Symbiosis between plants and arbuscular mycorrhizal (AM) fungi, involving great majority of extant plant species including most crops, is heavily implicated in plant mineral nutrition, abiotic and biotic stress tolerance, soil aggregate stabilization, as well as shaping soil microbiomes. The latter is particularly important for efficient recycling from soil to plants of nutrients such as phosphorus and nitrogen (N) bound in organic forms. Chitin is one of the most widespread polysaccharides on Earth, and contains substantial amounts of N (>6% by weight). Chitin is present in insect exoskeletons and cell walls of many fungi, and can be degraded by many prokaryotic as well as eukaryotic microbes normally present in soil. However, the AM fungi seem not to have the ability to directly access N bound in chitin molecules, thus relying on microbes in their hyphosphere to gain access to this nutrient-rich resource in the process referred to as organic N mineralization. Here we show, using data from two pot experiments, both including root-free compartments amended with 15N-labeled chitin, that AM fungi can channel substantial proportions (more than 20%) of N supplied as chitin into their plants hosts within as short as 5 weeks. Further, we show that overall N losses (leaching and/or volatilization), sometimes exceeding 50% of the N supplied to the soil as chitin within several weeks, were significantly lower in mycorrhizal as compared to non-mycorrhizal pots. Surprisingly, the rate of chitin mineralization and its N utilization by the AM fungi was at least as fast as that of green manure (clover biomass), based on direct 15N labeling and tracing. This efficient N recycling from soil to plant, observed in mycorrhizal pots, was not strongly affected by the composition of AM fungal communities or environmental context (glasshouse or outdoors, additional mineral N supply to the plants or not). These results indicate that AM fungi in general can be regarded as a critical and robust soil resource with respect to complex soil processes such as organic N mineralization and recycling. More specific research is warranted into the exact molecular mechanisms and microbial players behind the observed patterns.

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

See more in PubMed

Adamczyk B., Kitunen V., Smolander A. (2013). Response of soil C and N transformations to condensed tannins and different organic N-condensed tannin complexes. Appl. Soil Ecol. 64 163–170. 10.1016/j.apsoil.2012.12.003 DOI

Artursson V., Finlay R. D., Jansson J. K. (2006). Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ. Microbiol. 8 1–10. 10.1111/j.1462-2920.2005.00942.x PubMed DOI

Augé R. M., Toler H. D., Saxton A. M. (2015). Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25 13–24. 10.1007/s00572-014-0585-4 PubMed DOI

Babikova Z., Gilbert L., Bruce T. J. A., Birkett M., Caulfield J. C., Woodcock C., et al. (2013). Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol. Lett. 16 835–843. 10.1111/ele.12115 PubMed DOI

Bender S. F., Conen F., van der Heijden M. G. A. (2015). Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland. Soil Biol. Biochem. 80 283–292. 10.1016/j.soilbio.2014.10.016 DOI

Bever J. D., Dickie I. A., Facelli E., Facelli J. M., Klironomos J., Moora M., et al. (2010). Rooting theories of plant community ecology in microbial interactions. Trends Ecol. Evol. 25 468–478. 10.1016/j.tree.2010.05.004 PubMed DOI PMC

Bowles T. M., Jackson L. E., Cavagnaro T. R. (2018). Mycorrhizal fungi enhance plant nutrient acquisition and modulate nitrogen loss with variable water regimes. Glob. Change Biol. 24 E171–E182. PubMed

Brundrett M. C., Tedersoo L. (2018). Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol. 220 1108–1115. 10.1111/nph.14976 PubMed DOI

Bücking H., Kafle A. (2015). Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy Basel 5 587–612. 10.3390/agronomy5040587 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

Cavagnaro T. R., Bender S. F., Asghari H. R., van der Heijden M. G. A. (2015). The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci. 20 283–290. 10.1016/j.tplants.2015.03.004 PubMed DOI

Charters M. D., Sait S. M., Field K. J. (2020). Aphid herbivory drives asymmetry in carbon for nutrient exchange between plants and an arbuscular mycorrhizal fungus. Curr. Biol. 30 1801–1808. 10.1016/j.cub.2020.02.087 PubMed DOI PMC

de Boer W., Folman L. B., Summerbell R. C., Boddy L. (2005). Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol. Rev. 29 795–811. 10.1016/j.femsre.2004.11.005 PubMed DOI

Duhamel M., Pel R., Ooms A., Bücking H., Jansa J., Ellers J., et al. (2013). Do fungivores trigger the transfer of protective metabolites from host plants to arbuscular mycorrhizal hyphae? Ecology 94 2019–2029. 10.1890/12-1943.1 PubMed DOI

Fellbaum C. R., Gachomo E. W., Beesetty Y., Choudhari S., Strahan G. D., Pfeffer P. E., et al. (2012). Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 109 2666–2671. 10.1073/pnas.1118650109 PubMed DOI PMC

Fellbaum C. R., Mensah J. A., Cloos A. J., Strahan G. E., Pfeffer P. E., Kiers E. T., et al. (2014). Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytol. 203 646–656. 10.1111/nph.12827 PubMed DOI

Fernandez C. W., Koide R. T. (2012). The role of chitin in the decomposition of ectomycorrhizal fungal litter. Ecology 93 24–28. 10.1890/11-1346.1 PubMed DOI

Field K. J., Pressel S. (2018). Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi. New Phytol. 220 996–1011. 10.1111/nph.15158 PubMed DOI

George E., Haussler K. U., Vetterlein D., Gorgus E., Marschner H. (1992). Water and nutrient translocation by hyphae of Glomus mosseae. Can. J. Bot. 70 2130–2137. 10.1139/b92-265 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

Hart M. M., Reader R. J. (2002). Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol. 153 335–344. 10.1046/j.0028-646x.2001.00312.x DOI

Hartmann A., Schmid M., Van Tuinen D., Berg G. (2009). Plant-driven selection of microbes. Plant Soil 321 235–257. 10.1007/s11104-008-9814-y DOI

Hewitt E. J. (1966). Sand and water culture methods used in the study of plant nutrition. CAB Tech. Commun. 22 431–432.

Hodge A. (2001). Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil. New Phytol. 151 725–734. 10.1046/j.0028-646x.2001.00200.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., Helgason T., Fitter A. H. (2010). Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol. 3 267–273. 10.1016/j.funeco.2010.02.002 DOI

Hodge A., Robinson D., Fitter A. H. (2000). An arbuscular mycorrhizal inoculum enhances root proliferation in, but not nitrogen capture from, nutrient-rich patches in soil. New Phytol. 145 575–584. 10.1046/j.1469-8137.2000.00602.x PubMed DOI

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., Finlay R., Wallander H., Smith F. A., Smith S. E. (2011). “Role of mycorrhizal symbioses in phosphorus cycling,” in Phosphorus in Action: Biological Processes in Soil Phosphorus Cycling, eds Bunemann E. K., Oberson A., Frossard E. (Heidelberg: Springer; ), 137–168. 10.1007/978-3-642-15271-9_6 DOI

Jansa J., Forczek S. T., Rozmoš M., Püschel D., Bukovská P., Hršelová H. (2019). Arbuscular mycorrhiza and soil organic nitrogen: network of players and interactions. Chem. Biol. Technol. Agric. 6:10. 10.1186/s40538-019-0147-2 DOI

Jansa J., Mozafar A., Frossard E. (2003). Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie 23 481–488. 10.1051/agro:2003013 DOI

Jansa J., Šmilauer P., Borovička J., Hršelová H., Forczek S. T., Slámová K., et al. (2020). Dead Rhizophagus irregularis biomass mysteriously stimulates plant growth. Mycorrhiza 30 63–77. 10.1007/s00572-020-00937-z PubMed DOI

Jansa J., Smith F. A., Smith S. E. (2008). Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol. 177 779–789. 10.1111/j.1469-8137.2007.02294.x PubMed DOI

Johansen A., Jakobsen I., Jensen E. S. (1992). Hyphal transport of 15N-labelled nitrogen by a vesicular arbuscular mycorrhizal fungus and its effect on depletion of inorganic soil N. New Phytol. 122 281–288. 10.1111/j.1469-8137.1992.tb04232.x PubMed DOI

Johansen A., Jakobsen I., Jensen E. S. (1993). Hyphal transport by a vesicular-arbuscular mycorrhizal fungus of N applied to the soil as ammonium or nitrate. Biol. Fert. Soils 16 66–70. 10.1007/bf00336518 DOI

Johnson N. C. (2010). Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol. 185 631–647. 10.1111/j.1469-8137.2009.03110.x PubMed DOI

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

Kafle A., Garcia K., Wang X. R., Pfeffer P. E., Strahan G. D., Bücking H. (2019). Nutrient demand and fungal access to resources control the carbon allocation to the symbiotic partners in tripartite interactions of Medicago truncatula. Plant Cell Environ. 42 270–284. 10.1111/pce.13359 PubMed DOI

Kennedy P. G., Izzo A. D., Bruns T. D. (2003). There is high potential for the formation of common mycorrhizal networks between understorey and canopy trees in a mixed evergreen forest. J. Ecol. 91 1071–1080. 10.1046/j.1365-2745.2003.00829.x DOI

Kohl L., van der Heijden M. G. A. (2016). Arbuscular mycorrhizal fungal species differ in their effect on nutrient leaching. Soil Biol. Biochem. 94 191–199. 10.1016/j.soilbio.2015.11.019 DOI

Parniske M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6 763–775. 10.1038/nrmicro1987 PubMed DOI

Paymaneh Z., Gryndler M., Konvalinková T., Benada O., Borovička J., Bukovská P., et al. (2018). Soil matrix determines the outcome of interaction between mycorrhizal symbiosis and biochar for Andropogon gerardii growth and nutrition. Front. Microbiol. 9:2862. 10.3389/fmicb.2018.02862 PubMed DOI PMC

Püschel D., Bitterlich M., Rydlová J., Jansa J. (2020). Facilitation of plant water uptake by an arbuscular mycorrhizal fungus: a Gordian knot of roots and hyphae. Mycorrhiza 30 299–313. 10.1007/s00572-020-00949-9 PubMed DOI

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

Püschel D., Janoušková M., Voříšková A., Gryndlerová H., Vosátka M., Jansa J. (2017). Arbuscular mycorrhiza stimulates biological nitrogen fixation in two Medicago spp. through improved phosphorus acquisition. Front Plant Sci. 8:390. 10.3389/fpls.2017.00390 PubMed DOI PMC

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

Rillig M. C. (2004). Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol. Lett. 7 740–754. 10.1111/j.1461-0248.2004.00620.x DOI

Rillig M. C., Mummey D. L. (2006). Mycorrhizas and soil structure. New Phytol. 171 41–53. 10.1111/j.1469-8137.2006.01750.x PubMed DOI

Simard S. W., Durall D. M. (2004). Mycorrhizal networks: a review of their extent, function, and importance. Can. J. Bot. 82 1140–1165. 10.1139/b04-116 DOI

Smith D. D., Sperry J. S. (2014). Coordination between water transport capacity, biomass growth, metabolic scaling and species stature in co-occurring shrub and tree species. Plant Cell Environ. 37 2679–2690. 10.1111/pce.12408 PubMed DOI

Smith S. E., Read D. J. (2008). Mycorrhizal Symbiosis, 3rd Edn. New York: Academic Press.

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

Storer K., Coggan A., Ineson P., Hodge A. (2018). Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots. New Phytol. 220 1285–1295. 10.1111/nph.14931 PubMed DOI PMC

Thirkell T., Cameron D., Hodge A. (2019). Contrasting nitrogen fertilisation rates alter mycorrhizal contribution to barley nutrition in a field trial. Front. Plant Sci. 10:1312. 10.3389/fpls.2019.01312 PubMed DOI PMC

Thonar C., Erb A., Jansa J. (2012). Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communities - marker design, verification, calibration and field validation. Mol. Ecol. Resour. 12 219–232. 10.1111/j.1755-0998.2011.03086.x PubMed DOI

Tian C. J., Kasiborski B., Koul R., Lammers P. J., Bücking H., Shachar-Hill Y. (2010). Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux. Plant Physiol. 153 1175–1187. 10.1104/pp.110.156430 PubMed DOI PMC

Veresoglou S. D., Chen B. D., Rillig M. C. (2012). Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol. Biochem. 46 53–62. 10.1016/j.soilbio.2011.11.018 DOI

Veresoglou S. D., Verbruggen E., Makarova O., Mansour I., Sen R., Rillig M. C. (2019). Arbuscular mycorrhizal fungi alter the community structure of ammonia oxidizers at high fertility via competition for soil NH4+. Microb. Ecol. 78 147–158. 10.1007/s00248-018-1281-2 PubMed DOI

Vĕtrovský T., Baldrian P. (2013). Analysis of soil fungal communities by amplicon pyrosequencing: current approaches to data analysis and the introduction of the pipeline SEED. Biol. Fert. Soils 49 1027–1037. 10.1007/s00374-013-0801-y DOI

Voříšková A., Jansa J., Püschel D., Krüger M., Cajthaml T., Vosátka M., et al. (2017). Real-time PCR quantification of arbuscular mycorrhizal fungi: does the use of nuclear or mitochondrial markers make a difference? Mycorrhiza 27 577–585. 10.1007/s00572-017-0777-9 PubMed DOI

Walder F., Niemann H., Natarajan M., Lehmann M. F., Boller T., Wiemken A. (2012). Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol. 159 789–797. 10.1104/pp.112.195727 PubMed DOI PMC

Wattenburger C. J., Gutknecht J., Zhang Q., Brutnell T., Hofmockel K., Halverson L. (2020). The rhizosphere and cropping system, but not arbuscular mycorrhizae, affect ammonia oxidizing archaea and bacteria abundances in two agricultural soils. Appl. Soil Ecol. 151:103540. 10.1016/j.apsoil.2020.103540 DOI

Unraveling the diversity of hyphal explorative traits among Rhizophagus irregularis genotypes

Diversity of Mycorrhizal Fungi in Temperate Orchid Species: Comparison of Culture-Dependent and Culture-Independent Methods

Variability in Nutrient Use by Orchid Mycorrhizal Fungi in Two Medium Types

Nutrient-dependent cross-kingdom interactions in the hyphosphere of an arbuscular mycorrhizal fungus

Mycorrhiza governs plant-plant interactions through preferential allocation of shared nutritional resources: A triple (13C, 15N and 33P) labeling study

Arbuscular Mycorrhiza and Nitrification: Disentangling Processes and Players by Using Synthetic Nitrification Inhibitors

Organic nitrogen utilisation by an arbuscular mycorrhizal fungus is mediated by specific soil bacteria and a protist