Foraging speed and precision of arbuscular mycorrhizal fungi under field conditions: An experimental approach
Language English Country Great Britain, England Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
32248586
DOI
10.1111/mec.15425
Knihovny.cz E-resources
- Keywords
- Claroideoglomeraceae, Glomeraceae, foraging precision, foraging speed, functional traits, soil nutrients,
- MeSH
- Glomeromycota * MeSH
- Fungi MeSH
- Plant Roots MeSH
- Humans MeSH
- Mycorrhizae * MeSH
- Soil MeSH
- Soil Microbiology MeSH
- Symbiosis MeSH
- Check Tag
- Humans MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Soil MeSH
To better understand the ecology of arbuscular mycorrhizal (AM) symbiosis, we need to measure functional traits of individual fungal virtual taxa under field conditions. The efficiency of AM fungi in locating nutrient-rich patches in soil space is one of their central traits in this symbiotic relationship. We used plots of a long-term field experiment in grassland with manipulated functional group composition of host plant community to establish ingrowth patches with substrate free of roots and fungi and with varying nutrient availability. Comparison of the original AM fungal community before patch creation with that present 9 weeks after patch establishment enabled us to estimate relative hyphal foraging speed for 41 fungal taxa, and a comparison of the fungal community in neighbouring patches differing in nutrient availability provided estimates of hyphal foraging precision for 22 taxa. Members of two dominant fungal families, Glomeraceae and Claroideoglomeraceae, differed in their foraging speed and precision. Glomeraceae taxa responded more slowly, but with a higher focus on enriched patches. We further demonstrated the usefulness of the obtained fungal functional traits by testing the differences between grass and dicotyledonous plant hosts using a data set obtained in another experiment at the same plots. Grass species hosted AM fungal communities with higher foraging speed, but lower foraging precision than the dicotyledonous species. Our study results support the use of field experiments for measuring comparative characteristics of AM fungi, which are highly elusive (or misrepresented) under controlled conditions.
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Anslan, S., Bahram, M., Hiiesalu, I., & Tedersoo, L. (2017). PipeCraft: Flexible open-source toolkit for bioinformatics analysis of custom high-throughput amplicon sequencing data. Molecular Ecology Resources, 17, e234-e240. https://doi.org/10.1111/1755-0998.12692
Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effect models using lme4. Journal of Statistical Software, 67, 1-48.
Brundrett, M. C., & Tedersoo, L. (2018). Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytologist, 220, 1108-1115. https://doi.org/10.1111/nph.14976
Bunn, R. A., Simpson, D. T., Bullington, L. S., Lekberg, Y., & Janos, D. P. (2019). Revisiting the 'direct mineral cycling' hypothesis: Arbuscular mycorrhizal fungi colonize leaf litter, but why? ISME Journal, 13, 1891-1898. https://doi.org/10.1038/s41396-019-0403-2
Cahill, J. F. Jr, & McNickle, G. G. (2011). The behavioral ecology of nutrient foraging by plants. Annual Review of Ecology, Evolution, and Systematics, 42, 289-311.
Campbell, B. D., Grime, J. P., & Mackey, J. M. L. (1991). A trade-off between scale and precision in resource foraging. Oecologia, 87, 532-538. https://doi.org/10.1007/BF00320417
Carrino-Kyker, S. R., Kluber, L. A., Petersen, S. M., Coyle, K. P., Hewins, C. R., DeForest, J. L., … Burke, D. J. (2016). Mycorrhizal fungal communities respond to experimental elevation of soil pH and P availability in temperate hardwood forests. FEMS Microbiology Ecology, 92, fiw024. https://doi.org/10.1093/femsec/fiw024
Chagnon, P. L., Bradley, R. L., & Klironomos, J. N. (2015). Trait-based partner selection drives mycorrhizal network assembly. Oikos, 124, 1609-1616. https://doi.org/10.1111/oik.01987
Chagnon, P. L., Bradley, R. L., Maherali, H., & Klironomos, J. N. (2013). A trait-based framework to understand life history of mycorrhizal fungi. Trends in Plant Science, 18, 484-491. https://doi.org/10.1016/j.tplants.2013.05.001
Chen, W., Koide, R. T., & Eissenstat, D. M. (2018). Nutrient foraging by mycorrhizas: From species functional traits to ecosystem processes. Functional Ecology, 32, 858-869. https://doi.org/10.1111/1365-2435.13041
Devi, S. G., Fathima, A. A., Radha, S., Arunraj, R., Curtis, W. R., & Ramya, M. (2015). A rapid and economical method for efficient DNA extraction from diverse soils suitable for metagenomic applications. PLoS ONE, 10, e0132441. https://doi.org/10.1371/journal.pone.0132441
Díaz, S., Symstad, A. J., Chapin, F. S. III, Wardle, D. A., & Huenneke, L. F. (2003). Functional diversity revealed by removal experiments. Trends in Ecology and Evolution, 18, 140-146. https://doi.org/10.1016/S0169-5347(03)00007-7
Doyle, J. J., & Doyle, J. L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin, 19, 11-15.
Dumbrell, A. J., Ashton, P. D., Aziz, N., Feng, G., Nelson, M., Dytham, C., … Helgasson, T. (2011). Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massive parallel pyrosequencing. New Phytologist, 190, 794-804.
Guindon, S., Dufavard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology, 59, 307-321. https://doi.org/10.1093/sysbio/syq010
Hart, M. M., & Reader, R. J. (2002). Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytologist, 153, 335-344. https://doi.org/10.1046/j.0028-646X.2001.00312.x
Hausmann, N. T., & Hawkes, C. V. (2009). Plant neighborhood control of arbuscular mycorrhizal community composition. New Phytologist, 183, 1188-1200. https://doi.org/10.1111/j.1469-8137.2009.02882.x
Helgason, T., Merryweather, J. W., Denison, J., Wilson, P., Young, J. P. W., & Fitter, A. H. (2002). Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. Journal of Ecology, 90, 371-384. https://doi.org/10.1046/j.1365-2745.2001.00674.x
Hodge, A., & Fitter, A. H. (2010). Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proceedings of the National Academy of Sciences, 107(31), 13754-13759. https://doi.org/10.1073/pnas.1005874107
Hutchings, M. J., & de Kroon, H. (1994). Foraging in plants: The role of morphological plasticity in resource acquisition. Advances in Ecological Research, 25, 159-238.
Jansa, J., Mozafar, A., & Frossard, E. (2005). Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant and Soil, 276, 163-176. https://doi.org/10.1007/s11104-005-4274-0
Jiang, S., Liu, Y., Luo, J., Qin, M., Johnson, N. C., Öpik, M., … Feng, H. (2018). Dynamics of arbuscular mycorrhizal fungal community structure and functioning along a nitrogen enrichment gradient in an alpine meadow ecosystem. New Phytologist, 220, 1222-1235. https://doi.org/10.1111/nph.15112
Johnson, D., Leake, J. R., & Read, D. J. (2001). Novel in-growth core system enables functional studies of grassland mycorrhizal mycelial networks. New Phytologist, 152, 555-562. https://doi.org/10.1046/j.0028-646X.2001.00273.x
Kubát, K., Hrouda, L., Chrtek, J., Kaplan, Z., Kirschner, J., & Štěpánek, J. (2002). Klíč ke květeně České republiky [Key to the Flora of Czech Republic]. Prague, Czech Republic: Academia.
Lee, J., Lee, S., & Young, J. P. W. (2008). Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiology Ecology, 65, 339-349. https://doi.org/10.1111/j.1574-6941.2008.00531.x
Legendre, P., & Legendre, L. (2012). Numerical ecology (3rd English edition). Amsterdam, The Netherlands: Elsevier.
Lekberg, Y., & Helgason, T. (2018). In situ mycorrhizal function - knowledge gaps and future directions. New Phytologist, 220, 957-962.
Liu, B., Li, L., Rengel, Z., Tian, J., Li, H., & Lu, M. (2019). Roots and arbuscular mycorrhizal fungi are independent in nutrient foraging across subtropical tree species. Plant and Soil, 442, 97-112. https://doi.org/10.1007/s11104-019-04161-3
López-García, A., Varela-Cervero, S., Vasar, M., Öpik, M., Barea, J. M., & Azcón-Aguilar, C. (2017). Plant traits determine the phylogenetic structure of arbuscular mycorrhizal fungal communities. Molecular Ecology, 26, 6948-6959. https://doi.org/10.1111/mec.14403
Maherali, H., & Klironomos, J. N. (2012). Phylogenetic and trait-based assembly of arbuscular mycorrhizal fungal communities. PLoS ONE, 7, e36695. https://doi.org/10.1371/journal.pone.0036695
Ohsowski, B. M., Zaitsoff, P. D., Öpik, M., & Hart, M. M. (2014). Where the wild things are: Looking for uncultured Glomeromycota. New Phytologist, 204, 171-179. https://doi.org/10.1111/nph.12894
Olsson, P. A., Jakobsen, I., & Wallander, H. (2002). Foraging and resource allocation strategies of mycorrhizal fungi in a patchy environment. In M. G. A. Van der Heijden, & J. Sanders (Eds.), Mycorrhizal ecology (pp. 93-115). Berlin, Germany: Springer-Verlag.
Olsson, P. A., & Wilhelmsson, P. (2000). The growth of external AM fungal mycelium in sand dunes and in experimental systems. Plant and Soil, 226, 161-169.
Öpik, M., Vanatoa, A., Vanatoa, E., Moora, M., Davison, J., Kalwij, J. M., … Zobel, M. (2010). The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytologist, 188, 223-241. https://doi.org/10.1111/j.1469-8137.2010.03334.x
Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401, 877-884. https://doi.org/10.1038/44766
Pinheiro, J. C., & Bates, D. M. (2000). Mixed-effect models in S and S-PLUS. New York, NY: Springer.
Powell, J. R., Parrent, J. L., Hart, M. M., Klironomos, J. N., Rillig, M. C., & Maherali, H. (2009). Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proceedings of the Royal Society, Series B, 276, 4237-4245. https://doi.org/10.1098/rspb.2009.1015
R Core Team (2018). R - A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217-223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Rodríguez, F., Oliver, J. L., Marin, A., & Medina, J. R. (1990). The general stochastic model of nucleotide substitution. Journal of Theoretical Biology, 142, 485-501. https://doi.org/10.1016/S0022-5193(05)80104-3
Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., … Weber, C. F. (2009). Introducing Mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied Environmental Microbiology, 75, 7537-7541. https://doi.org/10.1128/AEM.01541-09
Schüßler, A., Gehrig, H., Schwarzott, D., & Walker, C. (2001). Analysis of partial Glomales SSU rRNA genes: Implications for primer design and phylogeny. Mycological Research, 105, 5-15.
Simpson, G. L. (2009). Cocorresp: co-correspondence analysis ordination methods. R package version 0.3-0. https://cran.r-project.org/package=cocorresp.
Šmilauer, P., Košnar, J., Kotilínek, M., & Šmilauerová, M. (2020). Contrasting effects of host identity, plant community, and local species pool on the composition and colonization levels of arbuscular mycorrhizal fungal community in a temperate grassland. New Phytologist, 225, 461-473. https://doi.org/10.1111/nph.16112
Šmilauer, P., & Lepš, J. (2014). Multivariate analysis of ecological data using Canoco 5 (2nd edn.). Cambridge, UK: Cambridge University Press.
Šmilauer, P., & Šmilauerová, M. (2013). Asymmetric relationship between grasses and forbs: Results from a field experiment under nutrient limitation. Grass and Forage Science, 68, 186-198. https://doi.org/10.1111/j.1365-2494.2012.00888.x
Šmilauer, P., Šmilauerová, M., Kotilínek, M., & Košnar, J. (2020). Data of the study Foraging speed and precision of arbuscular mycorrhizal fungi under field conditions - an experimental approach. Dryad, https://doi.org/10.5061/dryad.1ns1rn8qs
Šmilauerová, M., & Šmilauer, P. (2006). Co-occurring graminoid and forb species do not differ in their root morphological response to soil heterogeneity. Folia Geobotanica, 41, 121-135. https://doi.org/10.1007/BF02806474
Šmilauerová, M., & Šmilauer, P. (2010). First come, first served: Grasses have a head start on forbs with prompt nutrient patch occupation. Plant and Soil, 328, 327-336. https://doi.org/10.1007/s11104-009-0112-0
Sylvia, D. J. (1992). Quantification of external hyphae of vesicular-arbuscular mycorrhizal fungi. In M. J. R. Norris, D. J. Read, & A. K. Varma (Eds.), Methods in Microbiology (pp. 53-65). London, UK: Academic Press.
Ter Braak, C. J. F., & Šmilauer, P. (2018). Canoco reference manual and user's guide: Software for ordination (version 5.10). Ithaca, NY: Microcomputer Power.
Unger, S., Friede, M., Hundacker, J., Volkmar, K., & Beyschlag, W. (2016). Allocation trade-off between root and mycorrhizal surface defines nitrogen and phosphorus relations in 13 grassland species. Plant and Soil, 407, 279-292. https://doi.org/10.1007/s11104-016-2994-y
Vasar, M., Andreson, R., Davison, J., Jairus, T., Moora, M., Remm, M., … Öpik, M. (2017). Increased sequencing depth does not increase captured diversity of arbuscular mycorrhizal fungi. Mycorrhiza, 27, 761-773. https://doi.org/10.1007/s00572-017-0791-y
Verbylaité, R., Beišys, P., Rimas, V., & Kuusiené, S. (2010). Comparison of ten DNA extraction protocols from wood of European Aspen (Populus tremula L.). Baltic Forestry, 16, 35-42.
Verhoeven, K. J. F., Simonsen, K. L., & McIntyre, L. M. (2005). Implementing false discovery rate control: Increasing your power. Oikos, 108, 643-647. https://doi.org/10.1111/j.0030-1299.2005.13727.x
Větrovský, T., Baldrian, P., & Morais, D. (2018). SEED 2: A user-friendly platform for amplicon high-throughput sequencing data analyses. Bioinformatics, 34, 2292-2294. https://doi.org/10.1093/bioinformatics/bty071
Zheng, C., Chai, M., Jiang, S., Zhang, S., Christie, P., & Zhang, J. (2015). Foraging capability of extraradical mycelium of arbuscular mycorrhizal fungi to soil phosphorus patches and evidence of carry-over effect on new host plant. Plant and Soil, 387, 201-217. https://doi.org/10.1007/s11104-014-2286-3
Dryad
10.5061/dryad.1ns1rn8qs