Biochar has been heralded as a multipurpose soil amendment to sustainably increase soil fertility and crop yields, affect soil hydraulic properties, reduce nutrient losses, and sequester carbon. Some of the most spectacular results of biochar (and organic nutrient) inputs are the terra preta soils in the Amazon, dark anthropogenic soils with extremely high fertility sustained over centuries. Such soil improvements have been particularly difficult to achieve on a short run, leading to speculations that biochar may need to age (weather) in soil to show its best. Further, interaction of biochar with arbuscular mycorrhizal fungi (AMF), important root symbionts of a great majority of terrestrial plants including most agricultural crops, remains little explored. To study the effect of aged biochar on highly mycotrophic Andropogon gerardii plants and their associated AMF, we made use of softwood biochar, collected from a historic charcoal burning site. This biochar (either untreated or chemically activated, the latter serving as a proxy for freshly prepared biochar) was added into two agricultural soils (acid or alkaline), and compared to soils without biochar. These treatments were further crossed with inoculation with a synthetic AMF community to address possible interactions between biochar and the AMF. Biochar application was generally detrimental for growth and mineral nutrition of our experimental plants, but had no effect on the extent of their root colonized by the AMF, nor did it affect composition of their root-borne AMF communities. In contrast, biochar affected development of two out of five AMF (Claroideoglomus and Funneliformis) in the soil. Establishment of symbiosis with AMF largely mitigated biochar-induced suppression of plant growth and mineral nutrition, mainly by improving plant acquisition of phosphorus. Both mycorrhizal and non-mycorrhizal plants grew well in the acid soil without biochar application, whereas non-mycorrhizal plants remained stunted in the alkaline soils under all situations (with or without biochar). These different and strong effects indicate that response of plants to biochar application are largely dependent on soil matrix and also on microbes such as AMF, and call for further research to enable qualified predictions of the effects of different biochar applications on field-grown crops and soil processes.

Department of Soil Science Faculty of Agriculture Shahid Bahonar University of Kerman Kerman Iran

Faculty of Science Jan Evangelista Purkyně University in Ústí nad Labem Ústí nad Labem Czechia

Institute of Botany Czech Academy of Sciences Průhonice Czechia

Institute of Geology Czech Academy of Sciences Prague Czechia

Laboratory of Fungal Biology Institute of Microbiology Czech Academy of Sciences Prague Czechia

Laboratory of Molecular Structure Characterization Institute of Microbiology Czech Academy of Sciences Prague Czechia

Zobrazit více v PubMed

Alling V., Hale S. E., Martinsen V., Mulder J., Smebye A., Breedveld G. D., et al. (2014). The role of biochar in retaining nutrients in amended tropical soils. DOI

Ameloot N., Graber E. R., Verheijen F. G. A., De Neve S. (2013). Interactions between biochar stability and soil organisms: review and research needs. DOI

Atkinson C. J., Fitzgerald J. D., Hipps N. A. (2010). Potential mechanisms for achieving agricultural benefits from biochar application to temperate soils: a review. DOI

Biederman L. A., Harpole W. S. (2013). Biochar and its effects on plant productivity and nutrient cycling: a meta-analysis. DOI

Borchard N., Wolf A., Laabs V., Aeckersberg R., Scherer H. W., Moeller A., et al. (2012). Physical activation of biochar and its meaning for soil fertility and nutrient leaching - a greenhouse experiment. DOI

Borno M. L., Muller-Stover D. S., Liu F. L. (2018). Contrasting effects of biochar on phosphorus dynamics and bioavailability in different soil types. PubMed DOI

Bukovská P., Bonkowski M., Konvalinková T., Beskid O., Hujslová M., Püschel D., et al. (2018). Utilization of organic nitrogen by arbuscular mycorrhizal fungi-is there a specific role for protists and ammonia oxidizers? PubMed DOI

Bukovská P., Gryndler M., Gryndlerová H., Püschel D., Jansa J. (2016). Organic nitrogen-driven stimulation of arbuscular mycorrhizal fungal hyphae correlates with abundance of ammonia oxidizers. PubMed DOI PMC

Butnan S., Deenik J. L., Toomsan B., Antal M. J., Vityakon P. (2015). Biochar characteristics and application rates affecting corn growth and properties of soils contrasting in texture and mineralogy. DOI

Camenzind T., Hammer E. C., Lehmann J., Solomon D., Horn S., Rillig M. C., et al. (2018). Arbuscular mycorrhizal fungal and soil microbial communities in African Dark Earths. PubMed DOI

Cheng L., Booker F. L., Tu C., Burkey K. O., Zhou L. S., Shew H. D., et al. (2012). Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO PubMed DOI

Dai L. C., Tan F. R., Li H., Zhu N. M., He M. X., Zhu Q. L., et al. (2017). Calcium-rich biochar from the pyrolysis of crab shell for phosphorus removal. PubMed DOI

Drew E. A., Murray R. S., Smith S. E., Jakobsen I. (2003). Beyond the rhizosphere: growth and function of arbuscular mycorrhizal external hyphae in sands of varying pore sizes. DOI

Dutta T., Kwon E., Bhattacharya S. S., Jeon B. H., Deep A., Uchimiya M., et al. (2017). Polycyclic aromatic hydrocarbons and volatile organic compounds in biochar and biochar-amended soil: a review. DOI

Frossard E., Sinaj S. (1998). The isotope exchange kinetic technique: a method to describe the availability of inorganic nutrients. Applications to K, P, S and Zn.

Glaser B., Birk J. J. (2012). State of the scientific knowledge on properties and genesis of anthropogenic dark earths in central Amazonia (terra preta de Indio). DOI

Gryndler M., Černá L., Bukovská P., Hršelová H., Jansa J. (2014). PubMed DOI

Gryndler M., Šmilauer P., Püschel D., Bukovská P., Hršelová H., Hujslová M., et al. (2018). Appropriate nonmycorrhizal controls in arbuscular mycorrhiza research: a microbiome perspective. PubMed DOI

Gui H., Hyde K., Xu J. C., Mortimer P. (2017). Arbuscular mycorrhiza enhance the rate of litter decomposition while inhibiting soil microbial community development. PubMed DOI PMC

Gul S., Whalen J. K. (2016). Biochemical cycling of nitrogen and phosphorus in biochar-amended soils. DOI

Hagemann N., Spokas K., Schmidt H. P., Kägi R., Böhler M. A., Bucheli T. D. (2018). Activated carbon, biochar and charcoal: linkages and synergies across pyrogenic carbon’s ABCs. DOI

Hammer E. C., Balogh-Brunstad Z., Jakobsen I., Olsson P. A., Stipp S. L. S., Rillig M. C. (2014). A mycorrhizal fungus grows on biochar and captures phosphorus from its surfaces. DOI

Hammer E. C., Forstreuter M., Rillig M. C., Kohler J. (2015). Biochar increases arbuscular mycorrhizal plant growth enhancement and ameliorates salinity stress. DOI

Hazard C., Gosling P., Van Der Gast C. J., Mitchell D. T., Doohan F. M., Bending G. D. (2013). The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. PubMed DOI PMC

Herman D. J., Firestone M. K., Nuccio E., Hodge A. (2012). Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition. PubMed DOI

Hodge A., Campbell C. D., Fitter A. H. (2001). An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. PubMed DOI

Hodge A., Fitter A. H. (2010). Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. PubMed DOI PMC

Hodge A., Storer K. (2015). Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. DOI

Jansa J., Erb A., Oberholzer H. R., Smilauer P., Egli S. (2014). Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. PubMed DOI

Jansa J., Mozafar A., Anken T., Ruh R., Sanders I. R., Frossard E. (2002). Diversity and structure of AMF communities as affected by tillage in a temperate soil. PubMed DOI

Jansa J., Mozafar A., Kuhn G., Anken T., Ruh R., Sanders I. R., et al. (2003). Soil tillage affects the community structure of mycorrhizal fungi in maize roots. PubMed DOI

Jansa J., Wiemken A., Frossard E. (2006). “The effects of agricultural practices on arbuscular mycorrhizal fungi,” in

Jeffery S., Abalos D., Prodana M., Bastos A. C., Van Groenigen J. W., Hungate B. A., et al. (2017). Biochar boosts tropical but not temperate crop yields. DOI

Jeffery S., Verheijen F. G. A., Van Der Velde M., Bastos A. C. (2011). A quantitative review of the effects of biochar application to soils on crop productivity using meta-analysis. DOI

Johnson N. C., Wilson G. W. T., Bowker M. A., Wilson J. A., Miller R. M. (2010). Resource limitation is a driver of local adaptation in mycorrhizal symbioses. PubMed DOI PMC

Johnson N. C., Wilson G. W. T., Wilson J. A., Miller R. M., Bowker M. A. (2015). Mycorrhizal phenotypes and the law of the minimum. PubMed DOI

Kloss S., Zehetner F., Dellantonio A., Hamid R., Ottner F., Liedtke V., et al. (2012). Characterization of slow pyrolysis biochars: effects of feedstocks and pyrolysis temperature on biochar properties. PubMed DOI

Koide R. T. (2017). “Biochar-arbuscular mycorrhiza interaction in temperate soils,” in DOI

Koide R. T., Fernandez C. W. (2018). The continuing relevance of “older” mycorrhiza literature: insights from the work of John Laker Harley (1911-1990). PubMed DOI

Konvalinková T., Püschel D., Řezáčová V., Gryndlerová H., Jansa J. (2017). Carbon flow from plant to arbuscular mycorrhizal fungi is reduced under phosphorus fertilization. DOI

Koske R. E., Gemma J. N. (1989). A modified procedure for staining roots to detect VA mycorrhizas. DOI

Lehmann J., Rillig M. C., Thies J., Masiello C. A., Hockaday W. C., Crowley D. (2011). Biochar effects on soil biota - a review. DOI

Liu C., Liu F., Ravnskov S., Rubaek G. H., Sun Z., Andersen M. N. (2017). Impact of wood biochar and its interactions with mycorrhizal fungi, phosphorus fertilization and irrigation strategies on potato growth. DOI

Liu L., Li J. W., Yue F. X., Yan X. W., Wang F. Y., Bloszies S., et al. (2018). Effects of arbuscular mycorrhizal inoculation and biochar amendment on maize growth, cadmium uptake and soil cadmium speciation in Cd-contaminated soil. PubMed DOI

Luo S. S., Wang S. J., Tian L., Li S. Q., Li X. J., Shen Y. F., et al. (2017). Long-term biochar application influences soil microbial community and its potential roles in semiarid farmland. DOI

Mäder P., Vierheilig H., Streitwolf-Engel R., Boller T., Frey B., Christie P., et al. (2000). Transport of DOI

Mahmood T., Mehnaz S., Fleischmann F., Ali R., Hashmi Z. H., Iqbal Z. (2014). Soil sterilization effects on root growth and formation of rhizosheaths in wheat seedlings. DOI

Mao J. D., Johnson R. L., Lehmann J., Olk D. C., Neves E. G., Thompson M. L., et al. (2012). Abundant and stable char residues in soils: implications for soil fertility and carbon sequestration. PubMed DOI

Martin S. L., Mooney S. J., Dickinson M. J., West H. M. (2012). The effects of simultaneous root colonisation by three DOI

McGonigle T. P., Miller M. H., Evans D. G., Fairchild G. L., Swan J. A. (1990). A new method which gives an objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. PubMed DOI

Mickan B. S., Abbott L. K., Stefanova K., Solaiman Z. M. (2016). Interactions between biochar and mycorrhizal fungi in a water-stressed agricultural soil. PubMed DOI

Newsham K. K., Fitter A. H., Watkinson A. R. (1995). Multi-functionality and biodiversity in arbuscular mycorrhizas. PubMed DOI

Nuccio E. E., Hodge A., Pett-Ridge J., Herman D. J., Weber P. K., Firestone M. K. (2013). An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. PubMed DOI

Ohno T., Zibilske L. M. (1991). Determination of low concentrations of phosphorus in soil extracts using malachite green. DOI

Ohsowski B. M., Dunfield K., Klironomos J. N., Hart M. M. (2018). Plant response to biochar, compost, and mycorrhizal fungal amendments in post-mine sandpits. DOI

Prommer J., Wanek W., Hofhansl F., Trojan D., Offre P., Urich T., et al. (2014). Biochar delerates soil organic nitrogen cycling but stimulates soil nitrification in a temperate arable field trial. PubMed DOI PMC

Püschel D., Janoušková M., Hujslová M., Slavíková R., Gryndlerová H., Jansa J. (2016). Plant-fungus competition for nitrogen erases mycorrhizal growth benefits of PubMed DOI PMC

Ren X. H., Wang F., Zhang P., Guo J. K., Sun H. W. (2018). Aging effect of minerals on biochar properties and sorption capacities for atrazine and phenanthrene. PubMed DOI

Řezáčová V., Gryndler M., Bukovská P., Šmilauer P., Jansa J. (2016). Molecular community analysis of arbuscular mycorrhizal fungi - Contributions of PCR primer and host plant selectivity to the detected community profiles. DOI

Řezáčová V., Zemková L., Beskid O., Püschel D., Konvalinková T., Hujslová M., et al. (2018). Little cross-feeding of the mycorrhizal networks shared between C PubMed DOI PMC

Roberts K. G., Gloy B. A., Joseph S., Scott N. R., Lehmann J. (2010). Life cycle assessment of biochar systems: estimating the energetic, economic, and climate change potential. PubMed DOI

Schulz H., Glaser B. (2012). Effects of biochar compared to organic and inorganic fertilizers on soil quality and plant growth in a greenhouse experiment. DOI

Shen Q., Hedley M., Arbestain M. C., Kirschbaum M. U. F. (2016). Can biochar increase the bioavailability of phosphorus? DOI

Slavíková R., Püschel D., Janoušková M., Hujslová M., Konvalinková T., Gryndlerová H., et al. (2017). Monitoring CO PubMed DOI

Smith S. E., Smith F. A. (2012). Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. PubMed DOI

Smith S. E., Smith F. A., Jakobsen I. (2004). Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. DOI

Song Y. J., Zhang X. L., Ma B., Chang S. X., Gong J. (2014). Biochar addition affected the dynamics of ammonia oxidizers and nitrification in microcosms of a coastal alkaline soil. DOI

Spokas K. A., Cantrell K. B., Novak J. M., Archer D. W., Ippolito J. A., Collins H. P., et al. (2012). Biochar: a synthesis of its agronomic impact beyond carbon sequestration. PubMed DOI

Spokas K. A., Novak J. M., Stewart C. E., Cantrell K. B., Uchimiya M., Dusaire M. G., et al. (2011). Qualitative analysis of volatile organic compounds on biochar. PubMed DOI

Sun B. B., Lian F., Bao Q. L., Liu Z. Q., Song Z. G., Zhu L. Y. (2016). Impact of low molecular weight organic acids (LMWOAs) on biochar micropores and sorption properties for sulfamethoxazole. PubMed DOI

Thonar C., Erb A., Jansa J. (2012). Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communitiesumarker design, verification, calibration and field validation. PubMed DOI

Thonar C., Frossard E., Šmilauer P., Jansa J. (2014). Competition and facilitation in synthetic communities of arbuscular mycorrhizal fungi. PubMed DOI

van der Heijden M. G. A., Bardgett R. D., Van Straalen N. M. (2008). The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. PubMed DOI

Zhang H., Voroney R. P., Price G. W. (2017). Effects of temperature and activation on biochar chemical properties and their impact on ammonium, nitrate, and phosphate sorption. PubMed DOI

Zhang L. Y., Jing Y. M., Xiang Y. Z., Zhang R. D., Lu H. B. (2018). Responses of soil microbial community structure changes and activities to biochar addition: a meta-analysis. PubMed DOI

Zhu X. M., Chen B. L., Zhu L. Z., Xing B. S. (2017). Effects and mechanisms of biochar-microbe interactions in soil improvement and pollution remediation: a review. PubMed DOI

Arbuscular Mycorrhiza Mediates Efficient Recycling From Soil to Plants of Nitrogen Bound in Chitin