Global diversity and distribution of arbuscular mycorrhizal fungi

Abstract

Arbuscular mycorrhizal (AM) fungi form associations with most land plants and can control carbon, nitrogen, and phosphorus cycling between above- and belowground components of ecosystems. Current estimates of AM fungal distributions are mainly inferred from the individual distributions of plant biomes, and climatic factors. However, dispersal limitation, local environmental conditions,and interactions among AM fungal taxa may also determine local diversity and global distributions. We assessed the relative importance of these potential controls by collecting 14,961 DNA sequences from 111 published studies and testing for relationships between AM fungal community composition and geography, environment, and plant biomes. Our results indicated that the global species richness of AM fungi was up to six times higher than previously estimated, largely owing to high beta diversity among sampling sites. Geographic distance, soil temperature and moisture, and plant community type were each significantly related to AM fungal community structure, but explained only a small amount of the observed variance. AM fungal species also tended to be phylogenetically clustered within sites, further suggesting that habitat filtering or dispersal limitation is a driver of AM fungal community assembly. Therefore, predicted shifts in climate and plant species distributions under global change may alter AM fungal communities.

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.