Kadri Koorem

Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism

Cosmopolitan plant root symbionts The aboveground lives of plants are only sustainable because of the symbiotic soil fungi that encase their roots. These fungi swap nutrients with plants, defend them from attack, and help them withstand abrupt environmental changes. Out of necessity, fungal symbionts in the soil would appear to be restricted and local to certain plant species. Davison et al., however, discovered that some taxa are globally distributed. How these underground fungi have dispersed so widely remains a mystery; perhaps human farmers have had something to do with it. Science, this issue p. 970 The wide distribution of plant-root fungal symbionts seems to be driven by recent dispersal rather than ancient tectonics. The global biogeography of microorganisms remains largely unknown, in contrast to the well-studied diversity patterns of macroorganisms. We used arbuscular mycorrhizal (AM) fungus DNA from 1014 plant-root samples collected worldwide to determine the global distribution of these plant symbionts. We found that AM fungal communities reflected local environmental conditions and the spatial distance between sites. However, despite AM fungi apparently possessing limited dispersal ability, we found 93% of taxa on multiple continents and 34% on all six continents surveyed. This contrasts with the high spatial turnover of other fungal taxa and with the endemism displayed by plants at the global scale. We suggest that the biogeography of AM fungi is driven by unexpectedly efficient dispersal, probably via both abiotic and biotic vectors, including humans.

Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi.

We aimed to enhance understanding of the molecular diversity of arbuscular mycorrhizal fungi (AMF) by building a new global dataset targeting previously unstudied geographical areas. In total, we sampled 96 plant species from 25 sites that encompassed all continents except Antarctica. AMF in plant roots were detected by sequencing the nuclear SSU rRNA gene fragment using either cloning followed by Sanger sequencing or 454-sequencing. A total of 204 AMF phylogroups (virtual taxa, VT) were recorded, increasing the described number of Glomeromycota VT from 308 to 341 globally. Novel VT were detected from 21 sites; three novel but nevertheless widespread VT (Glomus spp. MO-G52, MO-G53, MO-G57) were recorded from six continents. The largest increases in regional VT number were recorded in previously little-studied Oceania and in the boreal and polar climatic zones — this study providing the first molecular data from the latter. Ordination revealed differences in AM fungal communities between different continents and climatic zones, suggesting that both biogeographic history and environmental conditions underlie the global variation of those communities. Our results show that a considerable proportion of Glomeromycota diversity has been recorded in many regions, though further large increases in richness can be expected in remaining unstudied areas.

Worldwide evidence of a unimodal relationship between productivity and plant species richness

Grassland diversity and ecosystem productivity The relationship between plant species diversity and ecosystem productivity is controversial. The debate concerns whether diversity peaks at intermediate levels of productivity—the so-called humped-back model—or whether there is no clear predictable relationship. Fraser et al. used a large, standardized, and geographically diverse sample of grasslands from six continents to confirm the validity and generality of the humped-back model. Their findings pave the way for a more mechanistic understanding of the factors controlling species diversity. Science, this issue p. 302 The humped-back model of plant species diversity is confirmed by a global grassland survey. The search for predictions of species diversity across environmental gradients has challenged ecologists for decades. The humped-back model (HBM) suggests that plant diversity peaks at intermediate productivity; at low productivity few species can tolerate the environmental stresses, and at high productivity a few highly competitive species dominate. Over time the HBM has become increasingly controversial, and recent studies claim to have refuted it. Here, by using data from coordinated surveys conducted throughout grasslands worldwide and comprising a wide range of site productivities, we provide evidence in support of the HBM pattern at both global and regional extents. The relationships described here provide a foundation for further research into the local, landscape, and historical factors that maintain biodiversity.

Soil Nutrient Content Influences the Abundance of Soil Microbes but Not Plant Biomass at the Small-Scale

Small-scale heterogeneity of abiotic and biotic factors is expected to play a crucial role in species coexistence. It is known that plants are able to concentrate their root biomass into areas with high nutrient content and also acquire nutrients via symbiotic microorganisms such as arbuscular mycorrhizal (AM) fungi. At the same time, little is known about the small-scale distribution of soil nutrients, microbes and plant biomass occurring in the same area. We examined small-scale temporal and spatial variation as well as covariation of soil nutrients, microbial biomass (using soil fatty acid biomarker content) and above- and belowground biomass of herbaceous plants in a natural herb-rich boreonemoral spruce forest. The abundance of AM fungi and bacteria decreased during the plant growing season while soil nutrient content rather increased. The abundance of all microbes studied also varied in space and was affected by soil nutrient content. In particular, the abundance of AM fungi was negatively related to soil phosphorus and positively influenced by soil nitrogen content. Neither shoot nor root biomass of herbaceous plants showed any significant relationship with variation in soil nutrient content or the abundance of soil microbes. Our study suggests that plants can compensate for low soil phosphorus concentration via interactions with soil microbes, most probably due to a more efficient symbiosis with AM fungi. This compensation results in relatively constant plant biomass despite variation in soil phosphorous content and in the abundance of AM fungi. Hence, it is crucial to consider both soil nutrient content and the abundance of soil microbes when exploring the mechanisms driving vegetation patterns.

Species-Specific Effects of Woody Litter on Seedling Emergence and Growth of Herbaceous Plants

The effect of litter on seedling establishment can influence species richness in plant communities. The effect of litter depends on amount, and also on litter type, but relatively little is known about the species-specific effects of litter. We conducted a factorial greenhouse experiment to examine the effect of litter type, using two woody species that commonly co-occur in boreonemoral forest—evergreen spruce (Picea abies), deciduous hazel (Corylus avellana), and a mixture of the two species—and litter amount—shallow (4 mm), deep (12 mm) and leachate—on seedling emergence and biomass of three understorey species. The effect of litter amount on seedling emergence was highly dependent on litter type; while spruce needle litter had a significant negative effect that increased with depth, seedling emergence in the presence of hazel broadleaf litter did not differ from control pots containing no litter. Mixed litter of both species also had a negative effect on seedling emergence that was intermediate compared to the single-species treatments. Spruce litter had a marginally positive (shallow) or neutral effect (deep) on seedling biomass, while hazel and mixed litter treatments had significant positive effects on biomass that increased with depth. We found non-additive effects of litter mixtures on seedling biomass indicating that high quality hazel litter can reduce the negative effects of spruce. Hazel litter does not inhibit seedling emergence; it increases seedling growth, and creates better conditions for seedling growth in mixtures by reducing the suppressive effect of spruce litter, having a positive effect on understorey species richness.

Arbuscular mycorrhizal fungal communities in forest plant roots are simultaneously shaped by host characteristics and canopy-mediated light availability

Background and aimsThe majority of terrestrial plant species associate with arbuscular mycorrhizal (AM) fungi, to exchange carbon compounds with nutrients. However, the factors that determine the composition of AM fungal communities in individual plant roots remain poorly understood. We hypothesized that AM fungal communities are simultaneously influenced by environmental conditions, such as light availability, and the photosynthetic capacity of host plant species.MethodsWe sampled individuals of shade-tolerant and shade-avoidant plant species, growing in the presence and absence of forest canopy, representing conditions of low and high light availability. We recorded photosynthetic parameters, shoot biomass and root AM fungal colonisation of these plant individuals and used 454-sequencing to characterise AM fungal communities in the roots of these plants.ResultsShade-avoidant plant species increased their photosynthetic capacity more than shade-tolerant plant species as a response to increased light availability due to canopy removal. Root AM fungal colonisation of all plants was higher when the forest canopy was absent, but canopy status had little influence on AM fungal richness in plant roots. The composition of AM fungal communities associating with shade-tolerant plants was significantly influenced by canopy status, while a less pronounced difference was observed among shade-avoidant plants.ConclusionsWe suggest that both environmental conditions and the ability of plant species to exploit available resources determine the dynamics of mutualistic associations between host plant species and AM fungal taxa.

Anthropogenic disturbance equalizes diversity levels in arbuscular mycorrhizal fungal communities

The arbuscular mycorrhizal (AM) symbiosis is a key plant-microbe interaction in sustainable functioning ecosystems. Increasing anthropogenic disturbance poses a threat to AM fungal communities worldwide, but there is little empirical evidence about its potential negative consequences. In this global study, we sequenced AM fungal DNA in soil samples collected from pairs of natural (undisturbed) and anthropogenic (disturbed) plots in two ecosystem types (10 naturally wooded and six naturally unwooded ecosystems). We found that ecosystem type had stronger directional effects than anthropogenic disturbance on AM fungal alpha and beta diversity. However, disturbance increased alpha and beta diversity at sites where natural diversity was low and decreased diversity at sites where natural diversity was high. Cultured AM fungal taxa were more prevalent in anthropogenic than natural plots, probably due to their efficient colonization strategies and ability to recover from disturbance. We conclude that anthropogenic disturbance does not have a consistent directional effect on AM fungal diversity; rather, disturbance equalizes levels of diversity at large scales and causes changes in community functional structure.

Microbial island biogeography: isolation shapes the life history characteristics but not diversity of root-symbiotic fungal communities

Island biogeography theory is one of the most influential paradigms in ecology. That island characteristics, including remoteness, can profoundly modulate biological diversity has been borne out by studies of animals and plants. By contrast, the processes influencing microbial diversity in island systems remain largely undetermined. We sequenced arbuscular mycorrhizal (AM) fungal DNA from plant roots collected on 13 islands worldwide and compared AM fungal diversity on islands with existing data from mainland sites. AM fungal communities on islands (even those >6000 km from the closest mainland) comprised few endemic taxa and were as diverse as mainland communities. Thus, in contrast to patterns recorded among macro-organisms, efficient dispersal appears to outweigh the effects of taxogenesis and extinction in regulating AM fungal diversity on islands. Nonetheless, AM fungal communities on more distant islands comprised a higher proportion of previously cultured and large-spored taxa, indicating that dispersal may be human-mediated or require tolerance of significant environmental stress, such as exposure to sunlight or high salinity. The processes driving large-scale patterns of microbial diversity are a key consideration for attempts to conserve and restore functioning ecosystems in this era of rapid global change.

Nematode community responses to range-expanding and native plant communities in original and new range soils

Abstract Many plant species expand their range to higher latitudes in response to climate change. However, it is poorly understood how biotic interactions in the new range differ from interactions in the original range. Here, in a mesocosm experiment, we analyze nematode community responses in original and new range soils to plant communities with either (a) species native in both the original and new range, (b) range‐expanding species related to these natives (related range expanders), or (c) range expanders without native congeneric species in the new range (unrelated range expanders). We hypothesized that nematode community shifts between ranges are strongest for unrelated range expanders and minimal for plant species that are native in both ranges. As a part of these community shifts, we hypothesized that range expanders, but not natives, would accumulate fewer root‐feeding nematodes in their new range compared to their original range. Analyses of responses of nematodes from both original and new ranges and comparison between range expanders with and without close relatives have not been made before. Our study reveals that none of the plant communities experienced evident nematode community shifts between the original and new range. However, in soils from the new range, root‐feeding nematode communities of natives and related range expanders were more similar than in soils from the original range, whereas the nematode community of unrelated range expanders was distinct from the communities of natives and related range expanders in soils from both ranges. The abundances of root‐feeding nematodes were comparable between the original and new range for all plant communities. Unexpectedly, unrelated range expanders overall accumulated most root‐feeding nematodes, whereas related range expanders accumulated fewest. We conclude that nematode communities associated with native and range‐expanding plant species differ between the original and the new range, but that range‐expanding plant species do not accumulate fewer root‐feeding nematodes in their new than in their original range.