• Energy Research

• Premise of the study: Fungal endophytes are symbionts that inhabit aboveground tissues of most terrestrial plants and can affect plant physiology and growth under stressed conditions. In a future faced with substantial climate change, endophytes have the potential to play an important role in plant stress resistance. Understanding both the distributions of endophytes and their functioning in symbiosis with plants are key aspects of predicting their role in an altered climate.• Methods: Here we characterized endophytes in grasses across a steep precipitation gradient to examine the relative importance of environmental and spatial factors in structuring endophyte communities. We also tested how 20 endophytes isolated from drier and wetter regions performed in symbiosis with grass seedlings under high and low soil moisture in the greenhouse.• Key results: Environmental factors related to historical and current precipitation were the most important predictors of endophyte communities in the field. On average, endophytic fungi from western sites also reduced plant water loss in the greenhouse compared to fungi from eastern sites. However, there was substantial variability in how individual endophytic taxa affected plant traits under high and low water availability, with up to two orders of magnitude difference in the plasticity of plant traits conferred by the different fungal taxa.• Conclusions: While species sorting appears to largely explain local endophyte community composition, their function in symbiosis is not predictable from local environmental conditions. The development of a predictive framework for endophyte function will require further study of individual fungal taxa and genotypes across environmental gradients.

Climate-induced changes in soil microbial physiology impact ecosystem carbon (C) storage and alter the rate of CO2 flux from soils to the atmosphere (Allison et al., 2010). The direction and magnitude of these microbial feedbacks depend on changes in saprotrophic bacterial and fungal C allocation in response to altered temperature, precipitation, and nutrient availability. Soil microbes may differentially allocate C in changing environments by altering processes such as enzyme production, C use efficiency (CUE), or biomass stoichiometry (Figure ​(Figure1).1). However, because these mechanisms may operate simultaneously and interact, microbial physiological feedbacks on soil C storage are difficult to predict. For example, initial increases in microbial CUE or biomass C:N may be counteracted by increases in enzyme production to acquire limiting organic nutrients. Figure 1 Three mechanisms through which microorganisms can shift C allocation: (A) extracellular enzyme activities, (B) carbon use efficiency, or (C) biomass stoichiometry. Each of these pathways can alter C storage in soils. Trend lines indicate expected responses ... Few studies have standardized microbial process rates, such as extracellular enzyme production or respiration, to the size of the microbial biomass. Examining process rates alone may obscure the microbial physiological mechanisms that underlie climate-induced changes in soil C cycling, leading to contradictory patterns among different studies. For instance, in a large-scale survey of soil protease activities from climate manipulations, drier and warmer conditions resulted in lower extracellular enzyme activities (EEA) compared to ambient conditions (Brzostek et al., 2012). In contrast, drier soils have also been found to stabilize extracellular enzymes in water films, reducing enzyme turnover rates and increasing potential activities (Lawrence et al., 2009; German et al., 2012).

A great deal of effort has been applied to maximizing switchgrass (Panicum virgatum L.) production for bioenergy by leveraging existing local adaptation to climate and via nutrient management in this perennial grass crop. However, the biotic component of soils can also affect plant production and long-term suitability at a given site. Here, we tested how productivity of four switchgrass cultivars were affected by four microbial sources from the Great Plains. All inoculum soil sources were previously conditioned by a mixture of switchgrass cultivars, allowing us to explicitly address plant-soil feedback effects. Microbial soil inocula were added to a consistent background soil to avoid physicochemical variation across the sources. We found that the soil microbial inoculum source mattered more than cultivar in determining switchgrass biomass. The addition of microbes resulted in smaller plants, with the largest plants found on control soils with no inoculum, but some inocula were less negative than others. There was no geographic matching between cultivars and soil microbial inoculum, suggesting little local adaptation to the biotic component of soils. In addition, measurements of fungal root colonization suggest that fungi are not responsible for the observed patterns. Based on these results, we suggest that switchgrass cultivation could benefit from considering effects of the soil biota. Additional work is needed to generalize these patterns over time, to a wider geographic area, and to a broader range of cultivars.

AbstractRespiration of soil organic carbon is one of the largest fluxes of CO2 on earth. Understanding the processes that regulate soil respiration is critical for predicting future climate. Recent work has suggested that soil carbon respiration may be reduced by competition for nitrogen between symbiotic ectomycorrhizal fungi that associate with plant roots and free‐living microbial decomposers, which is consistent with increased soil carbon storage in ectomycorrhizal ecosystems globally. However, experimental tests of the mycorrhizal competition hypothesis are lacking. Here we show that ectomycorrhizal roots and hyphae decrease soil carbon respiration rates by up to 67% under field conditions in two separate field exclusion experiments, and this likely occurs via competition for soil nitrogen, an effect larger than 2 °C soil warming. These findings support mycorrhizal competition for nitrogen as an independent driver of soil carbon balance and demonstrate the need to understand microbial community interactions to predict ecosystem feedbacks to global climate.

Significance Ecosystems’ feedback to climate change remains a source of uncertainty in global models that project future climate conditions. That uncertainty rests largely on how much soil carbon will be lost as microbial respiration and how that loss varies across ecosystems. Although there has been a large emphasis on microbial temperature responses, how soil microorganisms respond to changes in moisture remains poorly understood. Here we show that historical rainfall controls soil respiration responses to current moisture. This finding was robust, with historical climate repeatedly limiting current respiration regardless of alterations to soil moisture, rainfall, or the arrival of new taxa. This study highlights the importance that legacies in microbial responses to climate change can have in future ecosystem responses.

Understanding latitudinal adaptation of switchgrass (Panicum virgatum L.) and Miscanthus (Miscanthus × giganteus J. M. Greef & Deuter ex Hodk. & Renvoize) to the southern Great Plains is key to maximizing productivity by matching each grass variety to its optimal production environment. The objectives of this study were: (1) to quantify latitudinal variation in production of representative upland switchgrass ecotypes (Blackwell, Cave-in-Rock, and Shawnee), lowland switchgrass ecotypes (Alamo, Kanlow), and Miscanthus in the southern half of the US Great Plains and (2) to investigate the environmental factors affecting yield variation. Leaf area and yield were measured on plots at 10 locations in Missouri, Arkansas, Oklahoma, and Texas. More cold winter days led to decreased subsequent Alamo switchgrass yields and increased subsequent upland switchgrass yields. More hot-growing season days led to decreased Kanlow and Miscanthus yields. Increased drought intensity also contributed to decreased Miscanthus yields. Alamo switchgrass had the greatest radiation use efficiency (RUE) with a mean of 4.3 g per megajoule intercepted PAR and water use efficiency (WUE) with a mean of 4.5 mg of dry weight per gram of water transpired. The representative RUE values for other varieties ranged from 67 to 80 % of Alamo’s RUE value and 67 to 87 % of Alamo’s WUE. These results will provide valuable inputs to process-based models to realistically simulate these important perennial grasses in this region and to assess the environmental impacts of production on water use and nutrient demands. In addition, it will also be useful for landowners and companies choosing the most productive perennial grasses for biofuel production.

Fungal symbionts living inside plant leaves ("endophytes") can vary from beneficial to parasitic, but the mechanisms by which the fungi affect the plant host phenotype remain poorly understood. Chemical interactions are likely the proximal mechanism of interaction between foliar endophytes and the plant, as individual fungal strains are often exploited for their diverse secondary metabolite production. Here, we go beyond single strains to examine commonalities in how 16 fungal endophytes shift plant phenotypic traits such as growth and physiology, and how those relate to plant metabolomics profiles. We inoculated individual fungi on switchgrass, Panicum virgatum L. This created a limited range of plant growth and physiology (2-370% of fungus-free controls on average), but effects of most fungi overlapped, indicating functional similarities in unstressed conditions. Overall plant metabolomics profiles included almost 2000 metabolites, which were broadly correlated with plant traits across all the fungal treatments. Terpenoid-rich samples were associated with larger, more physiologically active plants and phenolic-rich samples were associated with smaller, less active plants. Only 47 metabolites were enriched in plants inoculated with fungi relative to fungus-free controls, and of these, Lasso regression identified 12 metabolites that explained from 14 to 43% of plant trait variation. Fungal long-chain fatty acids and sterol precursors were positively associated with plant photosynthesis, conductance, and shoot biomass, but negatively associated with survival. The phytohormone gibberellin, in contrast, was negatively associated with plant physiology and biomass. These results can inform ongoing efforts to develop metabolites as crop management tools, either by direct application or via breeding, by identifying how associations with more beneficial components of the microbiome may be affected.

Abstract Long-term climate history can influence rates of soil carbon cycling but the microbial traits underlying these legacy effects are not well understood. Legacies may result if historical climate differences alter the traits of soil microbial communities, particularly those associated with carbon cycling and stress tolerance. However, it is also possible that contemporary conditions can overcome the influence of historical climate, particularly under extreme conditions. Using shotgun metagenomics, we assessed the composition of soil microbial functional genes across a mean annual precipitation gradient that previously showed evidence of strong climate legacies in soil carbon flux and extracellular enzyme activity. Sampling coincided with recovery from a regional, multi-year severe drought, allowing us to document how the strength of climate legacies varied with contemporary conditions. We found increased investment in genes associated with resource cycling with historically higher precipitation across the gradient, particularly in traits related to resource transport and complex carbon degradation. This legacy effect was strongest in seasons with the lowest soil moisture, suggesting that contemporary conditions—particularly, resource stress under water limitation—influences the strength of legacy effects. In contrast, investment in stress tolerance did not vary with historical precipitation, likely due to frequent periodic drought throughout the gradient. Differences in the relative abundance of functional genes explained over half of variation in microbial functional capacity—potential enzyme activity—more so than historical precipitation or current moisture conditions. Together, these results suggest that long-term climate can alter the functional potential of soil microbial communities, leading to legacies in carbon cycling.