Mycorrhizal fungi modify decomposition: a meta-analysis.

It has been proposed that ectomycorrhizal fungi can reduce decomposition while arbuscular mycorrhizal fungi may enhance it. These phenomena are known as the 'Gadgil effect' and 'priming effect', respectively. However, it is unclear which one predominates globally. We evaluated whether mycorrhizal fungi decrease or increase decomposition, and identified conditions that mediate this effect. We obtained decomposition data from 43 studies (97 trials) conducted in field or laboratory settings that controlled the access of mycorrhizal fungi to substrates colonized by saprotrophs. Across studies, mycorrhizal fungi promoted decomposition of different substrates by 6.7% overall by favoring the priming effect over the Gadgil effect. However, we observed significant variation among studies. The substrate C : N ratio and absolute latitude influenced the effect of mycorrhizal fungi on decomposition and contributed to the variation. Specifically, mycorrhizal fungi increased decomposition at low substrate C : N and absolute latitude, but there was no discernable effect at high values. Unexpectedly, the effect of mycorrhizal fungi was not influenced by the mycorrhizal type. Our findings challenge previous assumptions about the universality of the Gadgil effect but highlight the potential of mycorrhizal fungi to negatively influence soil carbon storage by promoting the priming effect.

Los hongos ectomicorrízicos puden reducir la descomposición mientras que los hongos micorrízico­arbusculares pueden potenciarla. Ambos fenómenos son conocidos como "Gadgil effect" y "priming effect", respectivamente. Sin embargo, no es claro cuál predomina mundialmente. En este trabajo evaluamos si los hongos micorrízicos disminuyen o promueven la descomposición, e identificamos las condiciones que regulan este efecto. Para ello, recopilamos datos de descomposición de 43 estudios (97 observaciones) realizados en condiciones de campo o laboratorio que controlaron el acceso de los hongos micorrízicos a sustratos colonizados por saprótrofos. Los hongos micorrízicos promovieron la descomposición de diferentes sustratos en un 6.7%. Sin embargo, observamos una variación significativa entre estudios. La relación C : N del sustrato y la latitud influyeron en el efecto de los hongos micorrícicos sobre la descomposición y contribuyeron a la variabilidad. Específicamente, los hongos micorrízicos aumentaron la descomposición a valores bajos de C : N del sustrato y latitud, pero no hubo un efecto discernible en valores altos. Inesperadamente, el tipo de micorriza no influyó en el efecto de los hongos micorrízicos. Nuestros hallazgos cuestionan la universalidad del Gadgil effect, y resaltan el potencial de los hongos micorrízicos para influir negativamente en el almacenamiento de carbono del suelo al promover el priming effect.

Tracking fungal species-level responses in soil environments exposed to long-term warming and associated drying.

Climate change is affecting fungal communities and their function in terrestrial ecosystems. Despite making progress in the understanding of how the fungal community responds to global change drivers in natural ecosystems, little is known on how fungi respond at the species level. Understanding how fungal species respond to global change drivers, such as warming, is critical, as it could reveal adaptation pathways to help us to better understand ecosystem functioning in response to global change. Here, we present a model study to track species-level responses of fungi to warming-and associated drying-in a decade-long global change field experiment; we focused on two free-living saprotrophic fungi which were found in high abundance in our site, Mortierella and Penicillium. Using microbiological isolation techniques, combined with whole genome sequencing of fungal isolates, and community level metatranscriptomics, we investigated transcription-level differences of functional categories and specific genes involved in catabolic processes, cell homeostasis, cell morphogenesis, DNA regulation and organization, and protein biosynthesis. We found that transcription-level responses were mostly species-specific but that under warming, both fungi consistently invested in the transcription of critical genes involved in catabolic processes, cell morphogenesis, and protein biosynthesis, likely allowing them to withstand a decade of chronic stress. Overall, our work supports the idea that fungi that invest in maintaining their catabolic rates and processes while growing and protecting their cells may survive under global climate change.

Life history strategies of soil bacterial communities across global terrestrial biomes.

The life history strategies of soil microbes determine their metabolic potential and their response to environmental changes. Yet these strategies remain poorly understood. Here we use shotgun metagenomes from terrestrial biomes to characterize overarching covariations of the genomic traits that capture dominant life history strategies in bacterial communities. The emerging patterns show a triangle of life history strategies shaped by two trait dimensions, supporting previous theoretical and isolate-based studies. The first dimension ranges from streamlined genomes with simple metabolisms to larger genomes and expanded metabolic capacities. As metabolic capacities expand, bacterial communities increasingly differentiate along a second dimension that reflects a trade-off between increasing capacities for environmental responsiveness or for nutrient recycling. Random forest analyses show that soil pH, C:N ratio and precipitation patterns together drive the dominant life history strategy of soil bacterial communities and their biogeographic distribution. Our findings provide a trait-based framework to compare life history strategies of soil bacteria.

Assessing the Influence of Climate on the Spatial Pattern of West Nile Virus Incidence in the United States.

BACKGROUND: West Nile virus (WNV) is the leading cause of mosquito-borne disease in humans in the United States. Since the introduction of the disease in 1999, incidence levels have stabilized in many regions, allowing for analysis of climate conditions that shape the spatial structure of disease incidence. OBJECTIVES: Our goal was to identify the seasonal climate variables that influence the spatial extent and magnitude of WNV incidence in humans. METHODS: We developed a predictive model of contemporary mean annual WNV incidence using U.S. county-level case reports from 2005 to 2019 and seasonally averaged climate variables. We used a random forest model that had an out-of-sample model performance of R2=0.61. RESULTS: Our model accurately captured the V-shaped area of higher WNV incidence that extends from states on the Canadian border south through the middle of the Great Plains. It also captured a region of moderate WNV incidence in the southern Mississippi Valley. The highest levels of WNV incidence were in regions with dry and cold winters and wet and mild summers. The random forest model classified counties with average winter precipitation levels <23.3mm/month as having incidence levels over 11 times greater than those of counties that are wetter. Among the climate predictors, winter precipitation, fall precipitation, and winter temperature were the three most important predictive variables. DISCUSSION: We consider which aspects of the WNV transmission cycle climate conditions may benefit the most and argued that dry and cold winters are climate conditions optimal for the mosquito species key to amplifying WNV transmission. Our statistical model may be useful in projecting shifts in WNV risk in response to climate change. https://doi.org/10.1289/EHP10986.

Investigating the eco-evolutionary response of microbiomes to environmental change.

Microorganisms are the primary engines of biogeochemical processes and foundational to the provisioning of ecosystem services to human society. Free-living microbial communities (microbiomes) and their functioning are now known to be highly sensitive to environmental change. Given microorganisms' capacity for rapid evolution, evolutionary processes could play a role in this response. Currently, however, few models of biogeochemical processes explicitly consider how microbial evolution will affect biogeochemical responses to environmental change. Here, we propose a conceptual framework for explicitly integrating evolution into microbiome-functioning relationships. We consider how microbiomes respond simultaneously to environmental change via four interrelated processes that affect overall microbiome functioning (physiological acclimation, demography, dispersal and evolution). Recent evidence in both the laboratory and the field suggests that ecological and evolutionary dynamics occur simultaneously within microbiomes; however, the implications for biogeochemistry under environmental change will depend on the timescales over which these processes contribute to a microbiome's response. Over the long term, evolution may play an increasingly important role for microbially driven biogeochemical responses to environmental change, particularly to conditions without recent historical precedent.

Consequences of arthropod community structure for an at-risk insectivorous bird.

Global declines in bird and arthropod abundance highlights the importance of understanding the role of food limitation and arthropod community composition for the performance of insectivorous birds. In this study, we link data on nestling diet, arthropod availability and nesting performance for the Coastal Cactus Wren (Campylorhynchus brunneicapillus sandiegensis), an at-risk insectivorous bird native to coastal southern California and Baja Mexico. We used DNA metabarcoding to characterize nestling diets and monitored 8 bird territories over two years to assess the relationship between arthropod and vegetation community composition and bird reproductive success. We document a discordance between consumed prey and arthropod biomass within nesting territories, in which Diptera and Lepidoptera were the most frequently consumed prey taxa but were relatively rare in the environment. In contrast other Orders (e.g., Hemiptera, Hymenoptera)were abundant in the environment but were absent from nestling diets. Accordingly, variation in bird reproductive success among territories was positively related to the relative abundance of Lepidoptera (but not Diptera), which were most abundant on 2 shrub species (Eriogonum fasciculatum, Sambucus nigra) of the 9 habitat elements characterized (8 dominant plant species and bare ground). Bird reproductive success was in turn negatively related to two invasive arthropods whose abundance was not associated with preferred bird prey, but instead possibly acted through harassment (Linepithema humile; Argentine ants) and parasite transmission or low nutritional quality (Armadillidium vulgare; "pill-bug"). These results demonstrate how multiple aspects of arthropod community structure can influence bird performance through complementary mechanisms, and the importance of managing for arthropods in bird conservation efforts.

Fluorescent nanoparticles as tools in ecology and physiology.

Fluorescent nanoparticles (FNPs) have been widely used in chemistry and medicine for decades, but their employment in biology is relatively recent. Past reviews on FNPs have focused on chemical, physical or medical uses, making the extrapolation to biological applications difficult. In biology, FNPs have largely been used for biosensing and molecular tracking. However, concerns over toxicity in early types of FNPs, such as cadmium-containing quantum dots (QDs), may have prevented wide adoption. Recent developments, especially in non-Cd-containing FNPs, have alleviated toxicity problems, facilitating the use of FNPs for addressing ecological, physiological and molecule-level processes in biological research. Standardised protocols from synthesis to application and interdisciplinary approaches are critical for establishing FNPs in the biologists' tool kit. Here, we present an introduction to FNPs, summarise their use in biological applications, and discuss technical issues such as data reliability and biocompatibility. We assess whether biological research can benefit from FNPs and suggest ways in which FNPs can be applied to answer questions in biology. We conclude that FNPs have a great potential for studying various biological processes, especially tracking, sensing and imaging in physiology and ecology.

Exploring Trait Trade-Offs for Fungal Decomposers in a Southern California Grassland.

Fungi are important decomposers in terrestrial ecosystems, so their responses to climate change might influence carbon (C) and nitrogen (N) dynamics. We investigated whether growth and activity of fungi under drought conditions were structured by trade-offs among traits in 15 fungal isolates from a Mediterranean Southern California grassland. We inoculated fungi onto sterilized litter that was incubated at three moisture levels (4, 27, and 50% water holding capacity, WHC). For each isolate, we characterized traits that described three potential lifestyles within the newly proposed "YAS" framework: growth yield, resource acquisition, and stress tolerance. Specifically, we measured fungal hyphal length per unit litter decomposition for growth yield; the potential activities of the extracellular enzymes cellobiohydrolase (CBH), ß -glucosidase (BG), ß -xylosidase (BX), and N-acetyl- ß - D -glucosaminidase (NAG) for resource acquisition; and ability to grow in drought vs. higher moisture levels for drought stress tolerance. Although, we had hypothesized that evolutionary and physiological trade-offs would elicit negative relationships among traits, we found no supporting evidence for this hypothesis. Across isolates, growth yield, drought stress tolerance, and extracellular enzyme activities were not significantly related to each other. Thus, it is possible that drought-induced shifts in fungal community composition may not necessarily lead to changes in fungal biomass or decomposer ability in this arid grassland.

Phenotypic plasticity of fungal traits in response to moisture and temperature.

Phenotypic plasticity of traits is commonly measured in plants to improve understanding of organismal and ecosystem responses to climate change but is far less studied for microbes. Specifically, decomposer fungi are thought to display high levels of phenotypic plasticity and their functions have important implications for ecosystem dynamics. Assessing the phenotypic plasticity of fungal traits may therefore be important for predicting fungal community response to climate change. Here, we assess the phenotypic plasticity of 15 fungal isolates (12 species) from a Southern California grassland. Fungi were incubated on litter at five moisture levels (ranging from 4-50% water holding capacity) and at five temperatures (ranging from 4-36 °C). After incubation, fungal biomass and activities of four extracellular enzymes (cellobiohydrolase (CBH), ß-glucosidase (BG), ß-xylosidase (BX), and N-acetyl-ß-D-glucosaminidase (NAG)) were measured. We used response surface methodology to determine how fungal phenotypic plasticity differs across the moisture-temperature gradient. We hypothesized that fungal biomass and extracellular enzyme activities would vary with moisture and temperature and that the shape of the response surface would vary between fungal isolates. We further hypothesized that more closely related fungi would show more similar response surfaces across the moisture-temperature gradient. In support of our hypotheses, we found that plasticity differed between fungi along the temperature gradient for fungal biomass and for all the extracellular enzyme activities. Plasticity also differed between fungi along the moisture gradient for BG activity. These differences appear to be caused by variation mainly at the moisture and temperature extremes. We also found that more closely related fungi had more similar extracellular enzymes activities at the highest temperature. Altogether, this evidence suggests that with global warming, fungal biodiversity may become increasingly important as functional traits tend to diverge along phylogenetic lines at higher temperatures.

Embracing a new paradigm for temperature sensitivity of soil microbes.

The temperature sensitivity of soil processes is of major interest, especially in light of climate change. Originally formulated to explain the temperature dependence of chemical reactions, the Arrhenius equation, and related Q10 temperature coefficient, has a long history of application to soil biological processes. However, empirical data indicate that Q10 and Arrhenius model are often poor metrics of temperature sensitivity in soils. In this opinion piece, we aim to (a) review alternative approaches for characterizing temperature sensitivity, focusing on macromolecular rate theory (MMRT); (b) provide strategies and tools for implementing a new temperature sensitivity framework; (c) develop thermal adaptation hypotheses for the MMRT framework; and (d) explore new questions and opportunities stemming from this paradigm shift. Microbial ecologists should consider developing and adopting MMRT as the basis for predicting biological rates as a function of temperature. Improved understanding of temperature sensitivity in soils is particularly pertinent as microbial response to temperature has a large impact on global climate feedbacks.

Fungal functional ecology: bringing a trait-based approach to plant-associated fungi.

Fungi play many essential roles in ecosystems. They facilitate plant access to nutrients and water, serve as decay agents that cycle carbon and nutrients through the soil, water and atmosphere, and are major regulators of macro-organismal populations. Although technological advances are improving the detection and identification of fungi, there still exist key gaps in our ecological knowledge of this kingdom, especially related to function. Trait-based approaches have been instrumental in strengthening our understanding of plant functional ecology and, as such, provide excellent models for deepening our understanding of fungal functional ecology in ways that complement insights gained from traditional and -omics-based techniques. In this review, we synthesize current knowledge of fungal functional ecology, taxonomy and systematics and introduce a novel database of fungal functional traits (FunFun ). FunFun is built to interface with other databases to explore and predict how fungal functional diversity varies by taxonomy, guild, and other evolutionary or ecological grouping variables. To highlight how a quantitative trait-based approach can provide new insights, we describe multiple targeted examples and end by suggesting next steps in the rapidly growing field of fungal functional ecology.

Soil Metatranscriptomes Under Long-Term Experimental Warming and Drying: Fungi Allocate Resources to Cell Metabolic Maintenance Rather Than Decay.

Earth's temperature is rising, and with this increase, fungal communities are responding and affecting soil carbon processes. At a long-term soil-warming experiment in a boreal forest in interior Alaska, warming and warming-associated drying alters the function of microbes, and thus, decomposition of carbon. But what genetic mechanisms and resource allocation strategies are behind these community shifts and soil carbon changes? Here, we evaluate fungal resource allocation efforts under long-term experimental warming (including associated drying) using soil metatranscriptomics. We profiled resource allocation efforts toward decomposition and cell metabolic maintenance, and we characterized community composition. We found that under the warming treatment, fungi allocate resources to cell metabolic maintenance at the expense of allocating resources to decomposition. In addition, we found that fungal orders that house taxa with stress-tolerant traits were more abundant under the warmed treatment compared to control conditions. Our results suggest that the warming treatment elicits an ecological tradeoff in resource allocation in the fungal communities, with potential to change ecosystem-scale carbon dynamics. Fungi preferentially invest in mechanisms that will ensure survival under warming and drying, such as cell metabolic maintenance, rather than in decomposition. Through metatranscriptomes, we provide mechanistic insight behind the response of fungi to climate change and consequences to soil carbon processes.

Expansion of Coccidioidomycosis Endemic Regions in the United States in Response to Climate Change.

Coccidioidomycosis (Valley fever) is a fungal disease endemic to the southwestern United States. Across this region, temperature and precipitation influence the extent of the endemic region and number of Valley fever cases. Climate projections for the western United States indicate that temperatures will increase and precipitation patterns will shift, which may alter disease dynamics. We estimated the area potentially endemic to Valley fever using a climate niche model derived from contemporary climate and disease incidence data. We then used our model with projections of climate from Earth system models to assess how endemic areas will change during the 21st century. By 2100 in a high warming scenario, our model predicts that the area of climate-limited endemicity will more than double, the number of affected states will increase from 12 to 17, and the number of Valley fever cases will increase by 50%. The Valley fever endemic region will expand north into dry western states, including Idaho, Wyoming, Montana, Nebraska, South Dakota, and North Dakota. Precipitation will limit the disease from spreading into states farther east and along the central and northern Pacific coast. This is the first quantitative estimate of how climate change may influence Valley fever in the United States. Our predictive model of Valley fever endemicity may provide guidance to public health officials to establish disease surveillance programs and design mitigation efforts to limit the impacts of this disease.

Decomposition responses to climate depend on microbial community composition.

Bacteria and fungi drive decomposition, a fundamental process in the carbon cycle, yet the importance of microbial community composition for decomposition remains elusive. Here, we used an 18-month reciprocal transplant experiment along a climate gradient in Southern California to disentangle the effects of the microbial community versus the environment on decomposition. Specifically, we tested whether the decomposition response to climate change depends on the microbial community. We inoculated microbial decomposers from each site onto a common, irradiated leaf litter within "microbial cages" that prevent microbial exchange with the environment. We characterized fungal and bacterial composition and abundance over time and investigated the functional consequences through litter mass loss and chemistry. After 12 months, microbial communities altered both decomposition rate and litter chemistry. Further, the functional measurements depended on an interaction between the community and its climate in a manner not predicted by current theory. Moreover, microbial ecologists have traditionally considered fungi to be the primary agents of decomposition and for bacteria to play a minor role. Our results indicate that not only does climate change and transplantation have differential legacy effects among bacteria and fungi, but also that bacterial communities might be less functionally redundant than fungi with regards to decomposition. Thus, it may be time to reevaluate both the role of microbial community composition in its decomposition response to climate and the relative roles of bacterial and fungal communities in decomposition.

Drought increases the frequencies of fungal functional genes related to carbon and nitrogen acquisition.

Although water is a critical resource for organisms, microbially-mediated processes such as decomposition and nitrogen (N) transformations can endure within ecosystems even when water is scarce. To identify underlying mechanisms, we examined the genetic potential for fungi to contribute to specific aspects of carbon (C) and N cycling in a drought manipulation in Southern California grassland. In particular, we measured the frequency of fungal functional genes encoding enzymes that break down cellulose and chitin, and take up ammonium and amino acids, in decomposing litter. Furthermore, we used "microbial cages" to reciprocally transplant litter and microbes between control and drought plots. This approach allowed us to distinguish direct effects of drought in the plot environment versus indirect effects via shifts in the microbial community or changes in litter chemistry. For every fungal functional gene we examined, the frequency of that gene within the microbial community increased significantly in drought plots compared to control plots. In contrast, when plot environment was held constant, frequencies of these fungal functional genes did not differ significantly between control-derived microbes versus drought-derived microbes, or between control-derived litter versus drought-derived litter. It appears that drought directly selects for fungi with the genetic capacity to acquire these specific C- and N-containing compounds. This genetic trait may allow fungi to take advantage of ephemeral water supplies. Altogether, proliferation of fungi with the genetic capacity for C and N acquisition may contribute to the maintenance of biogeochemical cycling under drought.

Temperature sensitivities of extracellular enzyme Vmax and Km across thermal environments.

The magnitude and direction of carbon cycle feedbacks under climate warming remain uncertain due to insufficient knowledge about the temperature sensitivities of soil microbial processes. Enzymatic rates could increase at higher temperatures, but this response could change over time if soil microbes adapt to warming. We used the Arrhenius relationship, biochemical transition state theory, and thermal physiology theory to predict the responses of extracellular enzyme Vmax and Km to temperature. Based on these concepts, we hypothesized that Vmax and Km would correlate positively with each other and show positive temperature sensitivities. For enzymes from warmer environments, we expected to find lower Vmax , Km , and Km temperature sensitivity but higher Vmax temperature sensitivity. We tested these hypotheses with isolates of the filamentous fungus Neurospora discreta collected from around the globe and with decomposing leaf litter from a warming experiment in Alaskan boreal forest. For Neurospora extracellular enzymes, Vmax Q10 ranged from 1.48 to 2.25, and Km Q10 ranged from 0.71 to 2.80. In agreement with theory, Vmax and Km were positively correlated for some enzymes, and Vmax declined under experimental warming in Alaskan litter. However, the temperature sensitivities of Vmax and Km did not vary as expected with warming. We also found no relationship between temperature sensitivity of Vmax or Km and mean annual temperature of the isolation site for Neurospora strains. Declining Vmax in the Alaskan warming treatment implies a short-term negative feedback to climate change, but the Neurospora results suggest that climate-driven changes in plant inputs and soil properties are important controls on enzyme kinetics in the long term. Our empirical data on enzyme Vmax , Km , and temperature sensitivities should be useful for parameterizing existing biogeochemical models, but they reveal a need to develop new theory on thermal adaptation mechanisms.

Links between plant and fungal diversity in habitat fragments of coastal shrubland.

Habitat fragmentation is widespread across ecosystems, detrimentally affecting biodiversity. Although most habitat fragmentation studies have been conducted on macroscopic organisms, microbial communities and fungal processes may also be threatened by fragmentation. This study investigated whether fragmentation, and the effects of fragmentation on plants, altered fungal diversity and function within a fragmented shrubland in southern California. Using fluorimetric techniques, we assayed enzymes from plant litter collected from fragments of varying sizes to investigate enzymatic responses to fragmentation. To isolate the effects of plant richness from those of fragment size on fungi, we deployed litter bags containing different levels of plant litter diversity into the largest fragment and incubated in the field for one year. Following field incubation, we determined litter mass loss and conducted molecular analyses of fungal communities. We found that leaf-litter enzyme activity declined in smaller habitat fragments with less diverse vegetation. Moreover, we detected greater litter mass loss in litter bags containing more diverse plant litter. Additionally, bags with greater plant litter diversity harbored greater numbers of fungal taxa. These findings suggest that both plant litter resources and fungal function may be affected by habitat fragmentation's constraints on plants, possibly because plant species differ chemically, and may thus decompose at different rates. Diverse plant assemblages may produce a greater variety of litter resources and provide more ecological niche space, which may support greater numbers of fungal taxa. Thus, reduced plant diversity may constrain both fungal taxa richness and decomposition in fragmented coastal shrublands. Altogether, our findings provide evidence that even fungi may be affected by human-driven habitat fragmentation via direct effects of fragmentation on plants. Our findings underscore the importance of restoring diverse vegetation communities within larger coastal sage scrub fragments and suggest that this may be an effective way to improve the functional capacity of degraded sites.