Sleutel S, Tarquis A, Wang W, Wei Q, Sezgin M. (2010) Observer-dependent variability of the thresholding step in the quantitative analysis of soil images and X-ray microtomography data. Geoderma 157:51–63
Bird MI, Ascough PL, Young IM, Wood CV, Scott AC (2008) X-ray microtomographic imaging of charcoal. J Archaeol Sci 35(10):2698–2706
Bucheli TD, Bachmann HJ, Blum F, Bürge D, Giger R, Hilber I, Keita J, Leifeld J, Schmidt HP (2014) On the heterogeneity of biochar and consequences for its representative sampling. J Anal Appl Pyrolysis 107:25–30
Budai A, Wang L, Gronli M, Strand LT, Antal MJ, Abiven S, Dieguez-Alonso A, Anca-Couce A, Rasse DP (2014) Surface properties and chemical composition of corncob and Miscanthus biochars: effects of production temperature and method. J Agric Food Chem 62:3791–3799
Cayuela ML, Sánchez-Monedero MA, Roig A, Hanley K, Enders A, Lehmann J (2013) biochar and denitrification in soils: when, how much and why does biochar reduce N2O emissions? Sci Rep 3:1732
Demirbas A (2004) Effects of temperature and particle size on bio-char yield from pyrolysis of agricultural residues. J Anal Appl Pyrolysis 72(2):243–248
Doube M, Klosowksi MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, Jackson JS, Schmid B, Hutchinsin JR, Shefelbine SJ (2010) BoneJ: free and extensible bone image analysis in ImageJ. Bone 47(6):1076–1079
Dougherty R, Kunzelmann KH (2007) Computing local thickness of 3D structures with image J. Microsc Microanal 13(S02):1678–1679
EBC (2012) Guidelines for a sustainable production of biochar (No. 4.8). Arbaz, Switzerland. Retrieved from http://www.european-biochar.org/en/download
Ennis CJ, Evans AG, Islam M, Ralebitso-Senior TK, Senior E (2012) Biochar: carbon sequestration, land remediation, and impacts on soil microbiology. Crit Rev Environ Sci Technol 42(22):2311–2364
Gani SA, Mukherjee DC, Chattoraj DK (1999) Adsorption of biopolymer at solid-liquid interfaces. 1. Affinities of DNA to hydrophobic and hydrophilic solid surfaces. Langmuir 15:7130–7138
Gomez JD, Denef K, Stewart CE, Zheng J, Cotrufo MF (2014) Biochar addition rate influences soil microbial abundance and activity in temperate soils. Eur J Soil Sci 65:28–39
Gray M, Johnson MG, Dragila MI, Kleber M (2014) Water uptake in biochars: the roles of porosity and hydrophobicity. Biomass Bioenergy 61:196–205
Gul S, Whalen JK, Thomas BW, Sachdeva V, Deng H (2015) Physico-chemical properties and microbial responses in biochar-amended soils: mechanisms and future directions. Agric Ecosyst Environ 206:46–59
Hapca S, Houston A, Otten W, Baveye P (2013) New local segmentation method for 3D images of natural porous media, based on minimizing the intraclass grayscale variance. Vandose Zone J 12(3):12. doi:10.2136/vzj2012.0172
Hardie M, Clothier B, Bound S, Oliver G, Close D (2014) Does biochar influence soil physical properties and soil water availability? Plant Soil 376:347–361
Hattori T (1988) Soil aggregates as microhabitats of microorganisms. Rep Inst Agric Tohoku Univ 37:23–36
Hildebrand T, Rüegsegger P (1997) A new method for the model-independent assessment of thickness in three-dimensional images. J Miscroscopy 185:67–75
Hoshino YT, Morimoto S (2008) Comparison of 18S rDNA primers for estimating fungal diversity in agricultural soils using polymerase chain reaction-denaturing gradient gel electrophoresis. Soil Sci Plant Nutr 54(5):701–710
Houston AN, Otten W, Baveye PC, Hapca S (2013a) Adaptive-window indicator kriging. A thresholding method for computed tomography images of porous media. Comput Geosci 54:239–248
Houston AN, Schmidt S, Tarquis AM, Otten W, Baveye PC, Hapca SM (2013b) Effect of scanning and image reconstruction settings in X-ray computed microtomography on quality and segmentation of 3D soil images. Geoderma 207-208:154–165
Jaafar NM, Clode PL, Abbott LK (2014) Microscopy observations of habitable space in biochar for colonization by fungal hyphae from soil. J Integr Agric 13(3):483–490
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(8):1723–1731
Kim P, Johnson AM, Essington ME, Radosevich M, Kwon WT, Lee SH, Rials TG, Labbé N (2012) Effect of pH on surface characteristics of switchgrass-derived biochars produced by fast pyrolysis. Chemosphere 90(10):2623–2630
Kinney TJ, Masiello CA, Dugan B, Hockaday WC, Dean MR, Zygourakis K, Barnes RT (2012) Hydrologic properties of biochars produced at different temperatures. Biomass Bioenergy 41:34–43
Koide RT, Petprakob K, Peoples M (2011) Quantitative analysis of biochar in field soil. Soil Biol Biochem 43(7):1563–1568
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
Leite DCA, Balieiro FC, Pires CA, Madari BE, Rosado AS, Coutinho HLC, Peixoto RS (2014) Comparison of DNA extraction protocols for microbial communities from soil treated with biochar. Braz J Microbiol 45:175–183
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(11):2304–2314
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
Marchal G, Smith KEC, Rein A, Winding A, Trapp S, Karlson UG (2013) Comparing the desorption and biodegradation of low concentrations of phenanthrene sorbed to activated carbon, biochar and compost. Chemosphere 90(6):1767–1778
Morales VL, Perez-Reche FJ, Hapca SM, Hanley KL, Lehmann J, Zhang W (2015) Reverse engineering of biochar. Bioresour Technol 183:163–174
Muyzer G, Teske A, Wirsen CO, Jannasch HW (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164:165–172
Naisse C, Alexis M, Plante A, Wiedner K, Glaser B, Pozzi A, Carcaillet C, Criscuoli I, Rumpel C (2013) Can biochar and hydrochar stability be assessed with chemical methods? Org Geochem 60:40–44
Nguyen BT, Lehmann J, Kinyangi J, Smernik R, Riha SJ, Engelhard MH (2008) Long-term black carbon dynamics in cultivated soil. Biogeochemistry 92(1–2):163–176
Ouyang L, Wang F, Tang J, Yu L, Zhang R (2013) Effects of biochar amendment on soil aggregates and hydraulic properties. J Soil Sci Plant Nutr 13(4):991–1002
Pattanotai T, Watanabe H, Okazaki K (2014) Gasification characteristic of large wood chars with anisotropic structure. Fuel 117:331–339
Pietikäinen J, Kiikkilä O, Fritz H (2000) Charcoal as a habitat for microbes and its effect on the microbial. Oikos 89:231–242
Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinforma 28(14):1823–1829
Quilliam RS, Marsden KA, Gertler C, Rousk J, DeLuca TH, Jones DL (2012) Nutrient dynamics, microbial growth and weed emergence in biochar amended soil are influenced by time since application and reapplication rate. Agric Ecosyst Environ 158:192–199
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 65:287–293
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
R Core Team (2013) R project. Vienna, Austria. Retrieved from http://www.r-project.org/
Riedel T, Iden S, Geilich J, Wiedner K, Durner W, Biester H (2014) Changes in the molecular composition of organic matter leached from an agricultural topsoil following addition of biomass-derived black carbon (biochar). Org Geochem 69:52–60
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682
Simões M, Cleto S, Pereira MO, Vieira MJ (2007) Influence of biofilm composition on the resistance to detachment. Water Sci Technol 55:473–480
Spoering AL, Lewis K (2001) Biofilms and planktonic cells of Pseudomonas Aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol 183:6746–6751
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729
Thormann KM, Shukla S, Pelletier DA, Spormann AM (2004) Initial phases of biofilm formation in Shewanella oneidensis MR-1. J Bacteriol 186(23):8096–8104
Weber W, Pirbazari M, Melson G (1978) Biological growth on activated carbon: an investigation by scanning electron microscopy. Environ Sci Technol 12(7):817–819
Wiedner K, Rumpel C, Steiner C, Pozzi A, Maas R, Glaser B (2013) Chemical evaluation of chars produced by thermochemical conversion (gasification, pyrolysis and hydrothermal carbonization) of agro-industrial biomass on a commercial scale. Biomass Bioenergy 59:264–278
Willey JM, Sherwood LM, Woolverton CJ (2009) Prescott’s principles of microbiology. Watnick, New York
Xie Y, Snoeyink J, Xu J (2006) Efficient algorithm for approximating maximum inscribed sphere in high dimensional polytope. Proceedings of the twenty-second annual symposium on Computational Geometry, 21–29
Yanai Y, Toyota K, Okazaki M (2007) Effects of charcoal addition on N2O emissions from soil resulting from rewetting air-dried soil in short-term laboratory experiments. Soil Sci Plant Nutr 53(2):181–188
Zhang Z, Yani S, Zhu M, Li J, Zhang D (2013) Effect of temperature and heating rate in pyrolysis on the yield, structure and oxidation reactivity of pine sawdust biochar. In: Chemeca 2013: challenging tomorrow. Conference paper 30430 (7 pp.)
Zhu ZA, Liao Z, Orechia L (2014) Using optimization to find maximum inscribed balls and minimum enclosing balls. ArXiv:1412.1001
Acknowledgments
The X-ray μ-CT analyses were carried out by LS at Abertay University, Dundee, UK as part of a short term scientific mission funded by the COST Action Biochar TD1107. Both the COST Action Biochar and the SIMBIOS Centre at Abertay University are acknowledged for funding and hosting respectively. Special Thanks is given to Sonja Schmidt and Ruth Falconer for technical assistance in μ-CT scanning and to Alasdair Houston for provision and assistance with image processing algorithms. Daniel Grimm is acknowledged for provision of fungal inoculated biochars and Ingo Dobner for kind provision of non-colonised biochars.
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Schnee, L.S., Knauth, S., Hapca, S. et al. Analysis of physical pore space characteristics of two pyrolytic biochars and potential as microhabitat. Plant Soil 408, 357–368 (2016). https://doi.org/10.1007/s11104-016-2935-9
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DOI: https://doi.org/10.1007/s11104-016-2935-9
Keywords
- Biochar
- Microbial colonisation
- Pore geometry
- Habitat quality