Abstract
Aims
Arbuscular mycorrhizal (AM) fungi, a group of obligate symbionts of terrestrial plants, have a global distribution range. Yet, we lack concrete synthetic and empirical evidence that could reveal whether distinct ecological niches are distributed across Glomeromycota through determining linkages between environmental factors and the distribution of these taxa.
Methods
We have modelled the probability of occurrence of Gigasporaceae and Acaulosporaceae as a function of candidate environmental factors. These families are among the most common but non-ubiquitous taxa in AM-driven ecosystems. We have constructed our database using studies with a global scope and carried out our analysis through a logistic regression approach.
Results
The probability of occurrence of Acaulosporacae increased in acidic environments and soils with high bulk density. By contrast, a key factor that affected probability of occurrence of Gigasporaceae was precipitation.
Conclusions
Through the analysis of an unprecedentedly large amount of data we could infer that niche processes mediate occurrence of a group of fungi at scales broader than the local scale of the individual studies gathered in the analysed dataset. Knowledge of well-supported niche features could enhance discovery of new taxa of AM fungi, and would facilitate development of study designs with greater ecological realism.
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References
Adler PB, HilleRisLambers J, Levine JM (2007) A niche for neutrality. Ecol Lett 10:95–104
Amend AS, Seifert KA, Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19:5555–5565
Antunes PM, Koch AM, Morton JB, Rillig MC, Klironomos JN (2011) Evidence for functional divergence in arbuscular mycorrhizal fungi from contrasting climatic origins. New Phytol 189:507–514
Avis PG, Branco S, Tang Y, Mueller GM (2010) Pooled samples bias fungal community descriptions. Mol Ecol Resour 10:135–141
Baptista-Rosas PC, Hinojosa A, Riquelme M (2007) Ecological niche modeling of Coccidioides spp. in Western North American deserts. Ann NY Acad Sci 1111:35–46
Bartolomeesteban H, Schenck N (1994) Spore germination and hyphal growth of arbuscular mycorrhizal fungi in relation to soil aluminum saturation. Mycologia 86:217–226
Barton K (2011) MuMIn: multi-model inference. R package version 1.0.0. URL http://CRAN.R-project.org/package=MuMIn [accessed 10 October 2011]
Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-40. http://CRAN.R-project.org/package=lme4 [accessed 10 October 2011]
Brady NC, Weil RR (2008) The nature and properties of soils. Pearson Prentice Hall, New Jersey
Brito D (2010) Overcoming the Linnean shortfall: data deficiency and biological survey priorities. Basic Appl Ecol 11:709–713
Burke DJ (2008) Effects of Alliaria petiolata (Garlic mustard; Brassicaceae) on mycorrhizal colonisation and community structure in three herbaceous plants in a mixed deciduous forest. Am J Bot 95:1416–1425
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, Berlin
Caruso T, Hempel S, Powell JR, Barto EK, Rillig MC (2012) Compositional divergence and convergence in arbuscular mycorrhizal fungal communities. Ecology 93:1115–1124
Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. Chicago University Press, Chicago
Clark RB (1997) Arbuscular mycorrhizal adaptation, spore germination, root colonization, and host plant growth and mineral acquisition at low pH. Plant Soil 192:15–22
Clark JS (2012) The coherence problem with the unified neutral theory of biodiversity. Trends Ecol Evol 27:198–202
da Silva GA, Lumini E, Maia LC, Bonfante P, Bianciotto V (2006) Phylogenetic analysis of Glomeromycota by partial LSU rDNA sequences. Mycorrhiza 16:183–189
Dickie I, FitzJohn R (2007) Using terminal restriction fragment length polymorphism (T-RFLP) to identify mycorrhizal fungi: a methods review. Mycorrhiza 17:259–270
Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010a) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345
Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010b) 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
Egerton-Warburton LM, Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecol Appl 10:484–496
Egerton-Warburton LM, Johnson NC, Allen EB (2007) Mycorrhizal community dynamics following nitrogen fertilization: a cross-site test in five grasslands. Ecology 77:527–544
Fitzsimons MS, Miller RM, Jastrow JD (2008) Scale dependent niche axes of arbuscular mycorrhizal fungi. Oecologia 158:117–127
Gamper HA, Young JPW, Jones DL, Hodge A (2008) Real-time PCR and microscopy: are the two methods measuring the same unit of arbuscular mycorrhizal fungal abundance? Fungal Genet Biol 45:581–596
Grime JP, Hodgson JG, Hunt R (1990) The abridged comparative plant ecology. Chapman & Hall, London
Guo YJ, Ni Y, Raman H, Wilson BAL, Ash GJ, Wang AS, Li GD (2012) Arbuscular mycorrhizal fungal diversity in perennial pastures; responses to long-term lime application. Plant Soil 351:389–403
Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344
Helgason T, Fitter AH, Young JPW (1999) Molecular diversity of arbuscular mycorrhizal fungi colonizing Hyacinthoides non-scripta (bluebell) in a seminatural woodland. Mol Ecol 8:659–666
Helgason T, Merryweather JW, Young JPW, Fitter AH (2007) Specificity and resilience in the arbuscular mycorrhizal fungi of a natural woodland community. J Ecol 95:623–630
Hempel S, Renker C, Buscot F (2007) Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol 9:1930–1938
Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol and Evol 19:101–108
Johnson NC, Rowland DL, Corkidi L, Egerton-Warburton LM, Allen EB (2003) Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84:1895–1908
Klironomos JN, Hart MM (2002) Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculums. Mycorrhiza 12:181–184
Klironomos J, Zobel M, Tibbett M, Stock WD, Rillig MC, Parrent JL, Moora M, Koch AM, Facelli JM, Facelli E, Dickie IA, Bever JD (2011) Forces that structure plant communities: quantifying the importance of the mycorrhizal symbiosis. New Phytol 189:366–370
Lekberg Y, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95:95–105
Lekberg Y, Schnoor T, Kjøller R, Gibbons SM, Hansen LH, Al-Soud WA, Sørensen SJ, Rosendahl S (2011) 454-sequencing reveals stochastic local reassembly and high disturbance tolerance within arbuscular mycorrhizal fungal communities. J Ecol 100:151–160
MacKenzie DI, Nichols JD, Lachman GB, Droege S, Royle JA, Langtimm CA (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83:2248–2255
MacKenzie DI, Nichols JD, Hines JE, Knutson MG, Franklin AB (2003) Estimating site occupancy, colonization, and local extinction when a species is detected imperfectly. Ecology 84:2200–2207
MacKenzie DI, Nichols JD, Royle JA, Pollock KH, Bailey LL, Hines JE (2006) Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Elsevier, San Diego
Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748
Maherali H, Klironomos JN (2012) Phylogenetic and trait-based assembly of arbuscular mycorrhizal fungal communities. PlosOne 7:e36695
Morton J, Msiska Z (2010) Phylogenies from genetic and morphological characters do not support a revision of Gigasporaceae (Glomeromycota) into four families and five genera. Mycorrhiza 20:483–496
Nagekerke N (1991) A note on a general definition of the coefficient of determination. Biometrika 78:691–692
Nakagawa S, Freckleton RP (2011) Model averaging, missing data and multiple imputation: a case study for behavioural ecology. Behav Ecol Sociobiol 65:103–116
Oehl F, Sýkorová Z, Redecker D, Wiemken A, Sieverding E (2006) Acaulospora alpina, a new arbuscular mycorrhizal fungal species characteristic for high mountainous and alpine regions of the Swiss Alps. Mycologia 98:286–294
Oehl F, de Souza FA, Sieverding E (2008) Revision of Scutellospora and description of five new genera and three new families in the arbuscular mycorrhiza forming Glomeromycetes. Mycotaxon 106:311–360
Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241
Ponce RA, Águeda B, Ágreda T, Modrego MP, Aldea J, Fernández-Toirán LM, Martínez-Pena F (2011) Rockroses and Boletus edulis ectomycorrhizal association: realized niche and climatic suitability in Spain. Fungal Ecol 4:224–232
Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc Biol Sci 276:4237–4245
Powell JR, Monaghan MT, Öpik M, Rillig MC (2011) Evolutionary criteria outperform operational approaches in producing ecologically relevant fungal species inventories. Mol Ecol 20:655–666
R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reed KD, Meece JK, Archer JR, Peterson AT (2008) Ecologic niche modeling of Blastomyces dermatitidis in Wisconsin. PLoS One 3:e2034
Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754
Rosendahl S (2008) Communities, populations and individuals of arbuscular mycorrhizal fungi. New Phytol 178:253–266
Saxton KE, Rawls WJ, Romberger JS, Papendick RI (1986) Estimating generalized soil-water characteristics from texture. Soil Sci Soc Am J 50:1031–1036
Schenck NC, Peréz Y (1990) Manual for the identification of VA mycorrhizal fungi, 3rd edn. Synergistic, Cainesville
Schüßler A, Walker C (2010) The Glomeromycota. A species list with new families and new genera. Oregon State University, Gloucester
Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd Edition. Academic Press
Soberon J (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett 10:1115–1123
Sýkorová Z, Ineichen K, Wiemken A, Redecker D (2006) 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
Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363
Zalar P, Novak M, de Hoog GS, Gunde-Cimerman N (2011) Dishwashers—a man-made ecological niche accommodating human opportunistic fungal pathogens. Fungal Biol 115:997–1007
Zhu HH, Yao Q, Sun XT, Hu YL (2007) Colonization, ALP activity and plant growth promotion of native and exotic mycorrhizal fungi at low pH. Soil Biol Biochem 39:942–950
Acknowledgements
TC was supported by the Alexander von Humboldt Foundation. We thank Dr Jeff Powell and Dr Federico Luebert for comments on an earlier version of this manuscript.
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Responsible Editor: Duncan D. Cameron.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Esm 1
Sensitivity analysis and predictive models for Gigasporaceae and Acaulosporaceae (DOC 216 kb)
Esm 2
List of articles included in the database and their corresponding study codes. (PDF 89 kb)
Esm 3
Raw data used for the model construction (PDF 92 kb)
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Veresoglou, S.D., Caruso, T. & Rillig, M.C. Modelling the environmental and soil factors that shape the niches of two common arbuscular mycorrhizal fungal families. Plant Soil 368, 507–518 (2013). https://doi.org/10.1007/s11104-012-1531-x
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DOI: https://doi.org/10.1007/s11104-012-1531-x