Global diversity and distribution of arbuscular mycorrhizal fungi
Highlights
► We synthesize how dispersal, and abiotic and biotic interactions affect AM fungi. ► Diversity of AM fungi was six times higher than previously estimated. ► Distance, soils, and plant communities each affected AM fungal composition. ► AM fungal species also tended to be phylogenetically clustered within sites.
Introduction
The relative importance of dispersal limitation, environmental filtering, biotic interactions, and neutral processes for structuring biological communities remains unresolved for many organisms (Hubbell, 2001, Leibold et al., 2004). Moreover, although much work has documented spatial, environmental, and biological mechanisms that limit the distributions of plants and animals (Lomolino et al., 2005), the roles of these factors in microbial biogeography are less clear (Martiny et al., 2006). Some microorganisms exhibit species-area relationships and co-occurrence patterns that are equivalent to those of macroorganisms (Horner-Devine et al., 2004, Horner-Devine et al., 2007, Peay et al., 2007), while other microbial taxa have more cosmopolitan distributions (Fenchel and Finlay, 2005, Finlay, 2002). In particular, the biogeography of mycorrhizal fungi remains relatively unknown at the global scale despite recent advances in understanding global distributions of other microorganisms (Horner-Devine et al., 2004, Martiny et al., 2006).
Arbuscular mycorrhizal (AM) fungi colonize ∼75% of plant species (Newman and Reddell, 1987) and provide numerous benefits to their hosts, including increased N and P acquisition, drought tolerance, and pathogen protection (Auge, 2001, Johnson et al., 2010, Sikes et al., 2009). In these associations, AM fungi receive up to 30% of the host’s photosynthate (Drigo et al., 2010). In addition, AM fungal taxa can differ in their influences on net primary productivity (NPP), plant competition, aboveground plant diversity, and higher trophic levels (Mack and Rudgers, 2008, Maherali and Klironomos, 2007, Pearson and Jakobsen, 1993, Sikes et al., 2009, Sikes et al., 2010, van der Heijden et al., 2008, van der Heijden et al., 1998).
Given that AM fungi are best known for their relationships with plants, it is perhaps not surprising that current AM fungal biogeography is primarilydefined by the global distribution of known plant hosts and plant-defined biomes (Allen et al., 1995, Öpik et al., 2010). For instance, AM fungal communities are expected to dominate grasslands, but not boreal forests (Allen et al., 1995, Read, 1991). Indeed, the biomass and community composition of AM fungi differ with respect to biome, invasive plants, and plant species richness (Hawkes et al., 2006, Helgason et al., 2002, Kivlin and Hawkes, 2011, Öpik et al., 2006, Treseder and Cross, 2006), supporting the idea that spatial variation in plant community structure at many scales influences the distribution of AM fungal taxa.
Dispersal limitation, environmental filtering, and biotic interactions between AM fungal taxa, however, may also contribute to their biogeography (Dumbrell et al., 2010, Lekberg et al., 2007). Arbuscular mycorrhizal fungi produce relatively large spores (up to ∼640 μm) that are mainly wind or animal dispersed over intermediate ranges (<2 km); their hyphae can be dispersed over smaller areas (<10 m) (Mangan and Adler, 2000, Warner et al., 1987). Both can restrict the range of AM species. Nevertheless, the recent human-mediated introduction of microorganisms in soil and plant inoculum could result in large-scale dispersal of AM fungi (Schwartz et al., 2006, Vellinga et al., 2009). Distributions of arbuscular mycorrhizal fungi are also affected by many environmental parameters. For example, soil type and texture, disturbance, moisture, temperature, and nutrient availability are often correlated with AM fungal composition (Hawkes et al., 2011, Lekberg et al., 2007, Pringle and Bever, 2002, Rillig et al., 2002).
Trade-offs in phylogenetically-conserved traits have occurred during the evolution of the Glomeromycota lineage, affecting the growth of the fungus and plant host (Hart and Reader, 2002, Koide, 2000, Maherali and Klironomos, 2007, Powell et al., 2009), For example, Hart and Reader (2002) demonstrated that members of the Gigasporaceae family preferentially produce extraradical hyphal biomass in the soil, while members of the Glomeraceae family extensively colonize roots. These trade-offs in hyphal traits contribute to higher nutrient acquisition and biomass of plants in symbiosis with Gigasporaceae species, and greater pathogen protection of plants that associate with Glomeraceae species (Powell et al., 2009). They are also hypothesized to affect AM distributions; Glomeraceae species are expected to be prevalent in high nutrient soils while Gigasporaceae are predicted to dominate in low nutrient conditions (Treseder, 2005). These long-existing trade-offs may also lead to interactions between AM fungal taxa that could affect community assembly. If traits are phylogenetically conserved, competitive exclusion between closely related AM fungi could lead to a community in which species are less related than expected by chance (i.e., phylogenetic overdispersion). Alternatively, if environmental filtering or dispersal limitation selects for these traits, species within AM fungal communities could be more closely related than expected by chance (i.e., phylogenetic clustering) (Webb et al., 2002).
Arbuscular mycorrhizal fungi are often considered generalists, since only 200–300 species have been described to date (Öpik et al., 2010, Schüßler and Walker, 2010). However, current estimates of AM fungal diversity are largely based on spore morphology (Morton, 1988), which does not always separate genetically distinct taxa (Hijri and Sanders, 2005). Molecular surveys of AM fungi at the regional scale or larger are uncommon and have thus-far been restricted to only one gene (18S) in the most abundant taxa (Dumbrell et al., 2010, Öpik et al., 2006, Öpik et al., 2010). For example, Öpik et al. (2010), discovered that the distributions of the majority of AM fungal taxa are affected by associations with broad plant lineages or climate zones (i.e., tropical vs. temperate regions), but were unaffected by latitude, elevation or plant species richness. Here we expand upon these approaches by comparing the relative influence of spatial, environmental, and biotic drivers on global AM fungal distributions and examining how these factors, along with phylogenetic trait conservation, can structure local AM fungal communities. To our knowledge, our study is the first to examine how AM fungal community composition relates to soil characteristics and phylogenetic history on the global scale. We independently confirmed our analyses by comparing two genetic loci; the 18S and 28S genes.
We conducted a synthesis of published DNA sequences to determine controls over AM fungal distributions and community composition on the global scale. We hypothesized that AM fungi would be dispersal limited, owing to large spore size and belowground spore production. In addition, we predicted that AM fungal community composition would vary as a function of climate, soil characteristics, and plant community type. We predicted that local AM fungal communities would be phylogenetically clustered if environmental selection or dispersal limitation controlled community assembly, or overdispersed if interactions between fungal taxa were prevalent. We hypothesized that if AM fungi were influenced by one or more of these filters, community composition would differ significantly between sites (i.e., exhibit high beta diversity), perhaps leading to higher global diversity than previously estimated. Our analysis differs from other recent approaches in that we focus on how community-level interactions (based on phylogenetic history) affect AM fungal distributions and compare the relative strengths of abiotic, biotic and spatial drivers affecting community assembly patterns.
Section snippets
Sequence collection
Fungal 18S and 28S sequences were compiled from GenBank using the search terms of “soil, grassland, litter, tundra, agriculture, marsh, permafrost, forest, or desert” and “fung*”. All sequences were downloaded by 03/15/2010. We only included sequences collected from natural habitats that had not been manipulated by fertilization, tillage or heavy metal disturbances. We collected 9905 18S and 5056 28S Glomeromycota sequences from both published and unpublished sources. All non-identical
AM fungal richness
AM fungal richness was high in our dataset, with 563 OTUs and 669 OTUs observed for the 18S and 28S datasets, respectively, at the 97% similarity cutoff. At the 99% similarity cutoff, we observed 967 OTUs in the 18S region and 1159 OTUs in the 28S region. At the 97% similarity cutoff, the average OTU richness at each site (alpha diversity) was 15.39 (±1.30) OTUs for 18S and 21.40 (±3.29) OTUs for 28S. At the 99% similarity cutoff, alpha diversity increased marginally to 17.57 (±1.51) OTUs for
Discussion
Arbuscular mycorrhizal fungal diversity in our study was higher than previously observed in morphological and molecular surveys: up to three times higher at the 97% similarity level and six times higher at the 99% similarity level (Öpik et al., 2010, Schüßler and Walker, 2010). However, these high estimates were not due to high species richness within study sites; alphadiversity within sites was typically less than 25 OTUs. Instead, taxa were site-specific, leading to high beta diversity
Conclusions
Overall, we found evidence for substantial differences in AM fungal communities among locations, which resulted in high richness of AM fungal taxa at the global scale. Dispersal limitation, host plant communities, and other environmental factors could contribute to the high variability of AM fungi between sites. Furthermore, environmental filtering and dispersal limitation seemed to influence local AM fungal community assembly patterns.
High turnover between AM fungal communities is of
Acknowledgements
J.B.H. Martiny, S.D. Allison, N.A. Hynson, J.M. Talbot, S.R. Dooley, and three anonymous reviewers provided invaluable comments on earlier versions of this manuscript. This publication was developed under STAR Fellowship Assistance Agreement no. FP917191-01-0 awarded by the U.S. Environmental Protection Agency (EPA) to SNK. It has not been formally reviewed by the EPA. The views expressed in this publication are solely those of the authors and EPA does not endorse any products or commercial
References (90)
- et al.
Basic local alignment search tool
Journal of Molecular Biology
(1990) - et al.
On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages
Journal of Experimental Marine Biology and Ecology
(2006) Rote of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation
Journal of Trace Elements in Medicine and Biology
(2005)- et al.
Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation
Chemosphere
(2000) - et al.
Patterns and regulation of mycorrhizal plant and fungal diversity
Plant and Soil
(1995) - et al.
Warming and drying suppress microbial activity and carbon cycling in boreal forest soils
Global Change Biology
(2008) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis
Mycorrhiza
(2001)- et al.
Two invasive plants alter soil microbial community composition in serpentine grasslands
Biological Invasions
(2006) - et al.
Soil microbial community associated with an invasive grass differentially impacts native plant performance
Microbial Ecology
(2008) - et al.
Arbuscular mycorrhizal fungi: more diverse than meets the eye, and the ecological tale of why
Bioscience
(2001)
Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability
New Phytologist
Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2
Proceedings of the National Academy of Sciences of the United States of America
Idiosyncrasy and overdominance in the structure of natural communities of arbuscular mycorrhizal fungi: is there a role for stochastic processes?
Journal of Ecology
Bacteria and island biogeography
Science
Global dispersal of free-living microbial eukaryote species
Science
Interactions between mycorrhizal fungi and other soil organisms
Plant and Soil
An integrated biosphere model of land surface processes, terrestrial carbon balance, and vegetation dynamics
Global Biogeochemical Cycles
Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi
New Phytologist
Species-rich but distinct arbuscular mycorrhizal communities in reforestation plots on degraded pastures and in neighboring pristine tropical mountain rain forest
Tropical Ecology
Plant neighborhood control of arbuscular mycorrhizal community composition
New Phytologist
Order of plant host establishment alters the composition of arbuscular mycorrhizal communities
Ecology
Arbuscular mycorrhizal assemblages in native plant roots change in the presence of invasive exotic grasses
Plant and Soil
Soil temperature affects carbon allocation within arbuscular mycorrhizal networks and carbon transport from plant to fungus
Global Change Biology
Fungal community responses to precipitation
Global Change Biology
Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland
Journal of Ecology
Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity
Molecular Ecology
Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei
Nature
A taxa–area relationship for bacteria
Nature
A comparison of taxon co-occurrence patterns for macro and microorganisms
Ecology
The Unified Neutral Theory of Biodiversity and Biogeography
Molecular diversity of arbuscular mycorrhizal fungi and patterns of associations over time and space in a tropical forest
Molecular Ecology
Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands
Ecology
Resource limitation is a driver of local adaptation in mycorrhizal symbioses
Proceedings of the National Academy of Sciences of the United States of America
Picante: R tools for integrating phylogenies and ecology
Bioinformatics
Differentiating between effects of invasion and diversity: impacts of aboveground plant communities on belowground fungal communities
New Phytologist
Variation in plant response to native and exotic arbuscular mycorrhizal fungi
Ecology
Interspecific differences in the tolerance of arbuscular mycorrhizal fungi to freezing and drying
Canadian Journal of Botany
Functional complementarity in the arbuscular mycorrhizal symbiosis
New Phytologist
VA mycorrhizae in strand vegetation of Hawaii: evidence for long-distance codispersal of plants and fungi
American Journal of Botany
Testing the performance of a dynamic global ecosystem model: water balance, carbon balance, and vegetation structure
Global Biogeochemical Cycles
Spatial autocorrelation: trouble or new paradigm?
Ecology
The metacommunity concept: a framework for multi-scale community ecology
Ecology Letters
Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities
Journal of Ecology
Rapid and accurate large-scale coestimation of sequence alignments and phylogenetic trees
Science
Cited by (350)
Lithology and niche habitat have significant effect on arbuscular mycorrhizal fungal abundance and their interspecific interactions
2024, Science of the Total EnvironmentMycorrhizal ecology would benefit from region-specific hypotheses
2023, PedobiologiaEffects of land-use type on soil organic carbon and carbon pool management index through arbuscular mycorrhizal fungi pathways
2023, Global Ecology and Conservation