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Fungi are among the most diverse and ecologically important kingdoms in life. However, the distributional ranges of fungi remain largely unknown as do the ecological mechanisms that shape their distributions1,2. To provide an integrated view of the spatial and seasonal dynamics of fungi, we implemented a globally distributed standardized aerial sampling of fungal spores3. The vast majority of operational taxonomic units were detected within only one climatic zone, and the spatiotemporal patterns of species richness and community composition were mostly explained by annual mean air temperature. Tropical regions hosted the highest fungal diversity except for lichenized, ericoid mycorrhizal and ectomycorrhizal fungi, which reached their peak diversity in temperate regions. The sensitivity in climatic responses was associated with phylogenetic relatedness, suggesting that large-scale distributions of some fungal groups are partially constrained by their ancestral niche. There was a strong phylogenetic signal in seasonal sensitivity, suggesting that some groups of fungi have retained their ancestral trait of sporulating for only a short period. Overall, our results show that the hyperdiverse kingdom of fungi follows globally highly predictable spatial and temporal dynamics, with seasonality in both species richness and community composition increasing with latitude. Our study reports patterns resembling those described for other major groups of organisms, thus making a major contribution to the long-standing debate on whether organisms with a microbial lifestyle follow the global biodiversity paradigms known for macroorganisms4,5.
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Microbiologia do Ar , Biodiversidade , DNA Fúngico , Fungos , Estações do Ano , Análise Espaço-Temporal , DNA Fúngico/análise , DNA Fúngico/genética , Fungos/genética , Fungos/classificação , Fungos/isolamento & purificação , Micorrizas/genética , Micorrizas/classificação , Micorrizas/isolamento & purificação , Filogenia , Esporos Fúngicos/classificação , Esporos Fúngicos/isolamento & purificação , Temperatura , Clima Tropical , Mapeamento GeográficoRESUMO
Genomic traits reflect the evolutionary processes that have led to ecological variation among extant organisms, including variation in how they acquire and use resources. Soil fungi have diverse nutritional strategies and exhibit extensive variation in fitness along resource gradients. We tested for trade-offs in genomic traits with mycelial nutritional traits and hypothesize that such trade-offs differ among fungal guilds as they reflect contrasting resource exploitation and habitat preferences. We found species with large genomes exhibited nutrient-poor mycelium and low GC content. These patterns were observed across fungal guilds but with varying explanatory power. We then matched trait data to fungal species observed in 463 Australian grassland, woodland and forest soil samples. Fungi with large genomes and lower GC content dominated in nutrient-poor soils, associated with shifts in guild composition and with species turnover within guilds. These findings highlight fundamental mechanisms that underpin successful ecological strategies for soil fungi.
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Evolução Biológica , Micorrizas , Austrália , Fertilidade , Genoma Fúngico , Solo , Microbiologia do Solo , Fungos/genética , EcossistemaRESUMO
Despite host-fungal symbiotic interactions being ubiquitous in all ecosystems, understanding how symbiosis has shaped the ecology and evolution of fungal spores that are involved in dispersal and colonization of their hosts has been ignored in life-history studies. We assembled a spore morphology database covering over 26,000 species of free-living to symbiotic fungi of plants, insects and humans and found more than eight orders of variation in spore size. Evolutionary transitions in symbiotic status correlated with shifts in spore size, but the strength of this effect varied widely among phyla. Symbiotic status explained more variation than climatic variables in the current distribution of spore sizes of plant-associated fungi at a global scale while the dispersal potential of their spores is more restricted compared to free-living fungi. Our work advances life-history theory by highlighting how the interaction between symbiosis and offspring morphology shapes the reproductive and dispersal strategies among living forms.
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Micorrizas , Simbiose , Animais , Humanos , Ecossistema , Fungos , Insetos , Plantas , Esporos FúngicosRESUMO
Drought causes soil feedback effects on plant performance. However, how the linkages between conditioned soil biota and root traits contribute to explain plant-soil feedback (PSF) as a function of drought is unknown. We utilized soil inoculum from a conditioning experiment where grassland species grew under well-watered and drought conditions, and their soil fungi were analyzed. Under well-watered conditions, we grew 21 grassland species with those inocula from either conspecific or heterospecific soils. At harvest, plant biomass and root traits were measured. Negative PSF (higher biomass in heterospecific than in conspecific soils) was predominant, and favored in drought-conditioned soils. Previous drought affected the relationship between root traits and fungal groups. Specific root surface area (SRSA) was higher in heterospecific than in conspecific droughted soils and was linked to an increase in saprotroph richness. Overall, root diameter was higher in conspecific soils and was linked to mutualist and pathogen composition, whereas the decrease of root : shoot in heterospecific soils was linked to pathogenic fungi. Drought legacy affects biomass and root morphological traits via conditioned soil biota, even after the drought conditions have disappeared. This provides new insights into the role that soil biota have modulating PSF responses to drought.
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Secas , Solo , Biomassa , Biota , Retroalimentação , Plantas , Solo/química , ÁguaRESUMO
Root traits respond to drought in a species-specific manner, but little is known about how soil fungal communities and root traits respond to drought in concert. In a glasshouse experiment, we determined the response of soil pathogens, saprotrophs, and mutualistic and all fungi associated with the roots of 24 plant species subjected to drought. At harvest, soil fungal communities were characterized by sequencing. Data on root traits were extracted from a previously published work. Differences in fungal beta diversity between drought and control were plant species specific. For some species, saprotrophic fungi increased in relative abundance and richness with drought, whereas mutualistic fungi showed the opposite pattern. Community structure of pathogenic fungi was plant species specific but was slightly affected by drought. Pathogen composition was correlated with specific root surface area and root : shoot, saprotroph abundance with root tissue density, whereas mutualist composition was correlated with root : shoot. All these were the fungal attributes that best predicted shoot mass. Fungal response to drought depended highly on the fungal group and was related to root trait adjustments to water scarcity. This provides new insights into the role that root trait adjustments to drought may have in modulating plant-fungus interactions in grasslands ecosystems.
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Micobioma , Secas , Ecossistema , Fungos , Raízes de Plantas , Solo , Microbiologia do SoloRESUMO
In the current era of Big Data, existing synthesis tools such as formal meta-analyses are critical means to handle the deluge of information. However, there is a need for complementary tools that help to (a) organize evidence, (b) organize theory, and (c) closely connect evidence to theory. We present the hierarchy-of-hypotheses (HoH) approach to address these issues. In an HoH, hypotheses are conceptually and visually structured in a hierarchically nested way where the lower branches can be directly connected to empirical results. Used for organizing evidence, this tool allows researchers to conceptually connect empirical results derived through diverse approaches and to reveal under which circumstances hypotheses are applicable. Used for organizing theory, it allows researchers to uncover mechanistic components of hypotheses and previously neglected conceptual connections. In the present article, we offer guidance on how to build an HoH, provide examples from population and evolutionary biology and propose terminological clarifications.
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A recent study by Sugiura and coworkers reported the non-symbiotic growth and spore production of an arbuscular mycorrhizal (AM) fungus, Rhizophagus irregularis, when the fungus received an external supply of certain fatty acids, myristates (C:14). This discovery follows the insight that AM fungi receive fatty acids from their hosts when in symbiosis. If this result holds up and can be repeated under nonsterile conditions and with a broader range of fungi, it has numerous consequences for our understanding of AM fungal ecology, from the level of the fungus, at the plant community level, and to functional consequences in ecosystems. In addition, myristate may open up several avenues from a more applied perspective, including improved fungal culture and supplementation of AM fungi or inoculum in the field. We here map these potential opportunities, and additionally offer thoughts on potential risks of this potentially new technology. Lastly, we discuss the specific research challenges that need to be overcome to come to an understanding of the potential role of myristate in AM ecology.
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Glomeromycota , Micorrizas , Ecossistema , Fungos , Miristatos , Ácido Mirístico , Raízes de Plantas , SimbioseRESUMO
Established ecological theory has focused on unitary organisms, and thus its concepts have matured into a form that often hinders rather than facilitates the ecological study of modular organisms. Here, we use the example of filamentous fungi to develop concepts that enable integration of non-unitary (modular) organisms into the established community ecology theory, with particular focus on its spatial aspects. In doing so, we provide a link between fungal community ecology and modern coexistence theory (MCT). We first show how community processes and predictions made by MCT can be used to define meaningful scales in fungal ecology. This leads to the novel concept of the unit of community interactions (UCI), a promising conceptual tool for applying MCT to communities of modular organisms with indeterminate clonal growth and hierarchical individuality. We outline plausible coexistence mechanisms structuring fungal communities, and show at what spatial scales and in what habitats they are most likely to act. We end by describing challenges and opportunities for empirical and theoretical research in fungal competitive coexistence.
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Trait-based frameworks are promising tools to understand the functional consequences of community shifts in response to environmental change. The applicability of these tools to soil microbes is limited by a lack of functional trait data and a focus on categorical traits. To address this gap for an important group of soil microorganisms, we identify trade-offs underlying a fungal economics spectrum based on a large trait collection in 28 saprobic fungal isolates, derived from a common grassland soil and grown in culture plates. In this dataset, ecologically relevant trait variation is best captured by a three-dimensional fungal economics space. The primary explanatory axis represents a dense-fast continuum, resembling dominant life-history trade-offs in other taxa. A second significant axis reflects mycelial flexibility, and a third one carbon acquisition traits. All three axes correlate with traits involved in soil carbon cycling. Since stress tolerance and fundamental niche gradients are primarily related to the dense-fast continuum, traits of the 2nd (carbon-use efficiency) and especially the 3rd (decomposition) orthogonal axes are independent of tested environmental stressors. These findings suggest a fungal economics space which can now be tested at broader scales.
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Micélio , Solo , Fungos , Carbono , Microbiologia do Solo , EcossistemaRESUMO
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.
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Fungos/fisiologia , Plantas/microbiologia , Animais , Bases de Dados Factuais , Ecossistema , Fungos/genéticaRESUMO
Movement ecology aims to provide common terminology and an integrative framework of movement research across all groups of organisms. Yet such work has focused on unitary organisms so far, and thus the important group of filamentous fungi has not been considered in this context. With the exception of spore dispersal, movement in filamentous fungi has not been integrated into the movement ecology field. At the same time, the field of fungal ecology has been advancing research on topics like informed growth, mycelial translocations, or fungal highways using its own terminology and frameworks, overlooking the theoretical developments within movement ecology. We provide a conceptual and terminological framework for interdisciplinary collaboration between these two disciplines, and show how both can benefit from closer links: We show how placing the knowledge from fungal biology and ecology into the framework of movement ecology can inspire both theoretical and empirical developments, eventually leading towards a better understanding of fungal ecology and community assembly. Conversely, by a greater focus on movement specificities of filamentous fungi, movement ecology stands to benefit from the challenge to evolve its concepts and terminology towards even greater universality. We show how our concept can be applied for other modular organisms (such as clonal plants and slime molds), and how this can lead towards comparative studies with the relationship between organismal movement and ecosystems in the focus.
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Offspring size is a key trait for understanding the reproductive ecology of species, yet studies addressing the ecological meaning of offspring size have so far been limited to macro-organisms. We consider this a missed opportunity in microbial ecology and provide what we believe is the first formal study of offspring-size variation in microbes using reproductive models developed for macro-organisms. We mapped the entire distribution of fungal spore size in the arbuscular mycorrhizal (AM) fungi (subphylum Glomeromycotina) and tested allometric expectations of this trait to offspring (spore) output and body size. Our results reveal a potential paradox in the reproductive ecology of AM fungi: while large spore-size variation is maintained through evolutionary time (independent of body size), increases in spore size trade off with spore output. That is, parental mycelia of large-spored species produce fewer spores and thus may have a fitness disadvantage compared to small-spored species. The persistence of the large-spore strategy, despite this apparent fitness disadvantage, suggests the existence of advantages to large-spored species that could manifest later in fungal life history. Thus, we consider that solving this paradox opens the door to fruitful future research establishing the relationship between offspring size and other AM life history traits.
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Glomeromycota/fisiologia , Micorrizas/fisiologia , Esporos Fúngicos/citologia , Evolução Biológica , Fenótipo , Filogenia , ReproduçãoRESUMO
All ecological disciplines consider temporal dynamics, although relevant concepts have been developed almost independently. We here introduce basic principles of temporal dynamics in ecology. We figured out essential features that describe temporal dynamics by finding similarities among about 60 ecological concepts and theories. We found that considering the hierarchically nested structure of complexity in temporal patterns (i.e. hierarchical complexity) can well describe the fundamental nature of temporal dynamics by expressing which patterns are observed at each scale. Across all ecological levels, driver-response relationships can be temporally variant and dependent on both short- and long-term past conditions. The framework can help with designing experiments, improving predictive power of statistics, and enhancing communications among ecological disciplines.
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Ecologia , EcossistemaRESUMO
Soils underpin terrestrial ecosystem functions, but they face numerous anthropogenic pressures. Despite their crucial ecological role, we know little about how soils react to more than two environmental factors at a time. Here, we show experimentally that increasing the number of simultaneous global change factors (up to 10) caused increasing directional changes in soil properties, soil processes, and microbial communities, though there was greater uncertainty in predicting the magnitude of change. Our study provides a blueprint for addressing multifactor change with an efficient, broadly applicable experimental design for studying the impacts of global environmental change.
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Microbiota , Microbiologia do Solo , SoloRESUMO
Understanding the effects of root-associated microbes in explaining plant community patterns represents a challenge in community ecology. Although typically overlooked, several lines of evidence point out that nonmycorrhizal, root endophytic fungi in the Ascomycota may have the potential to drive changes in plant community ecology given their ubiquitous presence, wide host ranges, and plant species-specific fitness effects. Thus, we experimentally manipulated the presence of root endophytic fungal species in microcosms and measured its effects on plant communities. Specifically, we tested whether (1) three different root endophyte species can modify plant community structure; (2) those changes can also modified the way plant respond to different soil types; and (3) the effects are modified when all the fungi are present. As a model system, we used plant and fungal species that naturally co-occur in a temperate grassland. Further, the soil types used in our experiment reflected a strong gradient in soil texture that has been shown to drive changes in plant and fungal community structure in the field. Results showed that each plant species responded differently to infection, resulting in distinct patterns of plant community structure depending on the identity of the fungus present. Those effects depended on the soil type. For example, large positive effects due to presence of the fungi were able to compensate for less nutrients levels in one soil type. Further, host responses when all three fungi were present were different from the ones observed in single fungal inoculations, suggesting that endophyte-endophyte interactions may be important in structuring plant communities. Overall, these results indicate that plant responses to changes in the species identity of nonmycorrhizal fungal community species and their interactions can modify plant community structure.