Spore traits mediate disturbance effects on arbuscular mycorrhizal fungal community composition and mutualisms.

Trait-based approaches in ecology are powerful tools for understanding how organisms interact with their environment. These approaches show particular promise in disturbance and community ecology contexts for understanding how disturbances like prescribed fire and bison grazing influence interactions between mutualists like arbuscular mycorrhizal (AM) fungi and their plant hosts. In this work we examined how disturbance effects on AM fungal spore community composition and mutualisms were mediated by selection for specific functional spore traits at both the species and community level. We tested these questions by analyzing AM fungal spore communities and traits from a frequently burned and grazed (bison) tallgrass prairie system and using these spores to inoculate a plant growth response experiment. Selection for darker, pigmented AM fungal spores, changes in the abundance and volume of individual AM fungal taxa, and altered sporulation, were indicators of fire and grazing effects on AM fungal community composition. Disturbance associated changes in AM fungal community composition were then correlated with altered growth responses of Schizachyrium scoparium grass. Our work shows that utilization of trait-based approaches in ecology can clarify the mechanisms that underly belowground responses to disturbance, and provide a useful framework for understanding interactions between organisms and their environment.

Spatial Structure within Root Systems Moderates Stability of Arbuscular Mycorrhizal Mutualism and Plant-Soil Feedbacks.

AbstractThe persistence of mutualisms is paradoxical, as there are fitness incentives for exploitation. This is particularly true for plant-microbe mutualisms like arbuscular mycorrhizae (AM), which are promiscuously horizontally transmitted. Preferential allocation by hosts to the best mutualist can stabilize horizontal mutualisms; however, preferential allocation is imperfect, with its fidelity likely depending on the spatial structure of symbionts in plant roots. In this study we tested AM mutualisms' dependence on two dimensions of spatial structure-the initial spatial association of fungi and the ease of fungal dispersal-through three complementary experiments. We found that fitness of the beneficial AM fungus increased when fungi were initially separate, while initial spatial mixing benefited the fitness of the nonbeneficial fungus. These effects were strongest when dispersal was limited and hosts could discriminate. Additionally, we found that changes in AM fungal proportional abundance induced by spatial structure in roots of a preferentially allocating host produced positive feedbacks on plant growth, showing that interactions between spatial structure and host choice can determine the direction of plant-soil feedbacks. Our results suggest that symbiont spatial structure within plant roots may act as an important modifier of plant preferential allocation and the dynamics of mycorrhizal mutualisms, with potentially cascading effects on plant-plant interactions.

Pyrophilic Plants Respond to Postfire Soil Conditions in a Frequently Burned Longleaf Pine Savanna.

AbstractFire-plant feedbacks engineer recurrent fires in pyrophilic ecosystems like savannas. The mechanisms sustaining these feedbacks may be related to plant adaptations that trigger rapid responses to fire's effects on soil. Plants adapted for high fire frequencies should quickly regrow, flower, and produce seeds that mature rapidly and disperse postfire. We hypothesized that the offspring of such plants would germinate and grow rapidly, responding to fire-generated changes in soil nutrients and biota. We conducted an experiment using longleaf pine savanna plants that were paired on the basis of differences in reproduction and survival under annual ("more" pyrophilic) versus less frequent ("less" pyrophilic) fire regimes. Seeds were planted in different soil inoculations from experimental fires of varying severity. The more pyrophilic species displayed high germination rates followed by species-specific rapid growth responses to soil location and fire severity effects on soils. In contrast, the less pyrophilic species had lower germination rates that were not responsive to soil treatments. This suggests that rapid germination and growth constitute adaptations to frequent fires and that plants respond differently to fire severity effects on soil abiotic factors and microbes. Furthermore, variable plant responses to postfire soils may influence plant community diversity and fire-fuel feedbacks in pyrophilic ecosystems.

Substrate composition influences amino acid carbon isotope profiles of fungi: implications for tracing fungal contributions to food webs.

Fungi link detrital resources and metazoan consumers through their role as decomposers. However, fungal contributions to metazoans may be misestimated in amino acid isotope studies because fungi are capable of both synthesizing amino acids (AAs) de novo and absorbing AAs from their environment. While fungi cultured in AA-free media have been used to represent fungi in studies of natural environments, fungi likely gain energetic benefits by taking up substrate AAs directly in situ. Consequently, fungi cultured on AA-free media may not be representative of the true variability of natural fungal δ13 CAA profiles. Therefore, the objective of this experiment was to determine the effect of substrate AA availability on yeast δ13 CAA profiles. We found that yeasts cultured in media of relatively higher AA content had different δ13 CAA profiles than yeasts grown in AA-free media, in part because yeasts utilized two essential AAs (Leu and Val) directly from media substrates when available in sufficient amounts. Furthermore, these differences among yeast δ13 CAA profiles remained after normalization of δ13 CAA values. We recommend further characterization of the variation in fungal δ13 CAA profiles and the incorporation of this potential variability into interpretations of basal resource use by metazoans.

Fungal community structure and seasonal trajectories respond similarly to fire across pyrophilic ecosystems.

Fire alters microbial community composition, and is expected to increase in frequency due to climate change. Testing whether microbes in different ecosystems will respond similarly to increased fire disturbance is difficult though, because fires are often unpredictable and hard to manage. Fire recurrent or pyrophilic ecosystems, however, may be useful models for testing the effects of frequent disturbance on microbes. We hypothesized that across pyrophilic ecosystems, fire would drive similar alterations to fungal communities, including altering seasonal community dynamics. We tested fire's effects on fungal communities in two pyrophilic ecosystems, a longleaf pine savanna and tallgrass prairie. Fire caused similar fungal community shifts, including (i) driving immediate changes that favored taxa able to survive fire and take advantage of post-fire environments and (ii) altering seasonal trajectories due to fire-associated changes to soil nutrient availability. This suggests that fire has predictable effects on fungal community structure and intra-annual community dynamics in pyrophilic ecosystems, and that these changes could significantly alter fungal function. Parallel fire responses in these key microbes may also suggest that recurrent fires drive convergent changes across ecosystems, including less fire-frequented systems that may start burning more often due to climate change.

Frequent fire slows microbial decomposition of newly deposited fine fuels in a pyrophilic ecosystem.

Frequent fires maintain nearly 50% of terrestrial ecosystems, and drive ecosystem changes that govern future fires. Since fires are dependent on available plant or fine fuels, ecosystem processes that alter fine fuel loads like microbial decomposition are particularly important and could modify future fires. We hypothesized that variation in short-term fire history would influence fuel dynamics in such ecosystems. We predicted that frequent fires within a short-time period would slow microbial decomposition of new fine fuels. We expected that fire effects would differ based on dominant substrates and that fire history would also alter soil nutrient availability, indirectly slowing decomposition. We measured decomposition of newly deposited fine fuels in a Longleaf pine savanna, comparing plots that burned 0, 1, 2, or 3 times between 2014 and 2016, and which were located in either close proximity to or away from overstory pines (Longleaf pine, Pinus palustris). Microbial decomposition was slower in plots near longleaf pines and, as the numbers of fires increased, decomposition slowed. We then used structural equation modeling to assess pathways for these effects (number of fires, 2016 fuel/fire characteristics, and soil chemistry). Increased fire frequency was directly associated with decreased microbial decomposition. While increased fires decreased nutrient availability, changes in nutrients were not associated with decomposition. Our findings indicate that increasing numbers of fires over short-time intervals can slow microbial decomposition of newly deposited fine fuels. This could favor fine fuel accumulation and drive positive feedbacks on future fires.