in

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

  • 1.

    Redecker D, Kodner R, Graham LE. Glomalean fungi from the Ordovician. Science. 2000;289:1920–1.

    CAS 
    PubMed 

    Google Scholar 

  • 2.

    Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol. 2008;6:763–75.

    CAS 
    PubMed 

    Google Scholar 

  • 3.

    Raven JA, Lambers H, Smith SE, Westoby M. Costs of acquiring phosphorus by vascular land plants: patterns and implications for plant coexistence. N Phytol. 2018;217:1420–7.

    CAS 

    Google Scholar 

  • 4.

    Field KJ, Pressel S. Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi. N Phytol. 2018;220:996–1011.

    CAS 

    Google Scholar 

  • 5.

    Harrison MJ, Vanbuuren ML. A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature. 1995;378:626–9.

    CAS 
    PubMed 

    Google Scholar 

  • 6.

    Smith SE, Jakobsen I, Gronlund M, Smith FA. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 2011;156:1050–7.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 7.

    Zhang L, Feng G, Declerck S. Signal beyond nutrient, fructose, exuded by an arbuscular mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium. ISME J. 2018;12:23–51.

    Google Scholar 

  • 8.

    Zhang L, Xu MG, Liu Y, Zhang FS, Hodge A, Feng G. Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. N Phytol. 2016;210:1022–32.

    CAS 

    Google Scholar 

  • 9.

    Koide RT, Kabir Z. Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. N Phytol. 2000;148:511–7.

    CAS 

    Google Scholar 

  • 10.

    Jiang FY, Zhang L, Zhou JC, George TS, Feng G. Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. N Phytol. 2021;230:304–15.

    CAS 

    Google Scholar 

  • 11.

    Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, et al. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci USA. 2013;110:20117–22.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 12.

    Miyauchi S, Kiss E, Kuo A, Drula E, Kohler A, Sanchez-Garcia M, et al. Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. Nat Commun. 2020;11:5125.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 13.

    Johansen A, Jakobsen I, Jensen ES. Hyphal transport by a vesicular-arbuscular mycorrhizal fungus of N applied to the soil as ammonium or nitrate. Biol Fert Soils. 1993;16:66–70.

    CAS 

    Google Scholar 

  • 14.

    Wipf D, Krajinski F, van Tuinen D, Recorbet G, Courty PE. Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks. N Phytol. 2019;223:1127–42.

    CAS 

    Google Scholar 

  • 15.

    Johansen A, Jensen ES. Transfer of N and P from intact or decomposing roots of pea to barley interconnected by an arbuscular mycorrhizal fungus. Soil Biol Biochem. 1996;28:73–81.

    CAS 

    Google Scholar 

  • 16.

    Hodge A, Campbell CD, Fitter AH. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature. 2001;413:297–9.

    CAS 
    PubMed 

    Google Scholar 

  • 17.

    Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH. Competition between roots and soil micro-organisms for nutrients from nitrogen-rich patches of varying complexity. J Ecol. 2000;88:150–64.

    Google Scholar 

  • 18.

    Bukovská P, Bonkowski M, Konvalinková T, Beskid O, Hujslová M, Püschel D, et al. Utilization of organic nitrogen by arbuscular mycorrhizal fungi–is there a specific role for protists and ammonia oxidizers? Mycorrhiza. 2018;28:465.

    PubMed 

    Google Scholar 

  • 19.

    Püschel D, Janoušková M, Hujslová M, Slavíková R, Gryndlerová H, Jansa J. Plant-fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply. Ecol Evol. 2016;6:4332–46.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 20.

    Bukovská P, Rozmoš M, Kotianová M, Gančarčíková K, Dudáš M, Hršelová H, et al. Arbuscular mycorrhiza mediates efficient recycling from soil to plants of nitrogen bound in chitin. Front Microbiol. 2021;12:574060.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 21.

    Bunn RA, Simpson DT, Bullington LS, Lekberg Y, Janos DP. Revisiting the ‘direct mineral cycling’ hypothesis: arbuscular mycorrhizal fungi colonize leaf litter, but why? ISME J. 2019;13:1891–8.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 22.

    Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK. An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ Microbiol. 2013;15:1870–81.

    CAS 
    PubMed 

    Google Scholar 

  • 23.

    Herman DJ, Firestone MK, Nuccio E, Hodge A. Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition. FEMS Microbiol Ecol. 2012;80:236–47.

    CAS 
    PubMed 

    Google Scholar 

  • 24.

    Emmett BD, Lévesque-Tremblay V, Harrison MJ. Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi. ISME J. 2021;e-pub ahead of print 1 March 2021; https://doi.org/10.1038/s41396-021-00920-2.

  • 25.

    Trap J, Bonkowski M, Plassard C, Villenave C, Blanchart E. Ecological importance of soil bacterivores for ecosystem functions. Plant Soil. 2016;398:1–24.

    CAS 

    Google Scholar 

  • 26.

    Jansa J, Hodge A. Swimming, gliding, or hyphal riding? On microbial migration along the arbuscular mycorrhizal hyphal highway and functional consequences thereof. N Phytol. 2021;230:14–6.

    Google Scholar 

  • 27.

    Morin E, Miyauchi S, San Clemente H, Chen ECH, Pelin A, de la Providencia I, et al. Comparative genomics of Rhizophagus irregularis, R. cerebriforme, R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina. N Phytol. 2019;222:1584–98.

    CAS 

    Google Scholar 

  • 28.

    Gil-Cardeza ML, Calonne-Salmon M, Gomez E, Declerck S. Short-term chromium (VI) exposure increases phosphorus uptake by the extraradical mycelium of the arbuscular mycorrhizal fungus Rhizophagus irregularis MUCL 41833. Chemosphere. 2017;187:27–34.

    CAS 
    PubMed 

    Google Scholar 

  • 29.

    Voets L, Dupre de Boulois H, Renard L, Strullu DG, Declerck S. Development of an autotrophic culture system for the in vitro mycorrhization of potato plantlets. FEMS Microbiol Lett. 2005;248:111–8.

    CAS 
    PubMed 

    Google Scholar 

  • 30.

    Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science. 2011;333:880–2.

    CAS 
    PubMed 

    Google Scholar 

  • 31.

    van’t Padje A, Galvez LO, Klein M, Hink MA, Postma M, Shimizu T, et al. Temporal tracking of quantum-dot apatite across in vitro mycorrhizal networks shows how host demand can influence fungal nutrient transfer strategies. ISME J. 2021;15:435–49.

    PubMed 

    Google Scholar 

  • 32.

    Gryndler M, Šmilauer P, Püschel D, Bukovská P, Hršelová H, Hujslová M, et al. Appropriate nonmycorrhizal controls in arbuscular mycorrhiza research: a microbiome perspective. Mycorrhiza. 2018;28:435–50.

    PubMed 

    Google Scholar 

  • 33.

    Jansa J, Šmilauer P, Borovička J, Hršelová H, Forczek ST, Slámová K, et al. Dead Rhizophagus irregularis biomass mysteriously stimulates plant growth. Mycorrhiza. 2020;30:63–77.

    PubMed 

    Google Scholar 

  • 34.

    Bukovská P, Püschel D, Hršelová H, Jansa J, Gryndler M. Can inoculation with living soil standardize microbial communities in soilless potting substrates? Appl Soil Ecol. 2016;108:278–87.

    Google Scholar 

  • 35.

    Cranenbrouck S, Voets L, Bivort C, Renard L, Strullu DG, Declerck S. Methodologies for in vitro cultivation of arbuscular mycorrhizal fungi with root organs. In: Declerck S, Strullu DG, Fortin JA, (eds.). In vitro culture of mycorrhizas. Berlin: Springer; 2005. p. 341–75. pp

    Google Scholar 

  • 36.

    Ohno T, Zibilske LM. Determination of low concentrations of phosphorus is soil extracts using malachite green. Soil Sci Soc Am J. 1991;55:892–5.

    CAS 

    Google Scholar 

  • 37.

    Püschel D, Janoušková M, Voříšková A, Gryndlerová H, Vosátka M, Jansa J. Arbuscular mycorrhiza stimulates biological nitrogen fixation in two Medicago spp. through improved phosphorus acquisition. Front Plant Sci. 2017;8:390.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 38.

    Phillips DL, Gregg JW. Uncertainty in source partitioning using stable isotopes. Oecologia 2001;127:171–9.

    PubMed 

    Google Scholar 

  • 39.

    Perez-Tienda J, Valderas A, Camanes G, Garcia-Agustin P, Ferrol N. Kinetics of NH4+ uptake by the arbuscular mycorrhizal fungus Rhizophagus irregularis. Mycorrhiza. 2012;22:485–91.

    CAS 
    PubMed 

    Google Scholar 

  • 40.

    He XX, Chen YQ, Liu SJ, Gunina A, Wang XL, Chen W, et al. Cooperation of earthworm and arbuscular mycorrhizae enhanced plant N uptake by balancing absorption and supply of ammonia. Soil Biol Biochem. 2018;116:351–9.

    CAS 

    Google Scholar 

  • 41.

    Hestrin R, Weber PK, Pett-Ridge J, Lehmann J. Plants and mycorrhizal symbionts acquire substantial soil nitrogen from gaseous ammonia transport. New Phytol. 2021;e-pub ahead of print 2 June 2021; https://doi.org/10.1111/nph.17527

  • 42.

    Everett DH, Wynne-Jones WFK. The dissociation of the ammonium ion and the basic strength of ammonia in water. P R Soc Lond A Mat. 1938;169:190–204.

    CAS 

    Google Scholar 

  • 43.

    Bidondo LF, Colombo R, Bompadre J, Benavides M, Scorza V, Silvani V, et al. Cultivable bacteria associated with infective propagules of arbuscular mycorrhizal fungi. Implications for mycorrhizal activity. Appl Soil Ecol. 2016;105:86–90.

    Google Scholar 

  • 44.

    Cruz AF, Ishii T. Arbuscular mycorrhizal fungal spores host bacteria that affect nutrient biodynamics and biocontrol of soil-borne plant pathogens. Biol Open. 2012;1:52–7.

    PubMed 

    Google Scholar 

  • 45.

    Scheublin TR, Sanders IR, Keel C, van der Meer JR. Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. ISME J. 2010;4:752–63.

    PubMed 

    Google Scholar 

  • 46.

    Toljander JF, Artursson V, Paul LR, Jansson JK, Finlay RD. Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiol Lett. 2006;254:34–40.

    CAS 
    PubMed 

    Google Scholar 

  • 47.

    Jaderlund L, Arthurson V, Granhall U, Jansson JK. Specific interactions between arbuscular mycorrhizal fungi and plant growth-promoting bacteria: as revealed by different combinations. FEMS Microbiol Lett. 2008;287:174–80.

    PubMed 

    Google Scholar 

  • 48.

    Larsen J, Jaramillo-Lopez P, Najera-Rincon M, Gonzalez-Esquivel CE. Biotic interactions in the rhizosphere in relation to plant and soil nutrient dynamics. J Soil Sci Plant Nut. 2015;15:449–63.

    Google Scholar 

  • 49.

    Mansfeld-Giese K, Larsen J, Bodker L. Bacterial populations associated with mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. FEMS Microbiol Ecol. 2002;41:133–40.

    CAS 
    PubMed 

    Google Scholar 

  • 50.

    Hildebrandt U, Janetta K, Bothe H. Towards growth of arbuscular mycorrhizal fungi independent of a plant host. Appl Environ Microbiol. 2002;68:1919–24.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 51.

    Cruz AF, Horii S, Ochiai S, Yasuda A, Ishii T. Isolation and analysis of bacteria associated with spores of Gigaspora margarita. J Appl Microbiol. 2008;104:1711–7.

    CAS 
    PubMed 

    Google Scholar 

  • 52.

    Luthfiana N, Inamura N, Tantriani, Sato T, Saito K, Oikawa A, et al. Metabolite profiling of the hyphal exudates of Rhizophagus clarus and Rhizophagus irregularis under phosphorus deficiency. Mycorrhiza. 2021;31:403–12.

    CAS 
    PubMed 

    Google Scholar 

  • 53.

    Oliverio AM, Geisen S, Delgado-Baquerizo M, Maestre FT, Turner BL, Fierer N. The global-scale distributions of soil protists and their contributions to belowground systems. Sci Adv. 2020;6:eaax8787.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 54.

    Averill C, Turner BL, Finzi AC. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature. 2014;505:543–5.

    CAS 
    PubMed 

    Google Scholar 

  • 55.

    Mäder P, Fliessbach A, Dubois D, Gunst L, Fried P, Niggli U. Soil fertility and biodiversity in organic farming. Science 2002;296:1694–7.

    PubMed 

    Google Scholar 

  • 56.

    Cavagnaro TR. Biologically regulated nutrient supply systems: compost and arbuscular mycorrhizas—a review. Adv Agron. 2015;129:293–321.

    Google Scholar 


  • Source: Ecology - nature.com

    Genome-wide analysis reveals associations between climate and regional patterns of adaptive divergence and dispersal in American pikas

    Crossing disciplines, adding fresh eyes to nuclear engineering