Abstract
Life-history traits differ substantially among arbuscular mycorrhizal (AM) fungal families, potentially affecting hyphal nutrient acquisition efficiency, host nutrition, and thereby plant health and ecosystem function. Despite these implications, AM fungal community life-history strategies and community trait diversity effects on host nutrient acquisition are poorly understood. To address this knowledge gap, we grew sudangrass with AM fungal communities representing contrasting life-history traits and diversity: either (1) five species in the AM family Gigasporaceae, representing competitor traits, (2) five Glomerales species, representing ruderal traits, or (3) a mixed-trait community combining all ten AM fungal species. After 12 weeks, we measured above and belowground plant biomass and aboveground nutrient uptake and concentration. Overall, AM fungal colonization increased host nutrition, biomass, and foliar δ5nitrogen enrichment compared to the uncolonized control. Between the single-trait communities, the Glomeraceae community generally outperformed the Gigasporaceae community in host nutrition and plant growth, increasing plant phosphorus (P) uptake 1.5 times more than the Gigasporaceae community. We saw weak evidence for a synergistic effect of the mixed community, which was only higher for plant P concentration (1.26 times higher) and root colonization (1.26 times higher) compared to the single-trait communities. However, this higher P concentration did not translate to more P uptake or the highest plant biomass for the mixed community. These findings demonstrate that the AM symbiosis is affected by community differences at high taxonomic levels and provide insight into how different AM fungal communities and their associated traits affect host nutrition for fast-growing plant species.
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Data availability
The datasets generated during and/or analysed for the current study are available from the corresponding author on reasonable request.
References
Aguilar-Trigueros CA et al (2015) Branching out: towards a trait-based understanding of fungal ecology. Fungal Biol Rev 29(1):34–41. https://doi.org/10.1016/j.fbr.2015.03.001
Alguacil MM, Lozano Z, Campoy MJ, Roldán A (2010) Phosphorus fertilisation management modifies the biodiversity of AM fungi in a tropical savanna forage system. Soil Biol Biochem 42(7):1114–1122
Amundson R et al (2003) Global patterns of the isotopic composition of soil and plant nitrogen. Global Biogeochem Cycles 17(31):31–31
Bago B et al (1998) Branched absorbing structures (BAS): a feature of the extraradical mycelium of symbiotic arbuscular mycorrhizal fungi. New Phytol 139(2):375–388. https://doi.org/10.1046/J.1469-8137.1998.00199.x
Barnes CJ, Burns CA, Van der Gast CJ, McNamara NP, Bending GD (2016) Spatio-temporal variation of core and satellite arbuscular mycorrhizal fungus communities in Miscanthus giganteus. Front Microbiol 7:1278
Bennett AE, Bever JD (2009) Trade-offs between arbuscular mycorrhizal fungal competitive ability and host growth promotion in Plantago lanceolata. Oecologia 160(4):807–816
Bever JD, Schultz PA, Pringle A, Morton JB (2001) Arbuscular mycorrhizal fungi: more diverse than meets the eye, and the ecological tale of why: the high diversity of ecologically distinct species of arbuscular mycorrhizal fungi within a single community has broad implications for plant ecology. Bioscience 51:923–931
Boddington CL, Dodd JC (1999) Evidence that differences in phosphate metabolism in mycorrhizas formed by species of Glomus and Gigaspora might be related to their life-cycle strategies. New Phytol 142(3):531–538
Bowles TM, Jackson LE, Cavagnaro TR (2018) Mycorrhizal fungi enhance plant nutrient acquisition and modulate nitrogen loss with variable water regimes. Glob Change Biol 24(1):e171–e182
Bruce A, Smith SE, Tester M (1994) The development of mycorrhizal infection in cucumber: effects of P supply on root growth, formation of entry points and growth of infection units. New Phytol 127(3):507–514. https://doi.org/10.1111/J.1469-8137.1994.tb03968.x
Brundrett M, Melville L, Peterson L (1994) Extraction and staining of hyphae from soil. Mycologue Publications, Guelph, pp 24–34
Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220(4):1108–1115. https://doi.org/10.1111/nph.14976
Bücking H, Shachar-Hill Y (2005) Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. New Phytol 165(3):899–912. https://doi.org/10.1111/j.1469-8137.2004.01274.x
Cano C, Bago A (2005) Competition and substrate colonization strategies of three polyxenically grown arbuscular mycorrhizal fungi. Mycologia 97:1201–1214
Chagnon PL et al (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18(9):484–491. https://doi.org/10.1016/j.tplants.2013.05.001
Chaudhary VB et al (2002) What are mycorrhizal traits? Trends Ecol Evol 37(7):573–581
Chen EC et al (2018) High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis. New Phytol 220(4):1161–1171
Craine JM et al (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183(4):980–992
Craine JM, Morrow C, Stock WD (2008) Nutrient concentration ratios and co-limitation in South African grasslands. New Phytol 179(3):829–836
Crossay T et al (2019) Is a mixture of arbuscular mycorrhizal fungi better for plant growth than single-species inoculants? Mycorrhiza 29(4):325–339. https://doi.org/10.1007/s00572-019-00898-y/figures/6
Crowther TW et al (2014) Untangling the fungal niche: the trait-based approach. Front Microbiol 5(1):579. https://doi.org/10.3389/fmicb.2014.00579/bibtex
De Baar HJW (1994) von Liebig’s law of the minimum and plankton ecology (1899–1991). Prog Oceanogr 33(4):347–386. https://doi.org/10.1016/0079-6611(94)90022-1
Engelmoer DJ, Behm JE, Kiers TE (2014) Intense competition between arbuscular mycorrhizal mutualists in an in vitro root microbiome negatively affects total fungal abundance. Mol Ecol 23(6):1584–1593
Feddermann N, Finlay R, Boller T, Elfstrand M (2010) Functional diversity in arbuscular mycorrhiza–the role of gene expression, phosphorous nutrition and symbiotic efficiency. Fungal Ecol 3(1):1–8
Frey SD (2019) Mycorrhizal fungi as mediators of soil organic matter dynamics. Annu Rev Ecol Evol Syst 50(1):237
Giri B, Kapoor R, Mukerji KG (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 54(4):753–760. https://doi.org/10.1007/s00248-007-9239-9/tables/1
Gosling P, Jones J, Bending GD (2016) Evidence for functional redundancy in arbuscular mycorrhizal fungi and implications for agroecosystem management. Mycorrhiza 26(1):77–83. https://doi.org/10.1007/s00572-015-0651-6
Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111(982):1169–1194. https://doi.org/10.1086/283244
Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153(2):335–344. https://doi.org/10.1046/j.0028-646x.2001.00312.x
Hart MM, Reader RJ (2005) The role of the external mycelium in early colonization for three arbuscular mycorrhizal fungal species with different colonization strategies. Pedobiologia 49(3):269–279. https://doi.org/10.1016/j.pedobi.2004.12.001
Hobbie EA, Högberg P (2012) Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytol 196(2):367–382. https://doi.org/10.1111/J.1469-8137.2012.04300.x
Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci 107(31):13754–13759
Hodge A, Storer K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil 386(1–2):1–19. https://doi.org/10.1007/s11104-014-2162-1/figures/3
Hoeksema JD et al (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13(3):394–407. https://doi.org/10.1111/j.1461-0248.2009.01430.x
Huang J et al (2021) Plant carbon inputs through shoot, root, and mycorrhizal pathways affect soil organic carbon turnover differently. Soil Biol Biochem 160:108322
Janouskova M, Seddas P, Mrnka L et al (2009) Development and activity of Glomus intraradices as affected by co-existence with Glomus claroideum in one root system. Mycorrhiza 19:393–402
Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789
Javaid A (2009) Arbuscular mycorrhizal mediated nutrition in plants. J Plant Nutr 32(10):1595–1618
Johnson NC et al (2003) Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84(7):1895–1908. https://doi.org/10.1890/0012-9658
Kiers ET et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333(6044):880–882
Kil YJ, Eo JK, Lee EH, Eom AH (2014) Root age-dependent changes in arbuscular mycorrhizal fungal communities colonizing roots of Panax ginseng. Mycobiology 42(4):416–421
Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43(11):2294–2303
Koch AM, Antunes PM, Maherali H, Hart MM, Klironomos JN (2017) Evolutionary asymmetry in the arbuscular mycorrhizal symbiosis: conservatism in fungal morphology does not predict host plant growth. New Phytol 214(3):1330–1337
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. https://doi.org/10.1016/j.soilbio.2014.11.013
Li L, McCormack ML, Chen F, Wang H, Ma Z, Guo D (2019) Different responses of absorptive roots and arbuscular mycorrhizal fungi to fertilization provide diverse nutrient acquisition strategies in Chinese fir. For Ecol Manage 433:64–72
Ma M et al (2018) Chronic fertilization of 37 years alters the phylogenetic structure of soil arbuscular mycorrhizal fungi in Chinese Mollisols. AMB Express 8(1):1–10
Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316(5832):1746–1748. https://doi.org/10.1126/science.1143082/suppl_file/maherali.som.pdf
Malicka M, Magurno F, Posta K, Chmura D, Piotrowska-Seget Z (2021) Differences in the effects of single and mixed species of AMF on the growth and oxidative stress defense in Lolium perenne exposed to hydrocarbons. Ecotoxicol Environ Saf 217:112252
McGonigle TP et al (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol 115(3):495–501. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
McCune B, Mefford MJ (2016) Multivariate analysis of ecological data’, PC-ORD, Version 7.0 for Windows. Wild Blueberry Media, Corvallis, Oregon, U.S.A.
Millar NS, Bennett AE (2016) Stressed out symbiotes: hypotheses for the influence of abiotic stress on arbuscular mycorrhizal fungi. Oecologia 182:625–641
Morton JB, Bentivenga SP, Wheeler WW (1993) Germ plasm in the International Collection of Arbuscular and Vesicular-arbuscular Mycorrhizal Fungi (INVAM) and procedures for culture development, documentation and storage. Mycotaxon 48:491–528. Available at: https://ci.nii.ac.jp/naid/10004976809/. Accessed 28 Mar 2022
Neumann E, Eckhard G (2010) Nutrient uptake: the arbuscular mycorrhiza fungal symbiosis as a plant nutrient acquisition strategy. In Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function, 2nd edn. Springer, New York, pp 137–167. https://doi.org/10.1007/978-90-481-9489-6_7
Parvin S, Van Geel M, Yeasmin T, Verbruggen E, Honnay O (2020) Effects of single and multiple species inocula of arbuscular mycorrhizal fungi on the salinity tolerance of a Bangladeshi rice (Oryza sativa L.) cultivar. Mycorrhiza 30(4):431–444
Pianka ER (1970) On r- and K-selection. Am Nat 104(940):592–597. https://doi.org/10.1086/282697
Powell JR, Parrent JL, Hart MM, Klironomos LN, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc R Soc B Biol Sci 276(1676):4237–4245
Powell JR, Rillig MC (2018) Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. New Phytol 220(4):1059–1075. https://doi.org/10.1111/nph.15119
Redecker D et al (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23(7):515–531
Reznick D, Bryant MJ, Bashey F (2002) r-and K-selection revisited: the role of population regulation in life-history evolution. Spec Feature Ecol 83(6):1509–1520. https://doi.org/10.1890/0012-9658
Roger A, Colard A, Angelard C, Sanders IR (2013) Relatedness among arbuscular mycorrhizal fungi drives plant growth and intraspecific fungal coexistence. ISME J 7(11):2137–2146
Rosner B (1983) Percentage points for a generalized ESD many-outlier procedure. Technometrics 25(2):165–172
Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105(12):1413–1421. https://doi.org/10.1017/S0953756201005196
Seyfried GS, Dalling JW, Yang WH (2021) Mycorrhizal type effects on leaf litter decomposition depend on litter quality and environmental context. Biogeochemistry 155(1):21–38
Smith SE et al (2011) 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 156(3):1050–1057. https://doi.org/10.1104/PP.111.174581
Smith SE, Read DJ (2008) Arbuscular mycorrhizas. In: Smith SE, Read DJ (eds) Mycorrhizal symbiosis, 3rd edn. Academic Press, Boston, pp 11–145
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. https://doi.org/10.1146/annurev-arplant-042110-103846
Smith SE, Smith FA, 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(2):511–524. https://doi.org/10.1111/J.1469-8137.2004.01039.x
Souza FA de, Dalpé Y, Declerck S, de la Providencia IE, Séjalon-Delmas N (2005) Life history strategies in Gigasporaceae: insight from monoxenic culture. In: Declerck S, Strullu DG, Fortin JA (eds) In vitro culture of mycorrhizas, 1st edn. Springer, New York, pp 73–91. https://doi.org/10.1007/3-540-27331-X_5
Staddon PL et al (2003) Rapid turnover of hyphae of mycorrhizal fungi determined by AMS Microanalysis of 14C. Science 300(5622):1138–1140. https://doi.org/10.1126/science.1084269
Tian H, Drijber RA, Niu XS, Zhang JL, Li XL (2011) Spatio-temporal dynamics of an indigenous arbuscular mycorrhizal fungal community in an intensively managed maize agroecosystem in North China. Appl Soil Ecol 47:141–152. https://doi.org/10.1016/j.apsoil.2011.01.002
Tilman D et al (1997) The influence of functional diversity and composition on ecosystem processes. Science 277(5330):1300–1302
Treseder KK et al (2018) Arbuscular mycorrhizal fungi as mediators of ecosystem responses to nitrogen deposition: a trait-based predictive framework. J Ecol 106(2):480–489
Vályi K, Mardhiah U, Rillig MC, Hempel S (2016) Community assembly and coexistence in communities of arbuscular mycorrhizal fungi. ISME J 10:2341–2351
Van der Heijden MG, Scheublin TR (2007) Functional traits in mycorrhizal ecology: their use for predicting the impact of arbuscular mycorrhizal fungal communities on plant growth and ecosystem functioning. New Phytol 174(2):244–250
Verbruggen E, Kiers ET (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl 3:547–560
Veresoglou SD, Rillig MC (2012) Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi. Biol Let 8:214–217
Vierheilig H et al (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64(12):5004–5007. https://doi.org/10.1128/aem.64.12.5004-5007.1998/asset/e2520019-caa3-4d07-acf13e2612319d10/assets/graphic/am1280858001.jpeg
Vukicevich E, Lowery TD, Eissenstat D, Hart M (2019) Changes in arbuscular mycorrhizal fungi between young and old Vitis roots. Symbiosis 78(1):33–42
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
Wagg C, Schlaeppi K, Banerjee S, Kuramae EE, van der Heijden MG (2019) Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nat Commun 10(1):1–10
Wieder WR, Cleveland CC, Townsend AR (2009) Controls over leaf litter decomposition in wet tropical forests. Ecology 90(12):3333–3341
Wurzburger N, Hendrick RL (2009) Plant litter chemistry and mycorrhizal roots promote a nitrogen feedback in a temperate forest. J Ecol 97(3):528–536
Xu M et al (2017) Land use alters arbuscular mycorrhizal fungal communities and their potential role in carbon sequestration on the Tibetan Plateau. Sci Rep 7(1):1–11
Yang H et al (2017) Taxonomic resolution is a determinant of biodiversity effects in arbuscular mycorrhizal fungal communities. J Ecol 105(1):219–228
Funding
We are grateful for the financial support for this research provided by the McGill Sustainability Systems Initiative Ideas Fund, from the NSERC CREATE Climate-Smart Soils grant (#528274–2019). This work was also supported by a Discovery Grant (RGPIN-2015–06060) from the Natural Sciences and Engineering Council of Canada and a Canada Research Chair to PMA.
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CCAH, PMA, and CMK conceived and designed the study and CCAH carried out the experiment and collected and analyzed the experimental data. CCAH wrote the first draft of the manuscript with contributions from PMA and CMK. All authors contributed to the interpretation of the data and writing and revising manuscript drafts and are accountable for the accuracy and integrity of all aspects of the work.
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Horsch, C.C.A., Antunes, P.M. & Kallenbach, C.M. Arbuscular mycorrhizal fungal communities with contrasting life-history traits influence host nutrient acquisition. Mycorrhiza 33, 1–14 (2023). https://doi.org/10.1007/s00572-022-01098-x
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DOI: https://doi.org/10.1007/s00572-022-01098-x