Soil Matrix Determines the Outcome of Interaction Between Mycorrhizal Symbiosis and Biochar for Andropogon gerardii Growth and Nutrition

. 2018 ; 9 () : 2862. [epub] 20181127

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid30538687

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.

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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. J. Plant Nutr. Soil Sci. 177 671–680. 10.1002/jpln.201400109 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. Eur. J. Soil Sci. 64 379–390. 10.1111/ejss.12064 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. Plant Soil 337 1–18. 10.1007/s11104-010-0464-5 DOI

Biederman L. A., Harpole W. S. (2013). Biochar and its effects on plant productivity and nutrient cycling: a meta-analysis. Glob. Chang. Biol. Bioenergy 5 202–214. 10.1111/gcbb.12037 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. Soil Use Manag. 28 177–184. 10.1111/j.1475-2743.2012.00407.x 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. Sci. Total Environ. 627 963–974. 10.1016/j.scitotenv.2018.01.283 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? Mycorrhiza 28 269–283. 10.1007/s00572-018-0825-0 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. Front. Microbiol. 7:711. 10.3389/fmicb.2016.00711 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. Geoderma 237 105–116. 10.1016/j.geoderma.2014.08.010 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. FEMS Microbiol. Ecol. 94:fiy033. 10.1093/femsec/fiy033 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 CO2. Science 337 1084–1087. 10.1126/science.1224304 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. J. Environ. Manage. 198 70–74. 10.1016/j.jenvman.2017.04.057 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. Plant Soil 251 105–114. 10.1023/A:1022932414788 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. Glob. Chang. Biol. Bioenergy 9 990–1004. 10.1111/gcbb.12363 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. Isotopes Environ. Health Stud. 34 61–77.

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). Geochim. Cosmochim. Acta 82 39–51. 10.1016/j.gca.2010.11.029 DOI

Gryndler M., Černá L., Bukovská P., Hršelová H., Jansa J. (2014). Tuber aestivum association with non-host roots. Mycorrhiza 24 603–610. 10.1007/s00572-014-0580-9 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. Mycorrhiza 28 435–450. 10.1007/s00572-018-0844-x 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. Sci. Rep. 7:45947. 10.1038/srep45947 PubMed DOI PMC

Gul S., Whalen J. K. (2016). Biochemical cycling of nitrogen and phosphorus in biochar-amended soils. Soil Biol. Biochem. 103 1–15. 10.1016/j.soilbio.2016.08.001 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. Water 10:182 10.3390/w10020182 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. Soil Biol. Biochem. 77 252–260. 10.1016/j.soilbio.2014.06.012 DOI

Hammer E. C., Forstreuter M., Rillig M. C., Kohler J. (2015). Biochar increases arbuscular mycorrhizal plant growth enhancement and ameliorates salinity stress. Appl. Soil Ecol. 96 114–121. 10.1016/j.apsoil.2015.07.014 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. ISME J. 7 498–508. 10.1038/ismej.2012.127 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. FEMS Microbiol. Ecol. 80 236–247. 10.1111/j.1574-6941.2011.01292.x PubMed DOI

Hodge A., Campbell C. D., Fitter A. H. (2001). An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413 297–299. 10.1038/35095041 PubMed DOI

Hodge A., Fitter A. H. (2010). Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc. Natl. Acad. Sci. U.S.A. 107 13754–13759. 10.1073/pnas.1005874107 PubMed DOI PMC

Hodge A., Storer K. (2015). Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil 386 1–19. 10.1007/s11104-014-2162-1 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. Mol. Ecol. 23 2118–2135. 10.1111/mec.12706 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. Mycorrhiza 12 225–234. 10.1007/s00572-002-0163-z 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. Ecol. Appl. 13 1164–1176. 10.1007/s12275-015-5108-2 PubMed DOI

Jansa J., Wiemken A., Frossard E. (2006). “The effects of agricultural practices on arbuscular mycorrhizal fungi,” in Function of Soils for Human Societies and the Environment, eds Frossard E., Blum W. E. H., Warkentin B. P. (London: Geological Society; ), 89–115.

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. Environ. Res. Lett. 12:053001 10.1088/1748-9326/aa67bd 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. Agric. Ecosyst. Environ. 144 175–187. 10.1016/j.agee.2011.08.015 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. Proc. Natl. Acad. Sci. U.S.A. 107 2093–2098. 10.1073/pnas.0906710107 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. New Phytol. 205 1473–1484. 10.1111/nph.13172 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. J. Environ. Qual. 41 990–1000. 10.2134/jeq2011.0070 PubMed DOI

Koide R. T. (2017). “Biochar-arbuscular mycorrhiza interaction in temperate soils,” in Mycorrhizal Mediation of Soil: Fertility, Structure, and Carbon Storage, eds Johnson N. C., Gehring C., Jansa J. (Amsterdam: Elsevier; ), 461–477. 10.1016/b978-0-12-804312-7.00025-5 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). Mycorrhiza 28 577–586. 10.1007/s00572-018-0854-8 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. Plant Soil 419 319–333. 10.1007/s11104-017-3350-6 DOI

Koske R. E., Gemma J. N. (1989). A modified procedure for staining roots to detect VA mycorrhizas. Mycol. Res. 92 486–505. 10.1016/S0953-7562(89)80195-9 DOI

Lehmann J., Rillig M. C., Thies J., Masiello C. A., Hockaday W. C., Crowley D. (2011). Biochar effects on soil biota - a review. Soil Biol. Biochem. 43 1812–1836. 10.1016/j.soilbio.2011.04.022 PubMed 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. J. Agron. Crop Sci. 203 131–145. 10.1111/jac.12185 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. Chemosphere 194 495–503. 10.1016/j.chemosphere.2017.12.025 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. Appl. Soil Ecol. 117 10–15. 10.1016/j.apsoil.2017.04.024 DOI

Mäder P., Vierheilig H., Streitwolf-Engel R., Boller T., Frey B., Christie P., et al. (2000). Transport of 15N from a soil compartment separated by a polytetrafluoroethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi. New Phytol. 146 155–161. 10.1046/j.1469-8137.2000.00615.x 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. Pedobiologia 57 123–130. 10.1016/j.pedobi.2013.12.005 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. Environ. Sci. Technol. 46 9571–9576. 10.1021/es301107c PubMed DOI

Martin S. L., Mooney S. J., Dickinson M. J., West H. M. (2012). The effects of simultaneous root colonisation by three Glomus species on soil pore characteristics. Soil Biol. Biochem. 49 167–173. 10.1016/j.soilbio.2012.02.036 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. New Phytol. 115 495–501. 10.1111/j.1469-8137.1990.tb00476.x 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. Mycorrhiza 26 565–574. 10.1007/s00572-016-0693-4 PubMed DOI

Newsham K. K., Fitter A. H., Watkinson A. R. (1995). Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol. Evol. 10 407–411. 10.1016/S0169-5347(00)89157-0 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. Environ. Microbiol. 15 1870–1881. 10.1111/1462-2920.12081 PubMed DOI

Ohno T., Zibilske L. M. (1991). Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci. Soc. Am. J. 55 892–895. 10.2136/sssaj1991.03615995005500030046x PubMed 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. Restor. Ecol. 26 63–72. 10.1111/rec.12528 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. PLoS One 9:e86388. 10.1371/journal.pone.0086388 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 Andropogon gerardii under limited nitrogen supply. Ecol. Evol. 6 4332–4346. 10.1002/ece3.2207 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. Chemosphere 206 51–58. 10.1016/j.chemosphere.2018.04.125 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. Pedobiologia 59 179–187. 10.1016/j.pedobi.2016.04.002 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 C3-Panicum bisulcatum and C4-Panicum maximum under different temperature regimes. Front. Plant Sci. 9:449. 10.3389/fpls.2018.00449 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. Environ. Sci. Technol. 44 827–833. 10.1021/es902266r 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. J. Plant Nutr. Soil Sci. 175 410–422. 10.1002/jpln.201100143 DOI

Shen Q., Hedley M., Arbestain M. C., Kirschbaum M. U. F. (2016). Can biochar increase the bioavailability of phosphorus? J. Soil Sci. Plant Nutr. 16 268–286. 10.4067/S0718-95162016005000022 DOI

Slavíková R., Püschel D., Janoušková M., Hujslová M., Konvalinková T., Gryndlerová H., et al. (2017). Monitoring CO2 emissions to gain a dynamic view of carbon allocation to arbuscular mycorrhizal fungi. Mycorrhiza 27 35–51. 10.1007/s00572-016-0731-2 PubMed DOI

Smith S. E., Smith F. A. (2012). Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104 1–13. 10.3852/11-229 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. New Phytol. 162 511–524. 10.1111/j.1469-8137.2004.01039.x 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. Biol. Fertil. Soils 50 321–332. 10.1007/s00374-013-0857-8 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. J. Environ. Qual. 41 973–989. 10.2134/jeq2011.0069 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. Chemosphere 85 869–882. 10.1016/j.chemosphere.2011.06.108 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. Environ. Pollut. 214 142–148. 10.1016/j.envpol.2016.04.017 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. Mol. Ecol. Res. 12 219–232. 10.1111/j.1755-0998.2011.03086.x PubMed DOI

Thonar C., Frossard E., Šmilauer P., Jansa J. (2014). Competition and facilitation in synthetic communities of arbuscular mycorrhizal fungi. Mol. Ecol. 23 733–746. 10.1111/mec.12625 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. Ecol. Lett. 11 296–310. 10.1111/j.1461-0248.2007.01139.x 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. J. Environ. Qual. 46 889–896. 10.2134/jeq2017.02.0043 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. Sci. Total Environ. 643 926–935. 10.1016/j.scitotenv.2018.06.231 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. Environ. Pollut. 227 98–115. 10.1016/j.envpol.2017.04.032 PubMed DOI

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