Abstract
Despite the importance of arbuscular mycorrhizal (AM) fungi within terrestrial ecosystems, we know little about how natural AM fungal communities are structured. To date, the majority of studies examining AM fungal community diversity have focused on single habitats with similar environmental conditions, with relatively few studies having assessed the diversity of AM fungi over large-scale environmental gradients. In this study, we characterized AM fungal communities in the soil along a high-elevation gradient in the North American Rocky Mountains. We focused on phylogenetic patterns of AM fungal communities to gain insight into how AM fungal communities are naturally assembled. We found that alpine AM fungal communities had lower phylogenetic diversity relative to lower elevation communities, as well as being more heterogeneous in composition than either treeline or subalpine communities. AM fungal communities were phylogenetically clustered at all elevations sampled, suggesting that environmental filtering, either selection by host plants or fungal niches, is the primary ecological process structuring communities along the gradient.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agnarsson I, Cheng RC, Kuntner M (2014) A multi-clade test supports the intermediate dispersal model of biogeography. PLoS One 9:e86780. doi:10.1371/journal.pone.0086780
Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253. doi:10.1111/j.1541-0420.2005.00440.x
Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693. doi:10.1111/j.1461-0248.2006.00926.x
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. doi:10.1111/j.1462-2920.2005.00942.x
Bryant JA, Lamanna C, Morlon H et al (2008) Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci U S A 105:11505–11511. doi:10.1073/pnas.0801920105
Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi:10.1038/nmeth.f.303.QIIME
Caruso T, Hempel S, Powell JR et al (2012) Compositional divergence and convergence in arbuscular mycorrhizal fungal communities. Ecology 93:1115–1124. doi:10.1890/11-1030.1
Chagnon P-L, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491. doi:10.1016/j.tplants.2013.05.001
Chen J (2015) GUniFrac: generalized UniFrac distance package. R Packag. version 1.0
Chilvers G, Lapeyrie F, Horan D (1987) Ectomycorrhizal vs endomycorrhizal fungi within the same root system. New Phytol 107:441–448. doi:10.1111/j.1469-8137.1987.tb00195.x
Davison J, Öpik M, Zobel M et al (2012) Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. PLoS One 7:e141968. doi:10.1371/journal.pone.0041938
De Beenhouwer M, Van Geel M, Ceulemans T et al (2015) Changing soil characteristics alter the arbuscular mycorrhizal fungi communities of Arabica coffee (Coffea arabica) in Ethiopia across a management intensity gradient. Soil Biol Biochem 91:133–139. doi:10.1016/j.soilbio.2015.08.037
Dumbrell AJ, Nelson M, Helgason T et al (2010) Idiosyncrasy and overdominance in the structure of natural communities of arbuscular mycorrhizal fungi: is there a role for stochastic processes? J Ecol 98:419–428. doi:10.1111/j.1365-2745.2009.01622.x
Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113. doi:10.1186/1471-2105-5-113
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461
Egerton-Warburton LM, Johnson NC, Allen EB (2007) Mycorrhizal community dynamics following nitrogen fertilization: a cross-site test in five grasslands. Ecol Monogr 77:527–544
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. doi:10.1016/0006-3207(92)91201-3
Fierer N, Mccain CM, Meir P et al (2011) Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92:797–804. doi:10.1890/10-1170.1
Gai JP, Tian H, Yang FY et al (2012) Arbuscular mycorrhizal fungal diversity along a Tibetan elevation gradient. Pedobiologia (Jena) 55:145–151. doi:10.1016/j.pedobi.2011.12.004
Geml J, Pastor N, Fernandez L et al (2014) Large-scale fungal diversity assessment in the Andean Yungas forests reveals strong community turnover among forest types along an altitudinal gradient. Mol Ecol 23:2452–2472. doi:10.1111/mec.12765
Goberna M, García C, Verdú M (2014) A role for biotic filtering in driving phylogenetic clustering in soil bacterial communities. Glob Ecol Biogeogr 23:1346–1355. doi:10.1111/geb.12227
Gotelli NJ (2000) Null model analysis of species co-occurrence patterns. Ecology 81:2606–2621
Hart MM, Reader RJ (2002) Host plant benefit from association with arbuscular mycorrhizal fungi: variation due to differences in size of mycelium. Biol Fertil Soils 36:357–366. doi:10.1007/s00374-002-0539-4
Hazard C, Gosling P, van der Gast CJ et al (2013) The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. ISME J 7:498–508. doi:10.1038/ismej.2012.127
Helgason T, Daniell TJ, Husband R et al (1998) Ploughing up the wood-wide web? Nature 394:431. doi:10.1038/28764
Hervé M (2015) RVAideMemore. R Packag. version 0.9-54
Horn S, Caruso T, Verbruggen E et al (2014) Arbuscular mycorrhizal fungal communities are phylogenetically clustered at small scales. ISME J 8:2231–2242. doi:10.1038/ismej.2014.72
Horner-Devine MC, Bohannan BJM (2006) Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87:S100–S108. doi:10.1890/0012-9658(2006)87[100:PCAOIB]2.0.CO;2
Jankowski JE, Ciecka AL, Meyer NY, Rabenold KN (2009) Beta diversity along environmental gradients: implications of habitat specialization in tropical montane landscapes. J Anim Ecol 78:315–327. doi:10.1111/j.1365-2656.2008.01487.x
Kembel SW (2009) Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests. Ecol Lett 12:949–960. doi:10.1111/j.1461-0248.2009.01354.x
Kembel SW, Cowan PD, Helmus MR et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. doi:10.1093/bioinformatics/btq166
Kembel SW, Hubbell SP (2006) The phylogenetic structure of a neotropical forest tree community. Ecology 87:86–99. doi:10.1890/0012-9658(2006)87[86:TPSOAN]2.0.CO;2
Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303. doi:10.1016/j.soilbio.2011.07.012
Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301. doi:10.1890/02-0413
Klironomos JN, Kendrick WB (1995) Relationships among microartropods, fungi, and their environment. Plant Soil 170:183–197. doi:10.1007/BF02183066
Klironomos JN, Ursic M (1998) Density-dependent grazing on the extraradical hyphal network of the arbuscular mycorrhizal fungus, glomus intraradices, by the collembolan, Folsomia candida. Biol Fertil Soils 26:250–253. doi:10.1007/s003740050375
Kraft NJB, Comita LS, Chase JM et al (2011) Disentangling the drivers of beta diversity along latitudinal and elevational gradients. Science 333(80):1755–1758
Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47:583–624
Kunin V, Engelbrektson A, Ochman H, Hugenholtz P (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12:118–123. doi:10.1111/j.1462-2920.2009.02051.x
Lekberg Y, Hammer EC, Olsson PA (2010) Plants as resource islands and storage units—adopting the mycocentric viewofarbuscularmycorrhizal networks. FEMS Microbiol Ecol 74:336–345. doi:10.1111/j.1574-6941.2010.00956.x
Lekberg Y, Koide RT, Rohr JR et al (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95:95–105. doi:10.1111/j.1365-2745.2006.01193.x
Li X, Gai J, Cai X et al (2014) Molecular diversity of arbuscular mycorrhizal fungi associated with two co-occurring perennial plant species on a Tibetan altitudinal gradient. Mycorrhiza 24:95–107. doi:10.1007/s00572-013-0518-7
Liu L, Hart MM, Zhang J et al (2015a) Altitudinal distribution patterns of AM fungal assemblages in a Tibetan alpine grassland. FEMS Microbiol Ecol. doi:10.1093/femsec/fiv078
Liu Y, Johnson NC, Mao L et al (2015b) Phylogenetic structure of arbuscular mycorrhizal community shifts in response to increasing soil fertility. Soil Biol Biochem 89:196–205. doi:10.1016/j.soilbio.2015.07.007
Looby CI, Maltz MR, Treseder KK (2016) Belowground responses to elevation in a changing cloud forest. Ecol Evol 6:1996–2009. doi:10.1002/ece3.2025
Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316(80):1746–1748. doi:10.1126/science.1143082
Maherali H, Klironomos JN (2012) Phylogenetic and trait-based assembly of arbuscular mycorrhizal fungal communities. PLoS One 7:e36695. doi:10.1371/journal.pone.0036695
Mayfield MM, Levine JM (2010) Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol Lett 13:1085–1093. doi:10.1111/j.1461-0248.2010.01509.x
Moora M, Berger S, Davison J et al (2011) Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. J Biogeogr 38:1305–1317. doi:10.1111/j.1365-2699.2011.02478.x
Mueller RC, Bohannan BJM (2015) Shifts in the phylogenetic structure of arbuscular mycorrhizal fungi in response to experimental nitrogen and carbon dioxide additions. Oecologia 179:175–185. doi:10.1007/s00442-015-3337-z
Nagy L, Grabherr G (2009) The biology of alpine habitats. Oxford university press, Oxford
Narwani A, Matthews B, Fox J, Venail P (2015) Using phylogenetics in community assembly and ecosystem functioning research. Funct Ecol 29:589–591. doi:10.1111/1365-2435.12431
Oehl F, Sýkorová Z, Redecker D et al (2006) Acaulospora Alpina, a new arbuscular mycorrhizal fungal species characteristic for high mountainous and alpine regions of the Swiss alps. Mycologia 98:286–294. doi:10.3852/mycologia.98.2.286
Oksanen AJ, Blanchet FG, Kindt R, et al. (2015) Vegan: community ecology package. R Packag. version 2.3–1
Öpik M, Vanatoa A, Vanatoa E et al (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241. doi:10.1111/j.1469-8137.2010.03334.x
Öpik M, Zobel M, Cantero JJ et al (2013) Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23:411–430. doi:10.1007/s00572-013-0482-2
Powell JR, Parrent JL, Hart MM et al (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc R Soc B Biol Sci 276:4237–4245. doi:10.1098/rspb.2009.1015
Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12(1):38
Rambaut A (2012) FigTree version 1.4.2. http://tree.bio.ed.ac.uk/software/figtree/
Sabannavar SJ, Lakshman HC (2011) Synergistic interactions among Azotobacter, pseudomonas, and arbuscular mycorrhizal fungi on two varieties of Sesamum indicum L. Commun Soil Sci Plant Anal 42:2122–2133. doi:10.1111/j.1439-037X.2008.00338.x
Simon L, Lalonde M, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 58:291–295
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. doi:10.1093/bioinformatics/btl446
Stamatakis A, Ludwig T, Meier H (2005) RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456–463. doi:10.1093/bioinformatics/bti191
Swenson NG (2009) Phylogenetic resolution and quantifying the phylogenetic diversity and dispersion of communities. PLoS One 4:e4390. doi:10.1371/journal.pone.0004390
Swenson NG, Enquist BJ, Pither J et al (2006) The problem and promise of scale dependency in community phylogenetics. Ecology 87:2418–2424. doi:10.1890/0012-9658(2006)87[2418:TPAPOS]2.0.CO;2
Treseder KK, Cross A (2006) Global distributions of arbuscular mycorrhizal fungi. Ecosystems 9:305–316. doi:10.1007/s10021-005-0110-x
Wang J, Soininen J, He J, Shen J (2012) Phylogenetic clustering increases with elevation for microbes. Environ Microbiol Rep 4:217–226. doi:10.1111/j.1758-2229.2011.00324.x
Webb C (2000) Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am Nat 156:145–155. doi:10.1086/303378
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. doi:10.1146/annurev.ecolsys.33.010802.150448
Wilcoxon F (1945) Individual comparisons by ranking methods. Biometrics Bull 1:80–83. doi:10.2307/3001968
Xiang D, Verbruggen E, Hu Y et al (2014) Land use influences arbuscular mycorrhizal fungal communities in the farming—pastoral ecotone of northern China. New Phytol 204:968–978. doi:10.1111/nph.12961
Acknowledgements
We wish to thank the US National Park Service for the permission and access to the field sites. We also thank the Natural Sciences and Engineering Research Council of Canada for Discovery grants to MMH, JP and JK.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Egan, C.P., Callaway, R.M., Hart, M.M. et al. Phylogenetic structure of arbuscular mycorrhizal fungal communities along an elevation gradient. Mycorrhiza 27, 273–282 (2017). https://doi.org/10.1007/s00572-016-0752-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-016-0752-x