R. Michael Miller

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.

Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems.

Arbuscular mycorrhizal fungi (AMF) play an important role in regulating carbon fluxes between the biosphere and the atmosphere. A recent study showed that live hyphae can turn over rapidly, in five to six days on average, suggesting that carbon flow to AMF hyphae might be respired back to the atmosphere quickly. However, that study gives a limited view of the residence time of AMF hyphae in soils. AMF hyphae can also contribute to soil carbon storage through other mechanisms.

The GAAS Metagenomic Tool and Its Estimations of Viral and Microbial Average Genome Size in Four Major Biomes

Metagenomic studies characterize both the composition and diversity of uncultured viral and microbial communities. BLAST-based comparisons have typically been used for such analyses; however, sampling biases, high percentages of unknown sequences, and the use of arbitrary thresholds to find significant similarities can decrease the accuracy and validity of estimates. Here, we present Genome relative Abundance and Average Size (GAAS), a complete software package that provides improved estimates of community composition and average genome length for metagenomes in both textual and graphical formats. GAAS implements a novel methodology to control for sampling bias via length normalization, to adjust for multiple BLAST similarities by similarity weighting, and to select significant similarities using relative alignment lengths. In benchmark tests, the GAAS method was robust to both high percentages of unknown sequences and to variations in metagenomic sequence read lengths. Re-analysis of the Sargasso Sea virome using GAAS indicated that standard methodologies for metagenomic analysis may dramatically underestimate the abundance and importance of organisms with small genomes in environmental systems. Using GAAS, we conducted a meta-analysis of microbial and viral average genome lengths in over 150 metagenomes from four biomes to determine whether genome lengths vary consistently between and within biomes, and between microbial and viral communities from the same environment. Significant differences between biomes and within aquatic sub-biomes (oceans, hypersaline systems, freshwater, and microbialites) suggested that average genome length is a fundamental property of environments driven by factors at the sub-biome level. The behavior of paired viral and microbial metagenomes from the same environment indicated that microbial and viral average genome sizes are independent of each other, but indicative of community responses to stressors and environmental conditions.

Mycorrhizal status of the genus Carex (Cyperaceae)

The Cyperaceae have generally been considered nonmycorrhizal, although recent evidence suggests that mycotrophy may be considerably more widespread among sedges than was previously realized. This study surveyed 23 species of Carex occurring in upland and wetland habitats in northeastern Illinois. Mycorrhizal infection by arbuscular fungi was found in the roots of 16 species of Carex and appears to occur in response to many factors, both environmental and phylogenetic. While some species appear to be obligately nonmycorrhizal, edaphic influences may be responsible for infection in others. In five of the seven Carex species that were nonmycorrhizal, a novel root character, the presence of bulbous-based root hairs, was identified. The taxonomically patchy distribution of the distinctive root hair trait suggests that these structures may have evolved several times within the genus. Evidence of multiple independent origins of the root hair trait lends support to the hypothesis that root hairs represent an adaptation to nonmycotrophy. Although taxonomic position does seem to be of importance in determining the mycorrhizal dependence of sedges, the pattern may be a patchwork of both mycorrhizal clades and clades that have adapted to the nonmycorrhizal state.

Evidence of a mycorrhizal mechanism for the adaptation of Andropogon gerardii (Poaceae) to high- and low-nutrient prairies

Andropogon gerardii seed obtained from Kansas and Illinois was grown in a controlled environment in their own and each others soils, with and without arbuscular mycorrhizal fungi (AMF). Each ecotype grew comparatively better in its own soil indicating adaptation to its soil of origin. Overall, A. gerardii benefited more from AMF in low-nutrient Kansas soil than Illinois soil. The two ecotypes, however, did not benefit equally from mycorrhizal infection. The Kansas ecotype was three times more responsive to mycorrhizal infection in the Kansas soil than was the Illinois ecotype. Our results indicate that plant adaptation to the nutrient levels of their local soils is likely to be due, at least in part, to a shift in their dependence on mycorrhizal fungi. The Illinois ecotype of A. gerardii has evolved a reduced dependence upon these fungi and greater reliance on a more highly branched root system. In contrast, the Kansas ecotype had a significantly coarser root system and invested proportionately greater carbon in the symbiotic association with AMF as measured by spore production. This study provides the first demonstration that plants can adapt to changing soil nutrient levels by shifting their dependence on AMF. This result has broad implications for our understanding of the role of these fungi in agricultural systems.

From Lilliput to Brobdingnag: Extending Models of Mycorrhizal Function across Scales

ABSTRACT Mycorrhizae occur in nearly all terrestrial ecosystems. Resource exchange between host plants and mycorrhizal fungi influences community, ecosystem, and even global patterns and processes. Understanding the mechanisms and consequences of mycorrhizal symbioses across a hierarchy of scales will help predict system responses to environmental change and facilitate the management of these responses for sustainability and productivity. Conceptual and mathematical models have been developed to help understand and predict mycorrhizal functions. These models are most developed for individual- and population-scale processes, but models at community, ecosystem, and global scales are also beginning to emerge. We review seven types of mycorrhizal models that vary in their scale of resolution and dynamics, and discuss approaches for integrating these models with each other and with general models of terrestrial ecosystems.

Mycorrhizas: Gene to Function

Substantial progress has been made toward development of molecular tools for identification and quantification of mycorrhizal fungi in roots and evaluation of the diversity of ectomycorrhizal (ECM) fungi and the phylogeny and genetic structure of arbuscular mycorrhizal (AM) fungi. rDNA analysis confirms high diversity of ECM fungi on their hosts, and for AM fungi has revealed considerable genetic variation within and among morphologically similar AM fungal species. The fungal and plant genes, regulation of their expression, and biochemical pathways for nutrient exchange between symbiotic partners are now coming under intense study and will eventually be used to define the ecological nutritional role of the fungi. While molecular biological approaches have increased understanding of the mycorrhizal symbiosis, such knowledge about these lower-scale processes has yet to influence our understanding of larger-scale responses to any great extent.

Fungi in the future: interannual variation and effects of atmospheric change on arbuscular mycorrhizal fungal communities

Understanding the natural dynamics of arbuscular mycorrhizal (AM) fungi and their response to global environmental change is essential for the prediction of future plant growth and ecosystem functions. We investigated the long-term temporal dynamics and effect of elevated atmospheric carbon dioxide (CO2) and ozone (O3) concentrations on AM fungal communities. Molecular methods were used to characterize the AM fungal communities of soybean (Glycine max) grown under elevated and ambient atmospheric concentrations of both CO2 and O3 within a free air concentration enrichment experiment in three growing seasons over 5 yr. Elevated CO2 altered the community composition of AM fungi, increasing the ratio of Glomeraceae to Gigasporaceae. By contrast, no effect of elevated O3 on AM fungal communities was detected. However, the greatest compositional differences detected were between years, suggesting that, at least in the short term, large-scale interannual temporal dynamics are stronger mediators than atmospheric CO2 concentrations of AM fungal communities. We conclude that, although atmospheric change may significantly alter AM fungal communities, this effect may be masked by the influences of natural changes and successional patterns through time. We suggest that changes in carbon availability are important determinants of the community dynamics of AM fungi.

Serpentine soil has little influence on the root-associated microbial community composition of the serpentine tolerant grass species Avenula sulcata

Soil chemistry is a known influence on plant species distribution. Serpentine soils provide a striking example of this due to their discrete nature and long-studied influence on plant communities. Characterized by high levels of heavy metals and low levels of nutrients, they present a challenge for most plant species and allow only a relatively restricted set of species to grow. We do not yet fully understand the suite of adaptations present in serpentine endemics allowing them thrive where other plant species perform poorly or not at all. In this paper we explore the possibility that serpentine plants interact with a unique set of microbial endophytes, which allow them to make a living on this challenging substrate. To examine broad-scale patterns of microbial community composition we used phospholipid fatty acid analysis. To focus more narrowly on arbuscular mycorrhizal fungi community composition we used 18S rDNA markers specific to these fungi. We found only very weak evidence for a relationship with distinct microbial communities using either technique and no evidence to show increased reliance on AMF by serpentine plants. Our results indicate that adaptation of plants to serpentine soil does not involve adaptation to a unique community of soil mutualists.

Modeling forest ecosystem responses to elevated carbon dioxide and ozone using artificial neural networks

Rising atmospheric levels of carbon dioxide and ozone will impact productivity and carbon sequestration in forest ecosystems. The scale of this process and the potential economic consequences provide an incentive for the development of models to predict the types and rates of ecosystem responses and feedbacks that result from and influence of climate change. In this paper, we use phenotypic and molecular data derived from the Aspen Free Air CO2 Enrichment site (Aspen-FACE) to evaluate modeling approaches for ecosystem responses to changing conditions. At FACE, it was observed that different aspen clones exhibit clone-specific responses to elevated atmospheric levels of carbon dioxide and ozone. To identify the molecular basis for these observations, we used artificial neural networks (ANN) to examine above and below-ground community phenotype responses to elevated carbon dioxide, elevated ozone and gene expression profiles. The aspen community models generated using this approach identified specific genes and subnetworks of genes associated with variable sensitivities for aspen clones. The ANN model also predicts specific co-regulated gene clusters associated with differential sensitivity to elevated carbon dioxide and ozone in aspen species. The results suggest ANN is an effective approach to predict relevant gene expression changes resulting from environmental perturbation and provides useful information for the rational design of future biological experiments.