Nancy Collins Johnson

Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales

Despite the fact that arbuscular mycorrhizal (AM) associations are among the most ancient, abundant and important symbioses in terrestrial ecosystems, there are currently few unifying theories that can be used to help understand the factors that control their structure and function. This review explores how a stoichiometric perspective facilitates integration of three complementary ecological and evolutionary models of mycorrhizal structure and function. AM symbiotic function should be governed by the relative availability of carbon, nitrogen and phosphorus (trade balance model) and allocation to plant and fungal structures should depend on the availabilities of these resources (functional equilibrium model). Moreover, in an evolutionary framework, communities of plants and AM fungi are predicted to adapt to each other and their local soil environment (co-adaptation model). Anthropogenic enrichment of essential resources in the environment is known to impact AM symbioses. A more predictive theory of AM structure and function will help us to better understand how these impacts may influence plant communities and ecosystem properties.

Resource limitation is a driver of local adaptation in mycorrhizal symbioses

Symbioses may be important mechanisms of plant adaptation to their environment. We conducted a reciprocal inoculation experiment to test the hypothesis that soil fertility is a key driver of local adaptation in arbuscular mycorrhizal (AM) symbioses. Ecotypes of Andropogon gerardii from phosphorus-limited and nitrogen-limited grasslands were grown with all possible “home and away” combinations of soils and AM fungal communities. Our results indicate that Andropogon ecotypes adapt to their local soil and indigenous AM fungal communities such that mycorrhizal exchange of the most limiting resource is maximized. Grasses grown in home soil and inoculated with home AM fungi produced more arbuscules (symbiotic exchange structures) in their roots than those grown in away combinations. Also, regardless of the host ecotype, AM fungi produced more extraradical hyphae in their home soil, and locally adapted AM fungi were, therefore, able to sequester more carbon compared with nonlocal fungi. Locally adapted mycorrhizal associations were more mutualistic in the two phosphorus-limited sites and less parasitic at the nitrogen-limited site compared with novel combinations of plants, fungi, and soils. To our knowledge, these findings provide the strongest evidence to date that resource availability generates evolved geographic structure in symbioses among plants and soil organisms. Thus, edaphic origin of AM fungi should be considered when managing for their benefits in agriculture, ecosystem restoration, and soil-carbon sequestration.

NITROGEN ENRICHMENT ALTERS MYCORRHIZAL ALLOCATION AT FIVE MESIC TO SEMIARID GRASSLANDS

Arbuscular mycorrhizal (AM) fungi are integral components of grasslands because most plants are associated with interconnected networks of AM hyphae. Mycorrhizae generally facilitate plant uptake of nutrients from the soil. However, mycorrhizal associations are known to vary in their mutualistic function, and there is currently no metric that links AM functioning with fungal colonization of roots. Mycorrhizal structures differ in their physiological and ecological functioning, so changes in AM allocation to intraradical (inside roots) and extraradical (in soil) structures may signal shifts in mycorrhizal function. We hypothesize that the functional equilibrium model applies to AM fungi and that fertilization should reduce allocation to arbuscules, coils, and extraradical hyphae, the fungal structures that are directly involved in nutrient acquisition and transfer to plants. This study compared AM responses to experimental N enrichment at five grasslands distributed across North America. Samples were collected from replicated N-enriched (and some P-enriched) and control plots throughout the growing season for three years. Intraradical AM structures were measured in over 1400 root samples, extraradical hyphal density was measured in over 590 soil samples, and spore biovolume was analyzed in over 400 soil samples. There were significant site × N interactions for spore biovolume, extraradical hyphae, intraradical hyphae, and vesicles. Nitrogen enrichment strongly decreased AM structures at Cedar Creek, the site with the lowest soil N:P, and it increased AM structures at Konza Prairie, the site with the highest soil N:P. As predicted by the functional equilibrium model, in soils with sufficient P, relative allocation to arbuscules, coils, and extraradical hyphae was generally reduced by N enrichment. Allocation to spores and hyphae was most sensitive to fertilization. At the mesic sites, this response was associated with a shift in the relative abundance of Gigasporaceae within AM fungal communities. This study demonstrates that N enrichment impacts mycorrhizal allocation across a wide range of grassland ecosystems. Such changes are important because they suggest an alteration in mycorrhizal functioning that, in turn, may impact plant community composition and ecosystem function.

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.

MYCORRHIZAL COMMUNITY DYNAMICS FOLLOWING NITROGEN FERTILIZATION: A CROSS‐SITE TEST IN FIVE GRASSLANDS

Arbuscular mycorrhizal fungi (AMF) are considered both ecologically and physiologically important to many plant communities. As a result, any alteration in AMF community structure following soil nitrogen (N) enrichment may impact plant community function and contribute to widespread changes in grassland productivity. We evaluated the responses of AMF communities to N fertilization (≥100 kg N·ha−1·yr−1) in five perennial grasslands within the Long-Term Ecological Research network to generate a broader understanding of the drivers contributing to AMF species richness and diversity with increasing soil N fertility, and subsequent effects to host-plant communities. AMF spore and hyphal community data at three mesic sites (Cedar Creek, Kellogg Biological Station, Konza Prairie) and two semiarid sites (Sevilleta, Shortgrass Steppe) were collected over two consecutive years and used to test four hypotheses about AMF responses to N fertilization. Under ambient soil N, plant annual net primary productivity and soi...

Direct and indirect influences of 8 yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem

We measured the influences of soil fertility and plant community composition on Glomeromycota, and tested the prediction of the functional equilibrium hypothesis that increased availability of soil resources will reduce the abundance of arbuscular mycorrhizal (AM) fungi. Communities of plants and AM fungi were measured in mixed roots and in Elymus nutans roots across an experimental fertilization gradient in an alpine meadow on the Tibetan Plateau. As predicted, fertilization reduced the abundance of Glomeromycota as well as the species richness of plants and AM fungi. The response of the glomeromycotan community was strongly linked to the plant community shift towards dominance by Elymus nutans. A reduction in the extraradical hyphae of AM fungi was associated with both the changes in soil factors and shifts in the plant community composition that were caused by fertilization. Our findings highlight the importance of soil fertility in regulating both plant and glomeromycotan communities, and emphasize that high fertilizer inputs can reduce the biodiversity of plants and AM fungi, and influence the sustainability of ecosystems.

Nitrogen fertilization alters the functioning of arbuscular mycorrhizas at two semiarid grasslands

The effects of nitrogen (N) fertilization on arbuscular mycorrhizas were studied at two semiarid grasslands with different soil properties and N-enrichment history (Shortgrass Steppe in Colorado, and Sevilleta National Wildlife Refuge in New Mexico). These sites are part of the National Science Foundations Long-Term Ecological Research Network. The experimental plots at Shortgrass Steppe were fertilized with ammonium nitrate (NH4NO3) from 1971 to 1975, and have not received additional N since then. The experimental plots at Sevilleta were also fertilized with NH4NO3, but were established in 1995, 2 years before the soils were used for this study. Greenhouse experiments were conducted to compare the growth response of local grasses to arbuscular mycorrhizal (AM) fungi from fertilized (FERT) and unfertilized (UNFERT) field soils, at each site. Two species per site were chosen, Bouteloua gracilis and Elymus elymoides from Shortgrass Steppe, and B. gracilis and B. eriopoda from Sevilleta. Plants were grown for 3 months at HIGH N and LOW N levels, with FERT or UNFERT soil inoculum and in a non-mycorrhizal condition. Fertilization with N altered the functioning of AM fungi at both sites. Grasses inoculated with AM fungi from UNFERT soils had the most tillers, greatest biomass and highest relative growth rates. There were no significant differences in the growth response of plants inoculated with AM fungi from FERT soils and the non-mycorrhizal controls. These results were consistent across sites and species except for the plants grown at LOW N in Sevilleta soils. These plants were deficient in N and phosphorus (P) and did not show growth enhancement in response to AM inoculation with either FERT or UNFERT soils. Percent root length colonized by AM fungi was not directly related to plant performance. However, enrichment with N consistently decreased root colonization by AM fungi in the grasses grown in soils from Shortgrass Steppe with high P availability (18.4 mg kg−1), but not in the grasses grown in Sevilleta soils with low P availability (6.6 mg kg−1). Our study supports the hypotheses that (1) fertilization with N alters the balance between costs and benefits in mycorrhizal symbioses and (2) AM fungal communities from N fertilized soils are less beneficial mutualists than those from unfertilized soils.

Untangling the biological contributions to soil stability in semiarid shrublands.

Communities of plants, biological soil crusts (BSCs), and arbuscular mycorrhizal (AM) fungi are known to influence soil stability individually, but their relative contributions, interactions, and combined effects are not well understood, particularly in arid and semiarid ecosystems. In a landscape-scale field study we quantified plant, BSC, and AM fungal communities at 216 locations along a gradient of soil stability levels in southern Utah, USA. We used multivariate modeling to examine the relative influences of plants, BSCs, and AM fungi on surface and subsurface stability in a semiarid shrubland landscape. Models were found to be congruent with the data and explained 35% of the variation in surface stability and 54% of the variation in subsurface stability. The results support several tentative conclusions. While BSCs, plants, and AM fungi all contribute to surface stability, only plants and AM fungi contribute to subsurface stability. In both surface and subsurface models, the strongest contributions to soil stability are made by biological components of the system. Biological soil crust cover was found to have the strongest direct effect on surface soil stability (0.60; controlling for other factors). Surprisingly, AM fungi appeared to influence surface soil stability (0.37), even though they are not generally considered to exist in the top few millimeters of the soil. In the subsurface model, plant cover appeared to have the strongest direct influence on soil stability (0.42); in both models, results indicate that plant cover influences soil stability both directly (controlling for other factors) and indirectly through influences on other organisms. Soil organic matter was not found to have a direct contribution to surface or subsurface stability in this system. The relative influence of AM fungi on soil stability in these semiarid shrublands was similar to that reported for a mesic tallgrass prairie. Estimates of effects that BSCs, plants, and AM fungi have on soil stability in these models are used to suggest the relative amounts of resources that erosion control practitioners should devote to promoting these communities. This study highlights the need for system approaches in combating erosion, soil degradation, and arid-land desertification.

Predicting community and ecosystem outcomes of mycorrhizal responses to global change

Mycorrhizal symbioses link the biosphere with the lithosphere by mediating nutrient cycles and energy flow though terrestrial ecosystems. A more mechanistic understanding of these plant-fungal associations may help ameliorate anthropogenic changes to C and N cycles and biotic communities. We explore three interacting principles: (1) optimal allocation, (2) biotic context and (3) fungal adaptability that may help predict mycorrhizal responses to carbon dioxide enrichment, nitrogen eutrophication, invasive species and land-use changes. Plant-microbial feedbacks and thresholds are discussed in light of these principles with the goal of generating testable hypotheses. Ideas to develop large-scale collaborative research efforts are presented. It is our hope that mycorrhizal symbioses can be effectively integrated into global change models and eventually their ecology will be understood well enough so that they can be managed to help offset some of the detrimental effects of anthropogenic environmental change.

Seven years of carbon dioxide enrichment, nitrogen fertilization and plant diversity influence arbuscular mycorrhizal fungi in a grassland ecosystem

• We tested the prediction that the abundance and diversity of arbuscular mycorrhizal (AM) fungi are influenced by resource availability and plant community composition by examining the joint effects of carbon dioxide (CO(2) ) enrichment, nitrogen (N) fertilization and plant diversity on AM fungi. • We quantified AM fungal spores and extramatrical hyphae in 176 plots after 7 yr of treatment with all combinations of ambient or elevated CO(2) (368 or 560 ppm), with or without N fertilization (0 or 4 g Nm(-2) ), and one (monoculture) or 16 host plant species (polyculture) in the BioCON field experiment at Cedar Creek Ecosystem Science Reserve, Minnesota, USA. • Extramatrical hyphal lengths were increased by CO(2) enrichment, whereas AM spore abundance decreased with N fertilization. Spore abundance, morphotype richness and extramatrical hyphal lengths were all greater in monoculture plots. A structural equation model showed AM fungal biovolume was most influenced by CO(2) enrichment, plant community composition and plant richness, whereas spore richness was most influenced by fungal biovolume, plant community composition and plant richness. • Arbuscular mycorrhizal fungi responded to differences in host community and resource availability, suggesting that mycorrhizal functions, such as carbon sequestration and soil stability, will be affected by global change.