Skip to main content
SpringerLink
Log in

Proximal and distal mechanisms through which arbuscular mycorrhizal associations alter terrestrial denitrification

  • Review Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background

The vast majority of terrestrial plants, including most crops, associate with fungi of the phylum Glomeromycota to form symbiotic associations, known as arbuscular mycorrhizas. Arbuscular mycorrhizas play a pivotal role in the terrestrial cycling of nitrogen (N). Recent advances in mycorrhizal research show that arbuscular mycorrhizal fungi (AMF) can reduce denitrification rates and nitrous oxide (N2O) emissions from soils. The rapid increase in the literature, over the last five years, opens up the opportunity to address mechanisms through which AMF might control denitrification.

Scope

In this review, we classify likely mechanisms through which AMF modify through their hyphae denitrification and N2O emissions into two categories: proximal mechanisms, manifested through direct changes to denitrifiers and distal mechanisms which induce indirect changes to denitrifiers. We distinguish between two types of influences, (i) alterations in the size and activity of denitrifiers and (ii) alterations in the relative availability of two key groups of genes, nitrite reductases (nirK & nirS) and nitrous oxide reductases (nosZ).

Conclusion

Proximal mechanisms could reduce N2O emissions through depleting available soil N and C, metal ions, modifying soil moisture, immobilizing C and N or through altering the denitrifying community, and the relative abundance of genes involved in denitrification. Distal mechanisms could impact denitrification through changing soil pH, organic matter decomposition, improvement in soil aggregation, as well as promoting plant diversity and productivity. There are apparently many likely mechanisms, proximal and distal, through which AMF could alter N2O production, even though their ecological importance for N cycling remains open to question.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abalos D, de Deyn GB, Kuyper TW, van Groenigen JW (2014) Plant species identity surpasses species richness as a key driver of N2O emissions from grassland. Global Change Biol 20:265–275

    Article  Google Scholar 

  • Abalos D, de Deyn GB, van Groenigen JW (2017) What plant functional traits can reduce nitrous oxide emissions from intensively managed grasslands? Global Change Biol 24:e248–e258

    Article  Google Scholar 

  • Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid doils. Vedose Zone J 6:291–297

    Article  Google Scholar 

  • Amora-Lazcano E, Vázquez MM, Azcón R (1998) Response of nitrogen transforming microorganisms to arbuscular mycorrhizal fungi. Biol Fert Soils 27:65–70

    Article  CAS  Google Scholar 

  • Anderson TH, Heinemeyer O, Weigel HJ (2011) Changes in the fungal to-bacterial respiratory ratio and microbial biomass in agriculturally managed soils under free-air CO2 enrichment (FACE) -a six-year survey of a field study. Soil Biol Biochem 43:895–904

    Article  CAS  Google Scholar 

  • Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10

    Article  CAS  PubMed  Google Scholar 

  • Atul-Nayyar A, Hamel C, Hanson K, Germida J (2009) The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza 19:239–246

    Article  CAS  PubMed  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381

    Article  Google Scholar 

  • Augé RM, Saxton AM, Toler HD (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

    Article  PubMed  Google Scholar 

  • Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–545

    Article  CAS  PubMed  Google Scholar 

  • Bach EM, Williams RJ, Hargreavesa SK, Yanga F, Hofmockela KS (2018) Greatest soil microbial diversity found in micro-habitats. Soil Biol Biochem 118:217–226

    Article  CAS  Google Scholar 

  • Bago B, Azcón-Aguilar C (1997) Changes in the rhizospheric pH induced by arbuscular mycorrhiza formation in onion (Allium cepa L.). Zeitschrift für Pflanzenernährung und Bodenkunde 160:333–339

    Article  CAS  Google Scholar 

  • Bago B, Vierheilig H, Piché Y, Azcón-Aguilar C (1996) Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown in monoxenic culture. New Phytol 133:273–280

    Article  CAS  PubMed  Google Scholar 

  • Balaine N, Clough TJ, Beare MH, Thomas SM, Meenken ED (2016) Soil Gas Diffusivity Controls N2O and N2 Emissions and their Ratio. Soil Sci Soc Am J 80:529–540

    Article  CAS  Google Scholar 

  • Ball BC (2013) Soil structure and greenhouse gas emissions: a synthesis of 20 years of experimentation. Eur J Soil Sci 64:357–373

    Article  CAS  Google Scholar 

  • Barton L, Wolf B, Rowlings D, Scheer C, Kiese R, Grace P, Stefanova K, Butterbach-Bahl K (2015) Sampling frequency affects estimates of annual nitrous oxide fluxes. Sci Rep 5:15912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bender SF, Plantenga F, Neftel A, Jocher M, Oberholzer HR, Kohl L, Giles M, Daniell TJ, Van der Heijden MGA (2014) Symbiotic relationships between soil Fungi and plants reduce N2O emissions from soil. ISME J 8:1336–1345

    Article  CAS  PubMed  Google Scholar 

  • Bender SF, Conen F, Van der Heijden MGA (2015) Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland. Soil Biol Biochem 80:283–292

    Article  CAS  Google Scholar 

  • Bengtsson G, Fronæus S, Bengtsson-Kloo L (2002) The kinetics and mechanism of oxidation of hydroxylamine by iron(iii). J Chem Soc Dalton Trans 1:2548–2552

    Article  Google Scholar 

  • Bowles TM, Jackson LE, Loeher M, Cavagnaro TR (2016) Ecological intensification and arbuscular mycorrhizas: a meta-analysis of tillage and cover crop effects. J Appl Ecol 17:1785–1793

    Google Scholar 

  • Bremer C, Braker G, Matthies D, Reuter A, Engels C, Conrad R (2007) Impact of plant functional group, plant species and sampling time on the composition of nirK-type denitrifier communities in soil. App Environ Microbiol 73:6876–6884

    Article  CAS  Google Scholar 

  • Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115

    Article  PubMed  Google Scholar 

  • Burgin AJ, Groffman PM (2012) Soil O2 controls denitrification rates and N2O yield in a riparian wetland. J Geophys Res 117:G01010

    Google Scholar 

  • Butterbach-Bahl K, Dannenmann M (2011) Denitrification and associated soil N2O emissions due to agricultural activities in a changing climate. Curr Opin Environ Sustain 3:389–395

    Article  Google Scholar 

  • Butterbach-Bahl K, Baggs EM, Dannenmann M, Kiese R, Zechmeister BS (2013) Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Phil Trans R Soc B 368:20130122

    Article  PubMed  PubMed Central  Google Scholar 

  • Cavagnaro TR, Langley AJ, Jackson LE, Smukler SM, Koch GW (2008) Growth, nutrition, and soil respiration of a mycorrhiza-defective tomato mutant and its mycorrhizal wild-type progenitor. Funct Plant Biol 35:228–235

    Article  CAS  PubMed  Google Scholar 

  • Cavagnaro TR, Barrios-Masias FH, Jackson LE (2012) Arbuscular mycorrhizas and their role in plant growth, nitrogen interception and soil gas efflux in an organic production system. Plant Soil 353:181–194

    Article  CAS  Google Scholar 

  • Cavagnaro RT, Bender SF, Asghari HR, van der Heijden MGA (2015) The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci 20:283–290

    Article  CAS  PubMed  Google Scholar 

  • Chadwick DR, Cardenas L, Misselbrook TH, Smith KA, Rees RM, Watson CJ, Mcgeough KL, William JR, Clou JM, Thorman RE, Dhanoe MS (2014) Optimizing chamber methods for measuring nitrous oxide emissions from plot-based agricultural experiments. Eur J Soil Sci 65:295–307

    Article  CAS  Google Scholar 

  • Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087

    Article  CAS  PubMed  Google Scholar 

  • Compant S, van der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interaction. FEMS Microbiol Ecol 73:197–214

    CAS  PubMed  Google Scholar 

  • Conthe M, Wittorf L, Kuenen GK, Kleerebezem R, van Loosdrecht MCM, Hallin S (2018) Life on N2O: deciphering the ecophysiology of N2O respiring bacterial communities in a continuous culture. ISME J 12:1142–1153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dannenmann M, Butterbach-Bahl K, Gasche R, Willibald G, Papen H (2008) Dinitrogen emissions and the N2:N2O emission ratio of a Rendzic Leptosol as influenced by pH and forest thinning. Soil Biol Biochemi 40:2317–2323

    Article  CAS  Google Scholar 

  • Davidson EA, Keller M, Erickson HE, Verchot LV, Veldkamp E (2000) Testing a conceptual model of soil emissions of nitrous and nitric oxides. Bioscience 50:667–680

    Article  Google Scholar 

  • Domeignoz-Horta LA, Spor A, Bru D, Breuil MC, Bizouard F, Léonard J, Philippot L (2015) The diversity of the N2O reducers matters for the N2O:N2 denitrification end-product ratio across an annual and perennial cropping system. Front Microbiol 6:971

    Article  PubMed  PubMed Central  Google Scholar 

  • Drigo B, Donn S (2017) Trading carbon between arbuscular mycorrhizal fungi and their hyphae-associated microbes. In: Johnson NC, Gehring C, Jansa J (Eds). Mycorrhizal Mediation of Soil. Elsevier, pp 395–412

  • Ernfors M, Rütting T, Klemedtsson L (2011) Increased nitrous oxide emissions from a drained organic forest soil after exclusion of ectomycorrhizal mycelia. Plant Soil 343:161–170

    Article  CAS  Google Scholar 

  • Èuhel J, Šimek M (2011) Proximal and distal control by pH of denitrification rate in a pasture soil. Agric Ecosyst Environ 141:230–233

    Article  Google Scholar 

  • Fitter AH, Heinemeyer A, Staddon PL (2000) The impact of elevated CO2 and global climate change on arbuscular mycorrhizas: a mycocentric approach. New Phytol 147:179–187

    Article  CAS  Google Scholar 

  • Forster P, Ramaswamy V, Artaxo P, Berntsen T, Betts R, Fahey DW, Haywood J, Lean J, Lowe DC, Myhre G, Nganga J, Prinn R, Raga G, Schulz M, Van Dorland R (2007) Changes in Atmospheric Constituents and in Radiative Forcing. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA

    Google Scholar 

  • Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823

    Article  CAS  PubMed  Google Scholar 

  • Graf DRH, Jones CM, Hallin S (2014) Intergenomic comparisons highlight modularity of the denitrification pathway and underpin the importance of community structure for N2O emissions. PLoS ONE 9:e114118

    Article  PubMed  PubMed Central  Google Scholar 

  • Graf DRH, Zhao M, Jones CM, Hallin S (2016) Soil type overrides plant effect on genetic and enzymatic N2O production potential in arable soils. Soil Biol Biochem 100:125–128

    Article  CAS  Google Scholar 

  • Graham JH, Leonard RT, Menge JA (1981) Membrane-mediated decrease in root exudation responsible for phosphorus inhibition of vesicular-arbuscular mycorrhiza formation. Plant Physiol 68:548–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graw D (1979) The influence of soil pH on the efficiency of vesicular-arbuscular mycorrhiza. New Phytol 82:687–695

    Article  CAS  Google Scholar 

  • Griffis TJ, Chen Z, Baker JM, Wood JD, Millet DB, Lee X, Venterea RT, Turner PA (2017) Nitrous oxide emissions are enhanced in a warmer and wetter world. Proc Natl Acad Sci U S A 114:12081–12085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groffman PM, Tiedje JM, Robertson GP, Christensen S (1988) Dentrification at different temporal and geographical scales: proximal and distal controls. In: Wilson JR (ed) Advances in nitrogen cycling in agricultural ecosystems. CAB International, Walling ford, pp 174–192

    Google Scholar 

  • Groffman PM, Holland E, Myrold DD, Robertson GP, Zou X (1999) Denitrification. In: Robertson GP, Bledsoe CS, Coleman DC, Sollins P (eds) Standard soil methods for long term ecological research. Oxford University Press, New York, pp 272–288

    Google Scholar 

  • Gui H, Gao Y, Wang Z, Shi L, Yan K, Xu J (2021) Arbuscular mycorrhizal fungi potentially regulate N2O emissions from agricultural soils via altered expression of denitrification genes. Sci Total Environ 774:145133

    Article  CAS  PubMed  Google Scholar 

  • Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344

    Article  Google Scholar 

  • Heinemeyer A, Fitter AH (2004) Impact of temperature on the arbuscular mycorrhizal (AM) symbiosis: growth responses of the host plant and its AM fungal partner. J Exp Bot 55:525–534

    Article  CAS  PubMed  Google Scholar 

  • Heinemeyer A, Ineson P, Ostle N, Fitter AH (2006) Respiration of the external mycelium in the arbuscular mycorrhizal symbiosis shows strong dependence on recent photosynthates and acclimation to temperature. New Phytol 171:159–170

    Article  CAS  PubMed  Google Scholar 

  • Helgason T, Fitter AH (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J Exp Bot 60:2465–2480

    Article  CAS  PubMed  Google Scholar 

  • Henderson SL, Dandie CE, Pattern CL, Zebarth BJ, Burton DL, Trevors JT, Goyer C (2010) Changes in denitrifier abundance, denitrification gene mRNA levels, nitrous oxide emissions, and denitrification in anoxic soil microcosms amended with glucose and plant residues. Appl Environ Microbiol 76:2155–2164

  • Hino T, Matsumoto Y, Nagano S, Sugimoto H, Fukumori Y, Murata T, Iwata S, Shiro Y (2010) Structural basis of biological N2O generation by bacterial nitric oxide reductase. Science 330:1666–1670

    Article  CAS  PubMed  Google Scholar 

  • Hodge A (2001) Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil. New Phytol 151:725–734

    Article  CAS  PubMed  Google Scholar 

  • Hodge A, Fitter AH (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hodge A, Storer K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil 386:1–19

    Article  CAS  Google Scholar 

  • Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299

    Article  CAS  PubMed  Google Scholar 

  • Hughes JK, Hodge A, Fitter AH, Atkin OK (2008) Mycorrhizal respiration: implications for global scaling relationships. Trends Plant Sci 13:583–588

    Article  CAS  PubMed  Google Scholar 

  • IPCC (2021) Climate Change 2021: The physical science basis. Contribution of working group I to the sixth assessment report of the intergovernmental panel on climate change. In: Masson-Delmotte V., et al., (Eds.) Cambridge University Press

    Google Scholar 

  • Jia Y, van der Heijden MGA, Wagg C, Feng G, Walder F (2020) Symbiotic soil fungi enhance resistance and resilience of an experimental grassland to drought and nitrogen deposition. J Ecol 109:3171–3181

    Article  Google Scholar 

  • Johansen A, Jakobsen I, Jensen ES (1992) Hyphal transport of 15N-labeled nitrogen by a vesicular-arbuscular mycorrhizal fungus and its effect on depletion of inorganic soil-N. New Phytol 122:281–288

    Article  CAS  PubMed  Google Scholar 

  • Johnson D, Krsek M, Wellington EMH, Stott A, Cole L, Bardgett RD, Read DJ, Leake JR (2005) Soil invertebrates disrupt carbon flow through fungal networks. Nature 309:1047

    CAS  Google Scholar 

  • Jones MD, Durall DM, Tinker PB (1998) A comparison of arbuscular and ectomycorrhizal Eucalyptus coccifera: growth response, phosphorus uptake efficiency and external hyphal production. New Phytol 140:125–134

    Article  Google Scholar 

  • Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480

    Article  CAS  PubMed  Google Scholar 

  • Jones CM, Spor A, Brennan FP, Breuil MC, Bru D, Lemanceau P, Griffiths B, Hallin S, Philippot L (2014) Recently identified microbial guild mediates soil N2O sink capacity. Nat Clim Change 4:801–805

    Article  CAS  Google Scholar 

  • Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, Solaiman ZM, Murphy DV (2015) Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol 205:1537–1551

    Article  CAS  PubMed  Google Scholar 

  • Keeney DR (1986) Critique of the acetylene blockage technique for field measurement of denitrification. In: Hauck RD, Weaver RW (eds) Field measurement of dinitrogen fixation and denitrification, vol 18. SSSA Special Publications

    Google Scholar 

  • Khalil K, Renault P, Mary B (2005) Effects of transient anaerobic conditions in the presence of acetylene on subsequent aerobic respiration and N2O emission by soil aggregates. Soil Biol Biochem 37:1333–1342

    Article  CAS  Google Scholar 

  • Krause HM, Thonar C, Eschenbach W, Well R, Paul Mader P, Behrens S, Kappler A, Gattinger A (2017) Long term farming systems affect soils potential for N2O production and reduction processes under denitrifying conditions. Soil Biol Biochem 114:31–41

  • Langley JA, Johnson NC, Koch GW (2005) Mycorrhizal status influences the rate but not the temperature sensitivity of soil respiration. Plant Soil 277:335–344

    Article  CAS  Google Scholar 

  • Larimer AL, Clay K, Bever JD (2014) Synergism and context dependency of interactions between Arbuscular mycorrhizal fungi and Rhizobia with a prairie legume. Ecology 95:1045–1054

    Article  PubMed  Google Scholar 

  • Lazcano C, Barrios-Masias FH, Jackson LE (2015) Arbuscular mycorrhizal effects on plant water relations and soil greenhouse gas emissions under changing moisture regimes. Soil Biol Biochem 74:184–192

    Article  Google Scholar 

  • Lee DS, Bouwman AF, Asman WAH, Dentener FJ, van der Hoek KW, Olivier JGJ (1997) Emissions of nitric oxide, nitrous oxide and ammonia from grasslands on a global scale. In: Jarvis SC, Pains BF (eds) Gaseous nitrogen emissions from grasslands. CAB International, Wallingford, pp 353–371

    Google Scholar 

  • Lehmann A, Rillig MC (2015) Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops - A meta-analysis. Soil Biol Biochem 81:147–158

    Article  CAS  Google Scholar 

  • Leifheit EF, Veresoglou SD, Lehmann A, Morris EK, Rillig MC (2014) Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation- a meta-analysis. Plant Soil 374:523–537

    Article  CAS  Google Scholar 

  • Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207

    Article  CAS  PubMed  Google Scholar 

  • Li XL, George E, Marschner H (1991) Phosphorus depletion and pH decrease at the root-soil and hyphaesoil interfaces of VA mycorrhizal white clover fertilized with ammonium. New Phytol 119:397–404

    Article  CAS  Google Scholar 

  • Lin G, McCormack ML, Guo D (2015) Arbuscular mycorrhizal fungal effects on plant competition and community structure. J Ecol 103:1224–1232

    Article  CAS  Google Scholar 

  • Liu B, Frostegård Å, Bakken LR (2014) Impaired reduction of N2O to N2 in acid soils is due to a posttranscriptional interference with the expression of nosZ. Mbio 5:e01383–e1414

    Article  PubMed  PubMed Central  Google Scholar 

  • Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748

    Article  CAS  PubMed  Google Scholar 

  • Marschner P, Baumann K (2003) Changes in bacterial community structure induced by mycorrhizal colonisation in split-root maize. Plant Soil 251:279–289

    Article  CAS  Google Scholar 

  • Marschner P, Crowley DE, Higashi M (1997) Root exudation and physiological status of a root-colonizing fluorescent pseudomonad in mycorrhizal and non-mycorrhizal pepper (Capsicum annuum L.). Plant Soil 189:11–20

    Article  CAS  Google Scholar 

  • Martin J (1964) Bibliometric coupling. J Doc 20:236–236

    Article  Google Scholar 

  • Mushinski RM, Rayns ZC, Raff JD, Craig ME, Pusede SE, Rusch DB, White JR, Phillips RP (2021) Nitrogen cycling microbiomes are structured by plant mycorrhizal associations with consequences for nitrogen oxide fluxes in forests. Glob Chang Biol 27:1068–1082

    Article  CAS  Google Scholar 

  • Niklaus PA, Le Roux X, Poly F, Buchmann N, Lorenzen MS, Weigelt A, Barnard RL (2016) Plant species diversity affects soil-atmosphere fluxes of methane and nitrous oxide. Oecologia 181:919–930

    Article  PubMed  Google Scholar 

  • Nottingham AT, Turner BL, Winter K, van der Heijden MGA, Tanner EVJ (2010) Arbuscular mycorrhizal mycelial respiration in a moist tropical forest. New Phytol 186:957–967

    Article  CAS  PubMed  Google Scholar 

  • Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK (2013) An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ Microbiol 15:1870–1881

    Article  CAS  PubMed  Google Scholar 

  • Nwaga D, Jansa J, Abossolo AM, Frossard E (2010) The potential of soil beneficial micro-organisms for slash-and-burn agriculture in the humid forest zone of sub Saharan Africa. In: Dion P (ed) Soil biology and agriculture in the tropics. Springer Heidelberg Dordrecht, London, New York, pp 80–107

    Google Scholar 

  • Okiobe ST, Abossolo AM, Bougnom BP, Boyomo O, Nwaga D (2015) Improvement of arbuscular mycorrhizal fungi inoculum production by nutrient solution concentration and soil texture variation. Int J Agron Agric Res 6:7–20

    Google Scholar 

  • Okiobe ST, Augustin J, Mansour I, Veresoglou SD (2019) Disentangling direct and indirect effects of mycorrhiza on nitrous oxide activity and denitrification. Soil Biol Biochem 134:142–151

    Article  CAS  Google Scholar 

  • Okiobe ST, Rillig MC, Mola M, Augustin J, Parolly G, Veresoglou SD (2020) Arbuscular mycorrhiza has little influence on N2O potential emissions compared to plant diversity in experimental plant communities. FEMS Microbiol Ecol 96:fiz208

    Article  CAS  PubMed  Google Scholar 

  • Park JY, Yoo YJ (2009) Biological nitrate removal in industrial wastewater treatment: which electron donor we can choose. Appl Microbiol Biotechnol 82:415–429

    Article  CAS  PubMed  Google Scholar 

  • Philippot L, Cuhel J, Saby NP, Cheneby D, Chronakova A, Bru D, Arrouays D, Martin F, Laurent F, Simek M (2009) Mapping field-scale spatial patterns of size and activity of the denitrifier community. Environ Microbiol 11:1518–1526

    Article  PubMed  Google Scholar 

  • Philippot L, Andert J, Jones CM, Bru DI, Hallin S (2011) Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Glob Change Biol 17:1497–1504

    Article  Google Scholar 

  • Philippot L, Spor A, Hénault C, Bru D, Bizouard F, Jones CM, Sarr A, Maron PA (2013) Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7:1609–1619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol 199:41–51

    Article  CAS  PubMed  Google Scholar 

  • Powell JR, Rillig MC (2018) Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. New Phytol 220:1059–1075

    Article  PubMed  Google Scholar 

  • Prendergast-Miller MT, Baggs EM, Johnson D (2011) Nitrous oxide production by the ectomycorrhizal fungi Paxillus involutus and Tylospora fibrillosa. FEMS Microbiol Let 316:31–35

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): The dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125

    Article  CAS  PubMed  Google Scholar 

  • Reay DS, Davidson EA, Smith KA, Smith P, Melillo JM, Dentener F, Crutzen PJ (2012) Global agriculture and nitrous oxide emissions. Nat Clim Chang 2:140–416

    Article  Google Scholar 

  • Rillig MC (2004a) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754

    Article  Google Scholar 

  • Rillig MC (2004b) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Let 7:740–754

    Article  Google Scholar 

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53

    Article  CAS  PubMed  Google Scholar 

  • Rillig MC, Field CB, Allen MF (1999) Soil biota responses to long-term atmospheric CO2 enrichment in two California annual grasslands. Oecologia 119:572–577

    Article  PubMed  Google Scholar 

  • Rillig MC, Hernandez GY, Newton PCD (2000) Arbuscular mycorrhizae respond to elevated atmospheric CO2 after long-term exposure: evidence from a CO2 spring in New Zealand supports the resource balance model. Ecol Let 3:475–478

    Article  Google Scholar 

  • Rillig MC, Wright SF, Shaw MR, Field CB (2002) Artificial climate warming positively affects arbuscular mycorrhizae but decreases soil aggregate water stability in an annual grassland. Oikos 97:52–58

    Article  Google Scholar 

  • Rillig MC, Mardatin NF, Leifheit EF, Antunes PM (2010) Mycelium of arbuscular mycorrhizal fungi increases soil water repellency and is sufficient to maintain water-stable soil aggregates. Soil Biol Biochem 42:1189–1191

    Article  CAS  Google Scholar 

  • Rillig MC, Sosa-Hernandez MA, Roy J, Aguilar-Trigueros CA, Valyi K, Lehmann A (2016) Towards an integrated mycorrhizal technology: harnessing mycorrhizae for sustainable intensification in agriculture. Frontiers Plant Sci 7:1625

    Article  Google Scholar 

  • Rillig MC, Aguilar-Trigueros CA, Camenzind T, Cavagnaro T, Degrune F, Hohmann P, Lammel D, Mansour I, Roy J, van der Heijden MGA, Yang G (2018) Why farmers should manage the arbuscular mycorrhizal symbiosis - a response to Ryan and Graham. New Phytol 222:1171–1175

    Article  Google Scholar 

  • Robertson GP, Groffman PM (2015) Nitrogen transformations. In: Paul EA (ed) Soil microbiology, ecology and biochemistry, 4th edn. Academic Press, Burlington, pp 421–446

    Chapter  Google Scholar 

  • Saggar S, Jha N, Deslippe J, Bolan NS, Luo J, Giltrap DL, Kim DG, Zaman M, Tilman RW (2013) Denitrification and N2O:N2 production in temperate grasslands: Processes, measurements, modelling and mitigating negative impacts. Sci Tot Environ 465:173–195

    Article  CAS  Google Scholar 

  • Samad MS, Bakken LR, Nadeem S, Clough TJ, de Klein CAM, Richards KG, Lanigan GJ, Morales SE (2016) High resolution denitrification kinetics in pasture soils link N2O emissions to pH, and denitrification to C Mineralization. PLoS ONE 11:0151713

    Article  Google Scholar 

  • Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH, Cruz-García C, Rodríguez G, Massol-Deyá A, Krishnani KK, Ritalahti KM, Nissen S, Konstantinidis KT, Löffleret FE (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc Natl Acad Sci U S A 109:19709–19714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlüter S, Henjes S, Zawallich J, Bergaust L, Horn M, Ippisch O, Vogel HJ, Dörsch P (2018) Denitrification in soil aggregate analogues-effect of aggregate size and oxygen diffusion. Front Environ Sci 6:17

    Article  Google Scholar 

  • Sexstone AJ, Revsbech NP, Parkin TB, Tiedje JM (1985) Direct measurement of oxygen profiles and denitrification rates in soil aggregates. Soil Sci Soc Am J 49:645–651

    Article  CAS  Google Scholar 

  • Sey BS, Manceur AM, Wahlen JK, Gregorich EG, Rochette P (2008) Small-scale heterogeneity in carbon dioxide, nitrous oxide and methane production from aggregates of a cultivated sandy-loam soil. Soil Biol Biochem 40:2468–2473

    Article  CAS  Google Scholar 

  • Shi ZY, Zhang XF, Wang FY (2010) Influence of mycorrhizal fungi on soil respiration. Ecol Environ Sci l9:233–238

    Google Scholar 

  • Sikes BA, Powell JR, Rillig MC (2010) Deciphering the relative contributions of multiple functions within plant-microbe symbioses. Ecology 91:1591–1597

    Article  PubMed  Google Scholar 

  • Šimek M, Cooper JE (2002) The influence of soil pH on denitrification: progress towards the understanding of this interaction over the last 50 years. Eur J Soil Sci 53:345–354

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, Boston

    Google Scholar 

  • Smith KA, Ball T, Conen F, Dobbie KE, Massheder J, Rey A (2003) Exchange of greenhouse gases between soil and atmosphere: interactions of soil physical factors and biological processes. Eur J Soil Sci 54:779–791

  • Sokol NW, Bradford MA (2019) Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nat Geosci 12:46–53

    Article  CAS  Google Scholar 

  • Springmann M, Clark M, Mason-D’croz D, Wiebe K, Bodirsky BL, Lassaletta L, de Vries W, Vermeulen SJ, Herrero M, Carlson KM, Jonell M, Troell M, Declerck F, Gordon LJ, Zurayk R, Scarborough P, Rayner M, Loken B, Fanzo J, Godfray HCJ, Tilman D, Rockström J, Willett W (2018) Options for keeping the food system within environmental limits. Nature 562:519–525

    Article  CAS  PubMed  Google Scholar 

  • Staddon PL, Fitter AH (1998) Does elevated atmospheric carbon dioxide affect arbuscular mycorrhizas? Trends Ecol Evol 13:455–458

    Article  CAS  PubMed  Google Scholar 

  • Staddon PL, Fitter AH, Graves JD (1999a) Effect of elevated atmospheric CO2 on mycorrhizal colonization, external mycorrhizal colonization on photosynthesis and biomass hyphal production and phosphorus inflow in Plantago Lanceolata lanceolata and Trifolium repens in the association with the arbuscular mycorrhizal fungus Glomus mosseae. Glob Chang Biol 5:347–358

    Article  Google Scholar 

  • Staddon PL, Fitter AH, Robinson D (1999b) Effects of mycorrhizal colonization and elevated atmospheric carbon dioxide on carbon fixation and below-ground carbon partitioning in Plantago lanceolata. J Exp Bot 50:853–860

    Article  CAS  Google Scholar 

  • Staddon PL, Gregersen R, Jakobsen I (2004) The response of two Glomus mycorrhizal fungi and a fine endophyte to elevated atmospheric CO2, soil warming and drought. Glob Chang Biol 10:1909–1921

    Article  Google Scholar 

  • Stein LY (2011) Surveying N2O-Producing Pathways in Bacteria. Methods Enzymol 486:131–152

    Article  CAS  PubMed  Google Scholar 

  • Stockinger H, Walker C, Schüßler A (2009) ‘Glomus intraradices DAOM197198 ’, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytol 183:1176–1187

    Article  PubMed  Google Scholar 

  • Storer K, Coggan A, Ineson P, Hodge A (2018) Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots. New Phytol 220:1285–1295

    Article  CAS  PubMed  Google Scholar 

  • Suzuki S, Kataoka K, Yamaguchi K (2000) Metal coordination and mechanism of multicopper nitrite reductase. Acc Chem Res 33:728–735

    Article  CAS  PubMed  Google Scholar 

  • Syakila A, Kroeze C (2011) The global nitrogen budget revisited. Greenhouse Gas Meas Manage 1:17–26

    Article  CAS  Google Scholar 

  • Tamayo E, Gómez-Gallego T, Azcón-Aguilar C, Nuria Ferrol N (2014) Genome-wide analysis of copper, iron and zinc transporters in the arbuscular mycorrhizal fungus Rhizophagus irregularis. Front Plant Sci 5:547

    Article  PubMed  PubMed Central  Google Scholar 

  • Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ 28:1247–1254

    Article  CAS  Google Scholar 

  • Tatsumi C, Taniguchi T, Du S, Yamanaka N, Tateno R (2020) Soil nitrogen cycling is determined by the competition between mycorrhiza and ammonia-oxidizing prokaryotes. Ecology 101:e02963

    Article  PubMed  Google Scholar 

  • Teutscherova N, Vazquez E, Arango J, Arevalo A, Benito M, Pulleman M (2018) Native arbuscular mycorrhizal fungi increase the abundance of ammonia-oxidizing bacteria, but suppress nitrous oxide emissions shortly after urea application. Geoderma 338:493–501

    Article  Google Scholar 

  • Teutscherova N, Vazquez E, Arangoc J, Arevalo A, Benito M, Pulleman M (2019) Native arbuscular mycorrhizal fungi increase the abundance of ammonia-oxidizing bacteria, but suppress nitrous oxide emissions shortly after urea application. Geoderma 338:493–501

  • Thompson AJ, Giannopoulos G, Pretty J, Baggs EM, Richardson DJ (2012) Biological sources and sinks of nitrous oxide and strategies to mitigate emissions. Philos Trans R Soc Lond B Biol Sci 367:1157–1168

    Article  Google Scholar 

  • Tiedje JM, Simkins S, Groffman PM (1989) Perspectives on measurement of denitrification in the field including recommended protocols for acetylene based methods. Plant Soil 115:261–284

    Article  Google Scholar 

  • Tisdall JM, Oades JM (1982) Organic matter and water-stable aggregates in soils. J Soil Sci 33:141–163

    Article  CAS  Google Scholar 

  • Van der Heijden MGA (2002) Arbuscular mycorrhizal fungi as a determinant of plant diversity: in Search of Underlying Mechanisms and General Principles. van der Heijden MGA , Sanders IR (eds). In Mycorrhizal Ecology. pp 243–256

  • van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:72–75

  • Van der Heijden MGA, Bakker R, Verwaal J, Scheublin TR, Rutten M, van Logtestijn R, Staehelin C (2006a) Symbiotic bacteria as a determinant of plant community structure and plant productivity in dune grassland. FEMS Microbiol Ecol 56:178–187

    Article  PubMed  Google Scholar 

  • van der Heijden MGA, Streitwolf-Engel R, Riedl R, Siegrist S, Neudecker A, Ineichen K, Boller T, Wiemken A, Sanders IR (2006b) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol 172:739–752

    Article  PubMed  Google Scholar 

  • van der Heijden MGA, De Bruin S, Luckerhoff L, van Logtestijn RSP, Schlaeppi K (2015) A widespread plant-fungal-bacteria symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J 10:389–399

    Article  PubMed  PubMed Central  Google Scholar 

  • Verbruggen E, Veresoglou SD, Anderson IC, Caruso T, Hammer EC, Kohler J, Rillig MC (2013) Arbuscular mycorrhizal fungi – short-term liability but long-term benefits for soil carbon storage. New Phytol 197:366–368

    Article  PubMed  Google Scholar 

  • Veresoglou SD, Robin S, Mamolos AP, Veresoglou DS (2011) Plant species identity and arbuscular mycorrhizal status modulate potential nitrification rates in nitrogen-limited grassland soils. J Ecol 99:1339–1349

    Article  CAS  Google Scholar 

  • Veresoglou SD, Shaw LJ, Hooker JE, Sen R (2012a) Arbuscular mycorrhizal modulation of diazotrophic and denitrifying microbial communities in the (mycor)rhizosphere of Plantago lanceolata. Soil Biol Biochem 53:78–81

    Article  CAS  Google Scholar 

  • Veresoglou SD, Chen B, Rillig MC (2012b) Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol Biochem 46:53–62

    Article  CAS  Google Scholar 

  • Veresoglou SD, Verbruggen E, Makarova O, Mansour I, Sen R, Rillig MC (2019) Arbuscular mycorrhizal fungi alter the community structure of ammonia oxidizers at high fertility via competition for soil NH4+. Microb Ecol 78:147–158

    Article  CAS  PubMed  Google Scholar 

  • Villegas J, Fortin JA (2001) Phosphorus solubilization and pH changes as a result of the interactions between soil bacteria and arbuscular mycorrhizal fungi on a medium containing NH+4 as nitrogen source. Can J Bot 79:865–870

  • Wagg C, Jansa J, Schmid B, van der Heijden MGA (2011) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett 14:1001–1009

    Article  PubMed  Google Scholar 

  • Wallenstein MD, Myrold DD, Firestone M, Voytek M (2006) Environmental controls on denitrification communities and denitrification rates: insights from molecular methods. Ecol Appl 16:2143–2152

    Article  PubMed  Google Scholar 

  • Wang GM, Stribley DP, Tinker PB, Walker C (1993) Effects of pH on arbuscular mycorrhiza I. Field observations on the long-term liming experiments at Rothamsted and Woburn. New Phytol 124:465–472

    Article  CAS  Google Scholar 

  • Wang M, Hu R, Zhao J, Kuzyakov Y, Liu S (2016) Iron oxidation affects nitrous oxide emissions via donating electrons to denitrification in paddy soils. Geoderma 271:173–180

    Article  CAS  Google Scholar 

  • Watts SH, Seitzinger SP (2000) Denitrication rates in organic and mineral soils from riparian sites: a comparison of N2 flux and acetylene inhibition methods. Soil Biol Biochem 32:1383–1392

    Article  CAS  Google Scholar 

  • Wei W, Isobe K, Nishizawa T, Zhu L, Shiratori Y, Ohte N, Koba K, Otsuka S, Senoo K (2015) Higher diversity and abundance of denitrifying microorganisms in environments than considered previously. ISME J 9:1954–1965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wenjuan H, Mengmeng S, Jie C, Yuan R, Ronghua X, Chongbang Z, Ying G (2017) Plant species diversity reduces NO but not CH emissions from constructed wetlands under high nitrogen levels. Environ Sci Pollut Res 24:5938–6584

    Article  Google Scholar 

  • Zhang X, Wang L, Ma F, Shan D (2015) Effects of arbuscular mycorrhizal fungi on N2O emissions from rice paddies. Water Air Soil Pollut 226:222–232

    Article  Google Scholar 

  • Zhang B, Li S, Chen S, Ren T, Yang Z, Zhao H, Liang Y, Han X (2016) Arbuscular mycorrhizal fungi regulate soil respiration and its response to precipitation change in a semiarid steppe. Sci Rep 6:19990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Lehmann A, Zheng W, You Z, Rillig MC (2019) Arbuscular mycorrhizal fungi increase grain yields: a meta-analysis. New Phytol 222:543–555

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, You Z, Guo X, Yun W, Xia Y, Rillig MC (2020) Suitability of mycorrhiza-defective rice and its progenitor for studies on the control of nitrogen loss in paddy fields via arbuscular mycorrhiza. Frontiers Microbiol 11:186

    Article  Google Scholar 

  • Zhang H, Powell JR, Power SA, Churchill AC, Plett JM, Macdonald CA, Jacob V, Kim GW, Pendall E, Tissue DT, Catunda KLM, Igwenagu C, Carrillo Y, Moore BD, Anderson IC (2021) Arbuscular mycorrhizal fungal-mediated reductions in N2O emissions were not impacted by experimental warming for two common pasture species. Pedobiologia 87–88:150744

    Article  Google Scholar 

  • Zhou Y, Watts SE, Boutton TW, Archer SR (2019) Root density distribution and biomass allocation of co-occurring woody plants on contrasting soils in a subtropical savanna parkland. Plant Soil 438:263–279

    Article  CAS  Google Scholar 

  • Zhu X, Silva LCR, Doane TA, Horwath WR (2013) Iron: the forgotten driver of nitrous oxide production in agricultural soil. PLoS ONE 8:60146

    Article  Google Scholar 

  • Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The manuscript benefitted considerably from the constructive comments from four anonymous reviewers.

Author information

Authors and Affiliations

  1. Institut für Biologie, Freie Universität Berlin, Berlin, Germany

    Simon T. Okiobe, Karin Pirhofer-Walzl, Eva. F. Leifheit & Matthias C. Rillig

  2. Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), 14195, Berlin, Germany

    Simon T. Okiobe, Karin Pirhofer-Walzl, Eva. F. Leifheit & Matthias C. Rillig

  3. Leibniz Centre for Agricultural Landscape Research (ZALF), Eberswalder Str. 84, 15374, Müncheberg, Germany

    Karin Pirhofer-Walzl

  4. School of Ecology, State Key Laboratory of Biocontrol, Sun Yat-Sen University, Shenzhen, 518107, China

    Stavros D. Veresoglou

Authors
  1. Simon T. Okiobe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karin Pirhofer-Walzl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eva. F. Leifheit
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matthias C. Rillig
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stavros D. Veresoglou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Matthias C. Rillig or Stavros D. Veresoglou.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Katharina Pawlowski.

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 93 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Okiobe, S.T., Pirhofer-Walzl, K., Leifheit, E.F. et al. Proximal and distal mechanisms through which arbuscular mycorrhizal associations alter terrestrial denitrification. Plant Soil 476, 315–336 (2022). https://doi.org/10.1007/s11104-022-05534-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-022-05534-x

Keywords

Search

Navigation