Development of research methods to characterise arbuscular mycorrhizal fungal communities and potential effects of fungal endophyte biodiversity on vegetation
Abstract
Characterization and quantification of the functional and taxonomic diversity of microbial communities is essential for understanding all aspects of microbial ecology and is closely related to ecosystem function. Arbuscular mycorrhiza is the most widespread symbiosis on Earth, with arbuscular mycorrhizal (AM) fungi present in more than 2/3 of all plant species. Just over a decade after the publication of the first review article on molecular approaches to study the ecology of AM fungi in Acta Agriculturae Slovenica (Maček, 2009), the rapid development of molecular tools, especially next generation sequencing (NGS) technology, has accelerated the study of the research field of plant root endophytes. In this paper, the current approach to study the ecology and taxonomy of AM fungi is presented, which also provides some insights into the study of other plant root endophytes. In addition, a widely used system for classifying AM fungi with so-called virtual taxa (VT) is presented, which is used for ecological studies and comparison between different studies. Finally, a brief overview of the importance of climate and soil properties for AM fungal community composition and taxa distribution in global ecosystems is presented.
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Alzarhani, A.K., Clark, D.R., Underwood, G.J., Ford, H., Cotton, T.A., and Dumbrell, A.J. (2019). Are drivers of root-associated fungal community structure context specific? ISME Journal, 13, 1330–1344. https://doi.org/10.1038/s41396-019-0350-y
Besiana, S., Hoysted, G.A., Pressel, S., Bidartondo, M.I., and Field, K.J. (2021). Critical research challenges facing Mucoromycotina ‘fine root endophytes. New Phytologist, Forum, 1–7. https://doi.org/10.1111/nph.17684
Bouffaud, M.L., Creamer, R.E., Stone, D., Plassart, P., van Tuinen, D., Lemanceau, P., Wipf, D., and Redecker, D. (2016). Indicator species and co-occurrence in communities of arbuscular mycorrhizal fungi at the European scale. Soil Biology and Biochemistry, 103, 464–470. https://doi.org/10.1016/j.soilbio.2016.09.022
Błaszkowski J. (2012). Glomeromycota. W. Szafer Institute of Botany, Polish Academy of Sciences, Kraków., 300 pp.
Brachmann, A. and Parniske, M. (2006). The most widespread symbiosis on earth. PLoS Biol 4, e239. https://doi.org/10.1371/journal.pbio.0040239
Clapp, J.P., Helgason, T., Daniell, T.J., and Young, J.P.W. (2003). Chapter 8: Genetic studies of the structure and diversity of arbuscular mycorrhizal fungal communities. In: van der Heijden, M.G.A. and Sanders, I.R. (eds.). Mycorrhizal Ecology (Ecological Studies 157). Germany: Springer., pp. 201–221. https://doi.org/10.1007/978-3-540-38364-2_8
Corradi, N., Croll, D., Colard, A., Kuhn, G., Ehinger, M., and Sanders, I.R. (2007). Gene copy number polymorphisms in an arbuscular mycorrhizal fungal population. Applied an Environmental Microbiology, 73(1), 366–369. https://doi.org/10.1128/AEM.01574-06
Cotton, T.E., Dumbrell, A.J., Helgason, T. (2014). What goes in must come out: testing for biases in molecular analysis of arbuscular mycorrhizal fungal communities. PLoS One, 9(10), e109234, https://doi.org/10.1371/journal.pone.0109234
Davison, J., García de León, D., Zobel, M., Moora, M., Bueno, C.G., Barceló, M., Gerzm M., León, D., Meng, Y., Pillar, V.D., Sepp, S., Soudzilovaskaia, N.A., Tedersoo, L., Vaessen, S., Vahter, T., Winck, B., and Öpik, M. (2020). Plant functional groups associate with distinct arbuscular mycorrhizal fungal communities. New Phytologist, 226, 1117–1128.
https://doi.org/10.1111/nph.16423
Davison, J., Moora, M., Öpik, M., Adholeya, A., Ainsaar, L., Bâ, A., Burla, S., Diedhiou, A.G., Hiiesalu, I., Jairus, T., Johnson, N.C., Kane, A., Koorem, K., Kochar, M., Ndiaye, C., Pärtel, M., Reier, Ü., Saks, Ü., Singh, R., Vasar, M., and Zobel, M. (2015). Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science, 349, 970–973. https://doi.org/10.1126/science.aab1161
Davison, J. Moora, M., Semchenko, M., Adenan, S.B., Ahmed, T., Akhmetzhanova, A.A., Alatalo, J.M., Al-Quraishy, S., Andriyanova, E., Anslan, S., Bahram, M., Batbaatar, A., Brown, C., Bueno, C.G., Cahill, J., Cantero, J.J., Casper, B.B., Cherosov, M., Chideh, S., Coelho, A.P., Coghill, M., Decocq, G., Dudov, S., Fabiano, E..C., Fedosov, V.E., Fraser, L., Glassman, S.I., Helm, A., Henry, H.A.L., Hérault, B., Hiiesalu, I., Hiiesalu, I., Hozzein, W.N., Kohout, P., Kõljalg, U., Koorem, K., Laanisto, L., Mander, U., Mucina, L., Munyampundu, J., Neuenkamp, L., Niinemets, U., Nyamukondiwa, C., Oja, J., Onipchenko, V., Pärtel, M., Phosri, C., Põlme, S., Püssa, K., Ronk, A., Saitta, A., Semboli, O., Sepp, S., Seregin, A., Sudheer, S., Peña-Venegas, C.P., Paz, C., Vahter, T., Vasar, M., Veraart, A.J., Tedersoo, L., Zobel, M., and Öpik, M. (2021). Temperature and pH define the realised niche space of arbuscular mycorrhizal fungi. New Phytologist, 231, 763–776. https://doi.org/10.1111/nph.17240
Dickie, I.A. and FitzJohn, R.G. (2007). Using terminal restriction fragment length polymorphism (T-RFLP) to identify mycorrhizal fungi: a methods review. Mycorrhiza, 17, 259–270. https://doi.org/10.1007/s00572-007-0129-2
Dumbrell, A.J., Ashton, P.D., Aziz, N., Feng, G., Nelson, M., Dytham, C., Fitter, A.H., and Helgason, T. (2011). Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytologist, 190, 794–804. https://doi.org/10.1111/j.1469-8137.2010.03636.x
Dumbrell, A.J., Ferguson, R.M.W., and Clark, D.R. (2017). Microbial Community Analysis by Single-Amplicon High-Throughput Next Generation Sequencing: Data Analysis - From Raw Output to Ecology. In: McGenity, T.J., Timmis, K.N., and Nogales, B. (eds) Hydrocarbon and lipid microbiology protocols. Springer protocols handbooks. Springer, Heidelberg, pp. 155–206. https://doi.org/10.1007/8623_2016_228
Dumbrell, A.J., Nelson, M., Helgason, T., Dytham, C., and Fitter, A.H. (2010). Relative roles of niche and neutral processes in structuring a soil microbial community. ISME Journal, 4, 337–345. https://doi.org/10.1038/ismej.2009.122
Field, K.J., Rimington, W.R., Bidartondo, M.I., Allinson, K.E., Beerling, D.J., Cameron, D.D., Duckett, J.G., Leake, J.R., and Pressel, S. (2015). First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2. New Phytologist, 205, 743–756. https://doi.org/10.1111/nph.13024
Fitter, A.H. (2005). Darkness visible: reflections on underground ecology. Journal of Ecology, 93, 231–243. https://doi.org/10.1111/j.0022-0477.2005.00990.x
Hazard, C., Gosling. P., Van Der Gast, C.J., Mitchell, D.T., Doohan, F.M., and Bending, G.D. (2013). The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. ISME Journal, 7, 498–508. https://doi.org/10.1038/ismej.2012.127
Helgason T., Daniell T. J., Husband R., Fitter A. H., and Young J. P. W. (1998). Ploughing up the wood-wide web? Nature, 394, 431. https://doi.org/10.1038/28764
Helgason T., Merryweather J. W., Denison J., Wilson P., Young J. P. W., and 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
Helgason, T., Merryweather, J.W., Youngm J.P.W., and Fitter A.H. (2007). Specificity and resilience in the arbuscular mycorrhizal fungi of a natural woodland community. Journal of Ecology, 95, 623–630. https://doi.org/10.1111/j.1365-2745.2007.01239.x
Hoeksema, J.D., Bever, J.D., Chakraborty, S., Chaudhary, V.B., Gardes, M., Gehring, C.A., Hart, M.M., Housworth, E.A., Kaonongbua, W., Klironomos, J.N., Lajeunesse, M.J., Meadow, J., Milligan, B.G., Piculell, B.J., Pringle, A., Rúa, M.A., Umbanhowar, J., Viechtbauer, W., Wang, Y., Wilson, G.W.T, and Zee, P.C. (2018). Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism. Communications Biology, 1, 116. https://doi.org/10.1038/s42003-018-0120-9
Hoysted, G.A., Jacob, A.S., Kowal, J., Giesemann, P., Bidartondo, M.I., Duckett, J.G., Gebauer, G., Rimington, W.R., Schornack, S., Pressel, S., and Field, K.J. (2019). Mucoromycotina fine root endophyte fungi form nutritional mutualisms with vascular plants. Plant Physiology, 181, 565–577. https://doi.org/10.1104/pp.19.00729
Jansa, J., Smith, F.A., and Smith, S.E. (2008). Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytologist, 177, 779–789. https://doi.org/10.1111/j.1469-8137.2007.02294.x
Lee, J., Lee, S., and Young, J.P. (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
Lekberg, Y., Meadow, J., Rohr, J.R., Redecker, D., and Zabinski, C.A. (2011). Importance of dispersal and thermal environment for mycorrhizal communities: lessons from Yellowstone National Park. Ecology, 92, 1292–1302. https://doi.org/10.1890/10-1516.1
Kanagawa, T. (2003). Bias and artifacts in multitemplate polymerase chain reactions (PCR). Journal of Bioscience and Bioengineering, 96, 317–323. https://doi.org/10.1016/S1389-1723(03)90130-7
Kivlin, S.N., Hawkes, C.V., and Treseder, K.K. (2011). Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biology & Biochemistry, 43, 2294-2303. https://doi.org/10.1016/j.soilbio.2011.07.012
Knapp, D.G., Nemeth, J.B., Barry, K., Hainaut, M., Henrissat, B., Johnson, J., Kuo, A., Lim, J.H.P., Lipzen, A., Nolan, M., Ohm, R.A., Tamas, L., Grigoriev, I.V., Spatafora, J.W., Nagy, L.G., and Kovacs, G.M. (2018). Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi. Scientific Reports, 8, 6321. https://doi.org/10.1038/s41598-018-24686-4
Krüger, M., Stockinger, H., Krüger, C., and Schüssler, A. (2009). DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytologist, 183, 212–223. https://doi.org/10.1111/j.1469-8137.2009.02835.x
Maček, I. (2009). Molekulski pristopi pri raziskavah arbuskularne mikorize. Acta Agriculturae Slovenica, 93(1), 77–85.
Maček, I., Clark, D.R., Šibanc, N., Moser, G., Vodnik, D., Müller, C., and Dumbrell, A.J. (2019). Impacts of long-term elevated atmospheric CO2 concentrations on communities of arbuscular mycorrhizal fungi. Molecular Ecology, 28(14), 3445–3458. https://doi.org/10.1111/mec.15160
Maček, I., Dumbrell, A.J., Nelson, M., Fitter, A.H., Vodnik, D., and Helgason, T. (2011). Local adaptation to soil hypoxia determines the structure of an arbuscular mycorrhizal fungal community in roots from natural CO2 springs. Applied and Environmental Microbiology, 77(14), 4770–4777. https://doi.org/10.1128/AEM.00139-11
Moora, M., Berger, S., Davison, J., Öpik, M., Bommarco, R., Bruelheide, H., Kühn I, Kunin WE, Metsis M, Rortais A., Vanatoa, A., Vanatoa, E., Stout, J.C., Truusa, M., Westphal, C., Zobel, M., and Walther G. (2011). Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. Journal of Biogeography, 38, 1305–1317. https://doi.org/10.1111/j.1365-2699.2011.02478.x
Oehl, F., Laczko, E., Bogenrieder, A., Stahr, K., Bösch, R., van der Heijden, M., and Sieverding, E. (2010). Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biology & Biochemistry, 42, 724–738. https://doi.org/10.1016/j.soilbio.2010.01.006
Oehl, F., Sieverding, E., Palenzuela, J., Ineichen, K., and da Silva, G.A. (2011). Advances in Glomeromycota taxonomy and classification. IMA Fungus, 2, 191–199. https://doi.org/10.5598/imafungus.2011.02.02.10
Orchard, S., Standish, R.J., Dickie, I.A., Renton, M., Walker, C., Moot, D., and Ryan, M.H. (2017). Fine root endophytes under scrutiny: A review of the literature on arbuscule-producing fungi recently suggested to belong to the Mucoromycotina. Mycorrhiza, 27, 619–528. https://doi.org/10.1007/s00572-017-0782-z
Öpik, M. and Davison, J. (2016). Uniting species-and community-oriented approaches to understand arbuscular mycorrhizal fungal diversity. Fungal Ecology, 24, 106–113. https://doi.org/10.1016/j.funeco.2016.07.005
Öpik, M., Davison, J., Moora, M., and Zobel, M. (2014). DNA-based detection and identification of Glomeromycota: the virtual taxonomy of environmental sequences. Botany-Botanique, 92, 135–147. https://doi.org/10.1139/cjb-2013-0110
Öpik, M., Metsis, M., Daniell, T.J., Zobel, M., and Moora, M. (2009). Large-scale parallel 454 sequencing reveals ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytologist, 184, 424–437. https://doi.org/10.1111/j.1469-8137.2009.02920.x
Öpik, M., Moora, M., Liira, J., and Zobel, M. (2006). Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. Journal of Ecology, 94, 778–790. https://doi.org/10.1111/j.1365-2745.2006.01136.x
Öpik, M., Vanatoa, A., Vanatoa, E., Moora, M., Davison, J., Kalwij, J.M., Reier, U., and Zobel, M. (2010). The online database MaarjAM reveals global and ecosystem distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytologist, 188, 223–241. https://doi.org/10.1111/j.1469-8137.2010.03334.x
Öpik, M., Zobel, M., Cantero, J.J., Davison, J., Facelli, J.M., Hiiesalu, I., Jairus, T., Kalwij, J.M., Koorem, K., Leal, M.E., Liira, J., Metsis, M., Neshataeva, V., Paal, J., Phosri, C., Põlme, S., Reier, Ü., Saks, Ü., Orchard, S., Standish, R.J., Dickie, I.A., Renton, M., Walker, C., Moot, D., and Ryan, M.H. (2017). Fine root endophytes under scrutiny: a review of the literature on arbuscule-producing fungi recently suggested to belong to the Mucoromycotina. Mycorrhiza, 27, 619–638. https://doi.org/10.1007/s00572-017-0782-z
Powell, J.R., Parrent, J.L., Hart, M.M., Klironomos, J.N., Rillig, M.C., and Maherali, H. (2009). Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proceedings of the Royal Society of London B, 276, 4237–4245. https://doi.org/10.1098/rspb.2009.1015
Roberts, D.M., Schofield, P.G., Don, S., and Daniell, T.J. (2012). Directed terminal restriction analysis tool (DRAT): an aid to enzyme selection for directed terminal-restriction fragment length polymorphisms. Methods in Ecology and Evolution, 3(1), 24–28. https://doi.org/10.1111/j.2041-210X.2011.00139.x
Rodriguez, R.J., White, J.F., Arnold, A.E., and Redman, R.S. (2009). Fungal endophytes: diversity and functional roles. New Phytologist, 182, 314–330. https://doi.org/10.1111/j.1469-8137.2009.02773.x
Savary, R., Masclaux, F.G., Wyss, T., Droh. G., Corella, J.C., Machado, A.P., Morton, J.B., and Sanders, I.R. (2018). A population genomics approach shows widespread geographical distribution of cryptic genomic forms of the symbiotic fungus Rhizophagus irregularis. ISME Journal, 12, 17–30. https://doi.org/10.1038/ismej.2017.153
Schnitzer, S.A. and Klironomos, J. (2011). Soil microbes regulate ecosystem productivity and maintain species diversity. Plant Signaling & Behavior, 6-8, 1240–1243. https://doi.org/10.4161/psb.6.8.16455
Schwarzott, D. and Schüßler A. (2001). A simple and reliable method for SSU rRNA gene DNA extraction, amplification, and cloning from single AM fungal spores. Mycorrhiza, 10, 203–207. https://doi.org/10.1007/PL00009996
Simon, L., Lalonde, M., and Bruns, T.D. (1992). Specific amplification of 18S fungal ribosomal genes from vesicular arbuscular endomycorrhizal fungi colonising roots. Applied and Environmental Microbiology, 58, 291–295. https://doi.org/10.1128/aem.58.1.291-295.1992
Sinanaj, B., Hoysted, G.A., Pressel, S., Bidartondo, M.I., and Field, K.J. (2021). Critical research challenges facing Mucoromycotina ‘fine root endophytes’. New Phytologist. https://doi.org/10.1111/nph.17684
Smith, S.E and Read, D.J. (2008). Mycorrhizal Symbiosis, 3rd Edition. Academic Press, 800 pg.
Spatafora, J.W., Chang, Y., Benny,G.L., Lazarus, K., Smith, M.E., Berbee, M.L., Bonito, G., Corradi, N., Grigoriev, I., Gryganskyi, A, James, T.Y., O’Donnell, K., Roberson, R.W., Taylor, T.N., Uehling, J., Vilgalys, R., White, M.M., and Stajich, J.E. (2016). A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia, 108, 1028–1046. https://doi.org/10.3852/16-042
Sýkorová, Z., Ineichen., K., Wiemken, A., and Redecker, D. (2007). The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plants transplanted to the field, and from a greenhouse trap experiment. Mycorrhiza, 18, 1–14. https://doi.org/10.1007/s00572-007-0147-0
Tedersoo, L., Sánchez-Ramírez, S., Kõljalg, U., Bahram, M., Döring, M., Schigel, D., May, T., Ryberg, M., and Abarenkov, K. (2018). High-level classification of the Fungi and a tool for evolutionary ecological analyses. Fungal Diversity, 90, 135–159. https://doi.org/10.1007/s13225-018-0401-0
Tisserant, E., Malbreil, M., Kuo, A., Kohler, A., Symeonidi, A., Balestrini, R., Charron, P., Duensing, N., Frei Dit Frey, N., Gianinazzi-Pearson, V., Gilbert, L.B., Handa, Y., Herr, J.R., Hijri, M., Koul, R., Kawaguchi, M., Krajinski, F., Lammers, P.J., Masclaux, F.G., Murat, C., Morin, E., Ndikumana, S., Pagni, M., Petitpierre, D., Requena, N., Rosikiewicz, P., Riley, R., Saito, K., San Clemente, H., Shapiro, H., van Tuinen, D., Bécard, G., Bonfante, P., Paszkowski, U., Shachar-Hill, Y.Y., Tuskan, G.A., Young, P.W., Sanders, I.R., Henrissat, B., Rensing, S.A., Grigoriev, I.V., Corradi, N., Roux, C., and Martin, F. (2013). Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 110, 20117–20122. https://doi.org/10.1073/pnas.1313452110
Tonjer, L.R., Thoen, E., Morgado, L., Botnen, S., Mundra, S., Nybakken, L., Bryn, A., and Kauserud, H. (2021). Fungal community dynamics across a forest-alpine ecotone. Molecular Ecology, 30, 4926–4938. https://doi.org/10.1111/mec.16095
Vandenkoornhuyse, P., Husband, R., Daniell, T.J., Watson, I.J., Duck, J.M., Fitter, A.H., and Young, Y.P. (2002). Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Molecular Ecology, 11, 1555–1564. https://doi.org/10.1046/j.1365-294X.2002.01538.x
Větrovský, T., Kohout, P., Kopecký, M., Machac, A., Man, M., Bahnmann, B.D., Brabcová, V., Choi, J., Meszárošová, L., Human, Z.R., Lepinay, C., Lladó, S., López-Mondéjar, R., Martinović, T., Mašínová, T., Morais, D., Navrátilová, D., Odriozola, I., Štursová, M., Švec, K., Tláskal, V., Urbanová, M., Wan, J., Žifčáková, L., Howe, A., Ladau, J., Peay, K.G., Storch, D., Wild, J., and Baldrian, P. (2019). A meta-analysis of global fungal distribution reveals climate-driven patterns. Nature Communications, 10, 5142. https://doi.org/10.1038/s41467-019-13164-8
Wurzburger, N., Brookshire, E.N.J., Mccormack, M.L. and Lankau, R. (2017). Mycorrhizal fungi as drivers and modulators of terrestrial ecosystem processes. New Phytologist, 213(3), 996–999. https://doi.org/10.1111/nph.14409
Wheeler, D.A., Srinivasan, M., Egholm, M., Shen, Y., Chen, L., McGuire, A., He, W., Chen, Y., Makhijani, V., Roth, G.T., Gomes, X., Tartaro, K., Niazi, F., Turcotte, C.L., Irzyk, G.P., Lupski, J.R., Chinault, Xing-zhi Song, Yue Liu, Ye Yuan, Lynne Nazareth, Xiang Qin, Donna M. Muzny, Marcel Margulies, C., Weinstock, G.M., Gibbs, R.A., and Rothberg, J.M. (2008). The complete genome of an individual by massively parallel DNA sequencing. Nature, 452, 872–876. https://doi.org/10.1038/nature06884
DOI: http://dx.doi.org/10.14720/aas.2022.118.3.2419
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