Fire is a common disturbance that structures terrestrial ecosystems. Since climate change models predict increases in fire frequency, it is important to study how changes in fire regime influence plant fuel-related above- and belowground ecosystem components. Due to their role in plant fuel production, arbuscular mycorrhizal (AM) fungal spore communities and symbioses with plants are invaluable for understanding how changes in fire regime influence belowground communities and alter fuel-related above- and belowground processes such as plant growth. With a greenhouse experiment, we tested how variation in fire frequency and history influenced AM fungal community composition, traits, and their interactions with host plants by manipulating fire regimes over three successive generations of AM fungi and Rudbeckia hirta plants. We found that fire frequency effects on spore traits such as pigmentation and sporulation mediated changes in AM fungal spore communities, but these effects took time to develop and were associated with reduced plant growth. This demonstrates that increases in fire frequency can alter the fire-fuel feedbacks that underlie pyrophilic ecosystems.
Tillage effects on soils vary in their intensity of disturbance within a soil system. There are clear trade-offs between tillage methods, thus farmers must navigate a complex balance between the appropriate level of disturbance to produce soil conditions that facilitate plant growth while minimizing the long-term loss of soil related ecosystem services and effects of drought and extreme rainfall. This balance is exemplified in agricultural systems of the Midwestern US where climate models predict increases in intermittent drought and extreme rainfall events. Here we tested how tillage effects on soil abiotic and biotic characteristics influenced the yield of Zea mays under high rainfall conditions. We found that as tillage intensity increased the relative yield benefits provided by soil abiotic vs. biotic characteristics increased. Specifically, lower intensity tillage methods like notill (yield: 11.3 Mg/ha) and chisel till (yield: 12.5 Mg/ha) favored bacterial, fungal, and AM fungal taxa that were more beneficial to yield, while moldboard plowing (yield: 12.2 Mg/ha) benefited yield through increases to soil packed bulk density. While decreasing tillage intensity promoted positive effects of soil nutrient retention and soil microbes on yield, the lower soil packed bulk density in no-till plots reduced yield due to poor drainage (10 % yield decrease). Thus, there are complex interactions between tillage, climate, and soils that influence yield, and intermediate intensity tillage methods like chisel till may provide a useful balance between no-till and moldboard plowing with changing precipitation regimes.
The Stress Gradient Hypothesis (SGH) predicts that interspecific interactions shift from competition under low stress to facilitation under high stress. Historically, this framework has been extensively studied in plants, but its application to microbial communities remains underexplored. Here, we review literature to examine bacterial interactions under heavy metal stress, using selenium (Se) stress as a model for heavy metal-induced environmental pressures. Se, a naturally occurring and anthropogenic metalloid contaminant, provides oxidative stress on bacteria, which will modify competitive and facilitative behaviours under the SGH framework. At low Se concentrations, bacterial interactions are predominantly competitive, driven by resource competition and antimicrobial strategies. However, as Se stress increases, we predict facilitative interactions to increase, including detoxification mechanisms that reduce toxicity for Se intolerant species. We discuss methodologies to measure bacterial competition and facilitation, propose experimental approaches to identify the transition between these interaction modes, and explore the implications of species richness in microbial stress resilience. Understanding these interactions provides insights into microbial ecology, biogeochemical cycling and potential applications in bioremediation.
Fire is a common ecological disturbance that structures terrestrial ecosystems and biological communities. The ability of fires to contribute to ecosystem heterogeneity has been termed pyrodiversity and has been directly linked to biodiversity (i.e., the pyrodiversity-biodiversity hypothesis). Since climate change models predict increases in fire frequency, understanding how fire pyrodiversity influences soil microbes is important for predicting how ecosystems will respond to fire regime changes. Here we tested how fire frequency-driven changes in burn patterns (i.e., pyrodiversity) influenced soil microbial communities and diversity. We assessed pyrodiversity effects on soil microbes by manipulating fire frequency (annual vs. biennial fires) in a tallgrass prairie restoration and evaluating how changes in burn patterns influenced microbial communities (bacteria and fungi). Annual burns produced more heterogeneous burn patterns (higher pyrodiversity) that were linked to shifts in fungal and bacterial community composition. While fire frequency did not influence microbial (bacteria and fungi) alpha diversity, beta diversity did increase with pyrodiversity. Changes in fungal community composition were not linked to burn patterns, suggesting that pyrodiversity effects on other ecosystem components (e.g., plants and soil characteristics) influenced fungal community dynamics and the greater beta diversity observed in the annually burned plots. Shifts in bacterial community composition were linked to variation in higher severity burn pattern components (grey and white ash), suggesting that thermotolerance contributed to the observed changes in bacterial community composition and lower beta diversity in the biennially burned plots. This demonstrates that fire frequency-driven increases in pyrodiversity augment biodiversity and may influence productivity in fire-prone ecosystems.
Fire is a globally pervasive force reshaping ecosystems, yet its influence on the ecological processes structuring soil microbiomes remains poorly understood. Using a meta-analysis of > 2600 amplicon sequencing samples across 19 global studies, we tested whether fire alters soil microbiome assembly processes, diversity, and ecological selection for pyrophilic specialists. Contrary to prevailing assumptions, we found that fire did not significantly shift ecological selection processes in bacteria or fungi but instead constrained dispersal, particularly reducing dispersal in bacterial and fungal communities and increasing ecological drift in fungi. Despite limited evidence for ecological selection, fire consistently filtered for specialist taxa, increasing their relative abundance across microbial communities. Fire also reduced fungal diversity and evenness, while bacterial communities exhibited greater dominance and loss of rare taxa. These findings support the idea that fire promotes microbial post-fire niche specialization while disrupting dispersal pathways. Our results indicate that increasing fire frequency and severity under climate change may homogenize soil microbial communities, reduce microbial resilience, and constrain ecosystem recovery.
BackgroundMicrobiomes, essential to ecosystem processes, face strong selective forces that can drive rapid evolutionary adaptation. However, our understanding of evolutionary processes within natural systems remains limited. We investigated evolution in response to naturally occurring selenium in soils of different geological parental materials on the Western Slope of Colorado. Our study focused on examining changes in gene frequencies within microbial communities in response to selenium exposure.ResultsDespite expectations of taxonomic composition shifts and increased gene content changes at high-selenium sites, we found no significant alterations in microbial diversity or community composition. Surprisingly, we observed a significant increase in differentially abundant genes within high-selenium sites.ConclusionsThese findings are suggestive that selection within microbiomes primarily drives the accumulation of genes among existing microbial taxa, rather than microbial species turnover, in response to strong stressors like selenium. Our study highlights an unusual system that allows us to examine evolution in response to the same stressor annually in a non-model system, contributing to understanding microbiome evolution beyond model systems.
Background and aims Arbuscular mycorrhizal (AM) fungi are common mutualists in grassland and savanna systems that are adapted to recurrent fire disturbance. This long-term adaptation to fire means that AM fungi display disturbance associated traits which should be useful for understanding environmental and seasonal effects on AM fungal community assembly. Methods In this work, we evaluated how fire effects on AM fungal spore traits and community composition vary with fire season (Fall vs. Spring) and time since fire. We tested this by analyzing AM fungal spore traits (e.g., colorimetric, sporulation, and size) from a fire regime experiment. Results Immediately following Fall and Spring fires, spore pigmentation darkened (became less hyaline); however, this trait response was not linked to fire driven changes in spore community composition and likely implies a plastic spore pigmentation response to fire. Six months after Fall fires, spores in burned plots were lower in volume, produced less color rich pigment, and had higher sporulation rates, and these differences in spore traits were associated with shifts in AM fungal spore communities demonstrating environmental filtering. Conclusion Fire drove plastic and longer-term changes in AM fungal spore traits and community assembly that varied with fire season (stronger effects in Fall) and time since fire. This demonstrates the utility of applying trait-based approaches to microbial community assembly, and the importance of considering changes in community assembly across time.
Plant-associated microbial communities are key to shaping many aspects of plant biology. In this study, we tested whether soil microbial communities and herbivory influence the bacterial community of tomato plants and whether their influence in different plant compartments is driven by microbial spillover between compartments or whether plants are involved in mediating this effect. We grew our plants in soils hosting three different microbial communities and covered (or not) the soil surface to prevent (or allow) passive microbial spillover between compartments, and we exposed them (or not) to herbivory by Manduca sexta. Here we show that the soil-driven effect on aboveground compartments is consistently detected regardless of soil coverage, whereas soil cover influences the herbivore-driven effect on belowground microbiota. Together, our results suggest that the soil microbiota influences aboveground plant and insect microbial communities via changes in plant metabolism and physiology or by sharing microorganisms via xylem sap. In contrast, herbivores influence the belowground plant microbiota via a combination of microbial spillover and changes in plant metabolism. These results demonstrate the important role of plants in linking aboveground and belowground microbiota, and can foster further research on soil microbiota manipulation for sustainable pest management. This study shows that the soil microbial community and herbivory both influence the assembly of the plant-associated microbial communities, but their effects are generated through different mechanisms.
Abstract Fungi play key roles in the fire‐fuel feedbacks that structure ~40% of the Earth's terrestrial ecosystems, yet a general understanding of fungal responses to fire is lacking. While fire and associated stressor effects on fungi vary based on fire regime components like severity, intensity, and frequency, their influence on fungi can be categorized into three primary phases based on when they influence fungi: during fire, early post‐fire, and later post‐fire. We first identify key fire‐associated phenomic traits and similarities in fungal responses to fire across time. Then, we synthesize this information by linking fire effects to specific fungal traits and response groups to produce trait profiles useful for classifying pyrophilic fungi. The goal of this review is to consolidate fire‐associated phenomic trait data into trait profiles that can be used in combination with fungal genomic data and associated methodologies. These profiles produce an invaluable framework for understanding fungal roles in fire regimes and identify previously unknown trends in fungal responses to fire and associated stressors including heat shock responses, pigmentation, and dispersal into and out of burned environments.
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.
Sustainable food production is a grand challenge facing the global economy. Traditional agricultural practice requires numerous interventions, such as application of nutrients and pesticides, of which only a fraction are utilized by the target crop plants. Controlled release systems (CRSs) designed for agriculture could improve targeting of agrochemicals, reducing costs and improving environmental sustainability. CRSs have been extensively used in biomedical applications to generate spatiotemporal release patterns of targeted compounds. Such systems protect encapsulant molecules from the external environment and off-target uptake, increasing their biodistribution and pharmacokinetic profiles. Advanced ‘smart’ release designs enable on-demand release in response to environmental cues, and theranostic systems combine sensing and release for real-time monitoring of therapeutic interventions. This review examines the history of biomedical CRSs, highlighting opportunities to translate biomedical designs to agricultural applications. Common encapsulants and targets of agricultural CRSs are discussed, as well as additional demands of these systems, such as need for high volume, low cost, environmentally friendly materials and manufacturing processes. Existing agricultural CRSs are reviewed, and opportunities in emerging systems, such as nanoparticle, ‘smart’ release, and theranostic formulations are highlighted. This review is designed to provide a guide to researchers in the biomedical controlled release field for translating their knowledge to agricultural applications, and to provide a brief introduction of biomedical CRSs to experts in soil ecology, microbiology, horticulture, and crop sciences.
Microbiome science is revolutionizing many concepts of plant biology, ecology, and evolution. Understanding plant microbiomes is key to developing solutions that protect crop health without impacting the environment. In this perspective article, we highlight the importance of both the structure and functions of plant-associated microbial communities in protecting their host from pathogens. These new findings have a high potential to aid biocontrol programs and to replace traditional chemical products, guiding the transition towards a sustainable production.
The symbiotic interaction between plants and arbuscular mycorrhizal (AM) fungi is often perceived as beneficial for both partners, though a large ecological literature highlights the context dependency of this interaction. Changes in abiotic variables, such as nutrient availability, can drive the interaction along the mutualism-parasitism continuum with variable outcomes for plant growth and fitness. However, AM fungi can benefit plants in more ways than improved phosphorus nutrition and plant growth. For example, AM fungi can promote abiotic and biotic stress tolerance even when considered parasitic from a nutrient provision perspective. Other than being obligate biotrophs, very little is known about the benefits AM fungi gain from plants. In this review, we utilize both molecular biology and ecological approaches to expand our understanding of the plant-AM fungal interaction across disciplines.
The symbiosis between arbuscular mycorrhizal (AM) fungi, subphylum Glomeromycotina, and terrestrial plants is one of the most widespread and arguably most successful plant symbioses on Earth. This ancient relationship, going back 475 MY (Remy et al., 1994; Redecker & Raab, 2006; Field et al., 2015; Rich et al., 2021) is beneficial for the fungi and normally benefits their plant partners. Through colonisation of plant roots, the fungi provide their host plants with access to soil elements including phosphorus (P) and nitrogen (N) while the fungi are provided with carbon (Hodge et al., 2001; Smith & Read, 2008; Keymer & Gutjahr, 2018). The contribution of AM fungi to ecosystems goes beyond nutrient delivery to plants.
Rhizosphere microbiomes are influenced by abiotic stresses, but we know a little about their response to combinations of stresses. In this study we tested: (i) if drought and heat stress influence the maize rhizosphere microbial community; (ii) if the combination of drought and heat has a different outcome compared to a single stress; (iii) if rhizosphere microbiota clusters according to root class and root zone. We setup a microcosm system using maize as model plant. We exposed plants to drought, heat stress and their combination, and used 16S amplicon-sequencing to reconstruct bacterial communities of different root classes (crown and primary) and root zones (apical, sub-apical and basal). We found both drought and heat affect the structure of rhizosphere bacterial communities. The combination of these stressors also influenced the structure of rhizosphere microbial communities, but this effect did not differ compared to the single stresses. Interestingly, we found differences in microbial communities inhabiting the rhizosphere of crown and primary roots in the control treatment, but this difference disappeared once stresses were applied. Stress also lead to an increased abundance of beneficial organisms.
Interactions between plants and microbiomes play a key role in ecosystem functioning and are of broad interest due to their influence on nutrient cycling and plant protection. However, we do not yet have a complete understanding of how plant microbiomes are assembled. Here, we tested and quantified the effect of different factors driving the diversity and composition of plant-associated microbial communities. We manipulated soil microbial diversity (high or low diversity), plant species (Solanum tuberosum or S. vernei), and herbivory (presence or absence of a phloem-feeding insect, Macrosiphum euphorbiae) and found that soil microbial diversity influenced the herbivore-associated microbiome composition but also plant species and herbivory influenced the soil microbiome composition. We quantified the relative strength of these effects and demonstrated that the initial soil microbiome diversity explained the most variation in plant- and herbivore-associated microbial communities. Our findings strongly suggest that soil microbial community diversity is a driver of the composition of multiple associated microbiomes (plant and insect), and this has implications for the importance of management of soil microbiomes in multiple systems.
Plant-associated microbiomes assist their host in a variety of activities, spanning from nutrition to defence against herbivores and diseases. Previous research showed that plant-associated microbiomes shift their composition when plants are exposed to stressors, including herbivory. However, existing studies explored only single herbivore-plant combinations, whereas plants are often attacked by several different herbivores, but the effects of multiple herbivore types on the plant microbiome remain to be determined. Here, we first tested whether feeding by different herbivores (aphids, nematodes and slugs) produces a shift in the rhizosphere bacterial microbiota associated with potato plants. Then, we expanded this question asking whether the identity of the herbivore produces different effects on the rhizosphere microbial community. While we found shifts in microbial diversity and structure due to herbivory, we observed that the herbivore identity does not influence the diversity or community structure of bacteria thriving in the rhizosphere. However, a deeper analysis revealed that the herbivores differentially affected the structure of the network of microbial co-occurrences. Our results have the potential to increase our ability to predict how plant microbiomes assemble and aid our understanding of the role of plant microbiome in plant responses to biotic stress.
Biological invasions impact both agricultural and natural systems. The damage can be quantified in terms of both economic loss and reduction of biodiversity. Although the literature is quite rich about the impact of invasive species on plant and animal communities, their impact on environmental microbiomes is underexplored. Here, we re-analyze publicly available data using a common framework to create a global synthesis of the effects of biological invasions on environmental microbial communities. Our findings suggest that non-native species are responsible for the loss of microbial diversity and shifts in the structure of microbial populations. Therefore, the impact of biological invasions on native ecosystems might be more pervasive than previously thought, influencing both macro- and micro-biomes. We also identified gaps in the literature which encourage research on a wider variety of environments and invaders, and the influence of invaders across seasons and geographical ranges.
Climate change is altering the interactions among plants and soil organisms in ways that will alter the structure and function of ecosystems. We reviewed the literature and developed a map of studies focused on how the three most common types of mycorrhizal fungi (arbuscular mycorrhizal [AM], ectomycorrhizal [EcM], and ericoid mycorrhizal [ErM] fungi) respond to elevated atmospheric carbon dioxide concentrations (eCO(2)), climatic warming, and changes in the distribution of precipitation. Broadly, we ask how do mycorrhizal fungi respond to climate change, how do these responses vary by fungal type, and how do mycorrhizal traits influence plant adaptation, movement, or extinction in response to climatic change? First, we found that 92% of studies were conducted in the northern hemisphere, and plant host, ecosystem type and study location were only correlated with each other in the northern hemisphere because studies across all mycorrhizal fungal types were only common in the northern hemisphere. Second, we show that temperature and rainfall variability had more variable effects than eCO(2) on mycorrhizal fungal structures, but these effects were context dependent. Third, while mycorrhizal fungal types vary in their responses to climate change, it appears that warming leads to more variable responses in ectomycorrhizal than in arbuscular mycorrhizal fungi. Finally, we discuss common traits of mycorrhizal fungi that could aid in fungal and plant adaption to climate change. We posit that mycorrhizal fungi can buffer plant hosts against extinction risk, they can facilitate or retard the dispersal success of plants moving away from poor environments, and, by buffering host plants, they can enable host plant adaptation to new climates. All of these influences are, however, context dependent a finding that reflects the complex traits of mycorrhizal fungi as a group, the diversity of plant species they associate with and the variation in ecosystems in which they reside. Overall, while we point out many gaps in our understanding of the influence of climate changes on mycorrhizal fungi, we also highlight the large number of opportunities for researching plant and mycorrhizal fungal responses to and mitigation of climate changes.
Spore size, colour and melanin content are hypothesised to be functional in relation to environmental stress. Here, we studied AM fungal spores in arid environments of Australia and in an experimental platform simulating altered rainfall. We used microscopy and image analysis to measure spore colour and size, and a quantitative colorimetric assay to estimate melanin content in spores. In arid sites, melanin content tended to increase with increasing aridity. We observed a large range of spore colours at all sites but found a higher proportion of both dark and light spores, and fewer intermediate colours, in drier sites. Spore abundance and size varied among sites, but neither were related to aridity. In the experimental platform established in a grassland, we found no evidence that altered rainfall influenced spore traits. This study identifies traits associated with environmental stress to inform future work into AM fungal life history and assembly processes.