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Quantifying the abundances of fungi is key to understanding natural variation in mycorrhizal communities in relation to plant ecophysiology and environmental heterogeneity. High-throughput metabarcoding approaches have transformed our ability to characterize and compare complex mycorrhizal communities. However, it remains unclear how well metabarcoding read counts correlate with actual read abundances in the sample, potentially limiting their use as a proxy for species abundances. Here, we use droplet digital PCR (ddPCR) to evaluate the reliability of ITS2 metabarcoding data for quantitative assessments of mycorrhizal communities in the orchid species Neottia ovata sampled at multiple sites. We performed specific ddPCR assays for eight families of orchid mycorrhizal fungi and compared the results with read counts obtained from metabarcoding. Our results demonstrate a significant correlation between DNA copy numbers measured by ddPCR assays and metabarcoding read counts of major mycorrhizal partners of N. ovata, highlighting the usefulness of metabarcoding for quantifying the abundance of orchid mycorrhizal fungi. Yet, the levels of correlation between the two methods and the numbers of false zero values varied across fungal families, which warrants cautious evaluation of the reliability of low-abundance families. This study underscores the potential of metabarcoding data for more quantitative analyses of mycorrhizal communities and presents practical workflows for metabarcoding and ddPCR to achieve a more comprehensive understanding of orchid mycorrhizal communities.
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Stable isotope signatures of fungal sporocarps have been instrumental in identifying carbon gains of chlorophyllous orchids from a fungal source. Yet, not all mycorrhizal fungi produce macroscopic sporocarps and frequently fungi of different taxa occur in parallel in orchid roots. To overcome this obstacle, we investigated stable isotope signatures of fungal pelotons extracted from orchid roots and compared these data to the respective orchid and reference plant tissues. Anoectochilus sandvicensis and Epipactis palustris represented specialized or unspecialized rhizoctonia-associated orchids. Epipactis atrorubens and Epipactis leptochila are orchids considered ectomycorrhiza-associated with different preferences for Basidio- and Ascomycota. 13 C enrichment of rhizoctonia pelotons was minor compared with plant tissues and significantly lower than enrichments of pelotons from ectomycorrhizal Epipactis species. 15 N values of pelotons from E. leptochila and E. atrorubens showed similar patterns as known for respective sporocarps of ectomycorrhizal Ascomycota and Basidiomycota, however, with an offset towards lower 15 N enrichments and nitrogen concentrations. Our results suggest an explicit fungal nutrition source of orchids associated with ectomycorrhizal fungi, whereas the low 13 C enrichment in rhizoctonia-associated orchids and fungal pelotons hamper the detection of carbon gains from fungal partners. 15 N isotopic pattern of orchids further suggests a selective transfer of 15 N-enriched protein-nitrogen into orchids.
Assuntos
Micorrizas , Orchidaceae , Isótopos de Carbono/análise , Isótopos de Nitrogênio/análise , Carbono , Nitrogênio , Orchidaceae/microbiologia , Rhizoctonia , Simbiose , FilogeniaRESUMO
How mycoheterotrophic plants that obtain carbon and soil nutrients from fungi are integrated in the usually mutualistic arbuscular mycorrhizal networks is unknown. Here, we compare autotrophic and mycoheterotrophic plant associations with arbuscular mycorrhizal fungi and use network analysis to investigate interaction preferences in the tripartite network. We sequenced root tips from autotrophic and mycoheterotrophic plants to assemble the combined tripartite network between autotrophic plants, mycorrhizal fungi and mycoheterotrophic plants. We compared plant-fungi interactions between mutualistic and antagonist networks, and searched for a diamond-like module defined by a mycoheterotrophic and an autotrophic plant interacting with the same pair of fungi to investigate whether pairs of fungi simultaneously linked to plant species from each interaction type were overrepresented throughout the network. Mycoheterotrophic plants as a group interacted with a subset of the fungi detected in autotrophs but are indirectly linked to all autotrophic plants, and fungi with a high overlap in autotrophic partners tended to interact with a similar set of mycoheterotrophs. Moreover, pairs of fungi sharing the same mycoheterotrophic and autotrophic plant species are overrepresented in the network. We hypothesise that the maintenance of antagonistic interactions is maximised by targeting well linked mutualistic fungi, thereby minimising the risk of carbon supply shortages.
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Micorrizas , Processos Autotróficos , Carbono , Fungos , Plantas , SimbioseRESUMO
Mycorrhizal fungi are central to the biology of land plants. However, to what extent mycorrhizal shifts - broad evolutionary transitions in root-associated fungal symbionts - are related to changes in plant trophic modes remains poorly understood. We built a comprehensive DNA dataset of Orchidaceae fungal symbionts and a dated plant molecular phylogeny to test the hypothesis that shifts in orchid trophic modes follow a stepwise pattern, from autotrophy over partial mycoheterotrophy (mixotrophy) to full mycoheterotrophy, and that these shifts are accompanied by switches in fungal symbionts. We estimate that at least 17 independent shifts from autotrophy towards full mycoheterotrophy occurred in orchids, mostly through an intermediate state of partial mycoheterotrophy. A wide range of fungal partners was inferred to occur in the roots of the common ancestor of this family, including 'rhizoctonias', ectomycorrhizal, and wood- or litter-decaying saprotrophic fungi. Phylogenetic hypothesis tests further show that associations with ectomycorrhizal or saprotrophic fungi were most likely a prerequisite for evolutionary shifts towards full mycoheterotrophy. We show that shifts in trophic mode often coincided with switches in fungal symbionts, suggesting that the loss of photosynthesis selects for different fungal communities in orchids. We conclude that changes in symbiotic associations and ecophysiological traits are tightly correlated throughout the diversification of orchids.
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Micorrizas , Orchidaceae , Evolução Biológica , Filogenia , SimbioseRESUMO
Testing of ecological, biogeographical and phylogenetic hypotheses of mycorrhizal traits requires a comprehensive reference dataset about plant mycorrhizal associations. Here we present a database, FungalRoot, which summarizes publicly available data about vascular plant mycorrhizal type and intensity of root colonization by mycorrhizal fungi, accompanied with rich metadata. We compiled and digitized data about plant mycorrhizal colonization in nine widespread languages. The present version of the FungalRoot database contains 36 303 species-by-site observations for 14 870 plant species, tripling the previously available compiled information about plant mycorrhizal associations. Based on these data, we provide a recommended list of genus-level plant mycorrhizal associations, based on the majority of data for species and careful analysis of conflicting data. The majority of ectomycorrhizal and ericoid mycorrhizal plants are trees (92%) and shrubs (85%), respectively. The majority of arbuscular and nonmycorrhizal plant species are herbaceous (50% and 70%, respectively). Our publicly available database is a powerful resource for mycorrhizal scientists and ecologists. It features possibilities for dynamic updating and addition of data about plant mycorrhizal associations. The new database will promote research on plant and fungal biogeography and evolution, and on links between above- and belowground biodiversity and ecosystem functioning.
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Micorrizas , Biodiversidade , Ecossistema , Filogenia , Raízes de Plantas , PlantasRESUMO
Hundreds of nonphotosynthetic mycoheterotrophic plant species cheat the arbuscular mycorrhizal symbiosis. Their patchy local occurrence suggests constraints by biotic and abiotic factors, among which the role of soil chemistry and nutrient status has not been investigated. Here, we examine the edaphic drivers predicting the local-scale distribution of mycoheterotrophic plants in two lowland rainforests in South America. We compared soil chemistry and nutrient status in plots where mycoheterotrophic plants were present with those without these plants. Soil pH, soil nitrate, and the interaction between soil potassium and nitrate concentrations were the best predictors for the occurrence of mycoheterotrophic plants in these tropical rainforests. Mycoheterotrophic plant occurrences decreased with a rise in each of these predictors. This indicates that these plants are associated with low-fertility patches. Such low-fertility conditions coincide with conditions that potentially favour a weak mutualism between plants and arbuscular mycorrhizal fungi according to the trade balance model. Our study points out which soil properties favour the cheating of arbuscular mycorrhizal networks in tropical forests. The patchy occurrence of mycoheterotrophic plants suggests that local soil heterogeneity causes the stability of arbuscular mycorrhizal networks to vary at a very small scale.
Assuntos
Micorrizas/fisiologia , Floresta Úmida , Simbiose/fisiologia , Modelos Lineares , Análise de Componente Principal , Solo , Microbiologia do SoloAssuntos
Micorrizas , Orchidaceae , Rhizoctonia , Hifas , Raízes de Plantas/microbiologia , Isótopos , Orchidaceae/microbiologia , SimbioseRESUMO
In general, plants and arbuscular mycorrhizal (AM) fungi exchange photosynthetically fixed carbon for soil nutrients, but occasionally nonphotosynthetic plants obtain carbon from AM fungi. The interactions of these mycoheterotrophic plants with AM fungi are suggested to be more specialized than those of green plants, although direct comparisons are lacking. We investigated the mycorrhizal interactions of both green and mycoheterotrophic plants. We used next-generation DNA sequencing to compare the AM communities from roots of five closely related mycoheterotrophic species of Thismia (Thismiaceae), roots of surrounding green plants, and soil, sampled over the entire temperate distribution of Thismia in Australia and New Zealand. We observed that the fungal communities of mycoheterotrophic and green plants are phylogenetically more similar within than between these groups of plants, suggesting a specific association pattern according to plant trophic mode. Moreover, mycoheterotrophic plants follow a more restricted association with their fungal partners in terms of phylogenetic diversity when compared with green plants, targeting more clustered lineages of fungi, independent of geographic origin. Our findings demonstrate that these mycoheterotrophic plants target more narrow lineages of fungi than green plants, despite the larger fungal pool available in the soil, and thus they are more specialized towards mycorrhizal fungi than autotrophic plants.
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Processos Autotróficos , Fungos/fisiologia , Micorrizas/fisiologia , Orchidaceae/microbiologia , Sequência de Bases , Funções Verossimilhança , Filogenia , Solo , Especificidade da EspécieRESUMO
Co-flowering plant species commonly share flower visitors, and thus have the potential to influence each other's pollination. In this study we analysed 750 quantitative plant-pollinator networks from 28 studies representing diverse biomes worldwide. We show that the potential for one plant species to influence another indirectly via shared pollinators was greater for plants whose resources were more abundant (higher floral unit number and nectar sugar content) and more accessible. The potential indirect influence was also stronger between phylogenetically closer plant species and was independent of plant geographic origin (native vs. non-native). The positive effect of nectar sugar content and phylogenetic proximity was much more accentuated for bees than for other groups. Consequently, the impact of these factors depends on the pollination mode of plants, e.g. bee or fly pollinated. Our findings may help predict which plant species have the greatest importance in the functioning of plant-pollination networks.
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Flores/genética , Magnoliopsida/genética , Filogenia , Polinização , Animais , Abelhas , Dípteros , Modelos Biológicos , Néctar de Plantas/químicaRESUMO
The prevalence and potential functions of common mycorrhizal networks, or the 'wood-wide web', resulting from the simultaneous interaction of mycorrhizal fungi and roots of different neighbouring plants have been increasingly capturing the interest of science and society, sometimes leading to hyperbole and misinterpretation. Several recent reviews conclude that popular claims regarding the widespread nature of these networks in forests and their role in the transfer of resources and information between plants lack evidence. Here we argue that mycoheterotrophic plants associated with ectomycorrhizal or arbuscular mycorrhizal fungi require resource transfer through common mycorrhizal networks and thus are natural evidence for the occurrence and function of these networks, offering a largely overlooked window into this methodologically challenging underground phenomenon. The wide evolutionary and geographic distribution of mycoheterotrophs and their interactions with a broad phylogenetic range of mycorrhizal fungi indicate that common mycorrhizal networks are prevalent, particularly in forests, and result in net carbon transfer among diverse plants through shared mycorrhizal fungi. On the basis of the available scientific evidence, we propose a continuum of carbon transfer options within common mycorrhizal networks, and we discuss how knowledge on the biology of mycoheterotrophic plants can be instrumental for the study of mycorrhizal-mediated transfers between plants.
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Micorrizas , Plantas , Madeira , Micorrizas/fisiologia , Plantas/microbiologia , Madeira/microbiologia , Processos Heterotróficos , Simbiose , Raízes de Plantas/microbiologia , Carbono/metabolismo , FlorestasRESUMO
Merckx and Gomes introduce mycoheterotrophy, the ability of a plant to take up its carbon from a close fungal partner.
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Micorrizas , Orchidaceae , Simbiose , Evolução Biológica , CarbonoRESUMO
Fusarium is one of the most important fungal genera of plant pathogens that affect the cultivation of a wide range of crops. Agricultural losses caused by Fusariumoxysporumf.sp.cubense (Foc) directly affect the income, subsistence, and nourishment of thousands of farmers worldwide. For Viet Nam, predictions on the impact of Foc for the future are dramatic, with an estimated loss in the banana production area of 8% within the next five years and up to 71% within the next 25 years. In the current study, we applied a combined morphological-molecular approach to assess the taxonomic identity and phylogenetic position of the different Foc isolates collected in northern Viet Nam. In addition, we aimed to estimate the proportion of the different Fusarium races infecting bananas in northern Viet Nam. The morphology of the isolates was investigated by growing the collected Fusarium isolates on four distinct nutritious media (PDA, SNA, CLA, and OMA). Molecular phylogenetic relationships were inferred by sequencing partial rpb1, rpb2, and tef1a genes and adding the obtained sequences into a phylogenetic framework. Molecular characterization shows that c. 74% of the Fusarium isolates obtained from infected banana pseudostem tissue belong to F.tardichlamydosporum. Compared to F.tardichlamydosporum, F.odoratissimum accounts for c.10% of the Fusarium wilt in northern Viet Nam, demonstrating that Foc TR4 is not yet a dominant strain in the region. Fusariumcugenangense - considered to cause Race 2 infections among bananas - is only found in c. 10% of the tissue material that was obtained from infected Vietnamese bananas. Additionally, one of the isolates cultured from diseased bananas was phylogenetically not positioned within the F.oxysporum species complex (FOSC), but in contrast, fell within the Fusariumfujikuroi species complex (FFSC). As a result, a possible new pathogen for bananas may have been found. Besides being present on several ABB 'Tay banana', F.tardichlamydosporum was also derived from infected tissue of a wild Musalutea, showing the importance of wild bananas as a possible sink for Foc.
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Epiphytic orchids exhibit varying degrees of phorophyte tree specificity. We performed a pilot study to investigate why epiphytic orchids prefer or avoid certain trees. We selected two orchid species, Panisea uniflora and Bulbophyllum odoratissimum co-occurring in a forest habitat in southern China, where they showed a specific association with Quercus yiwuensis and Pistacia weinmannifolia trees, respectively. We analysed a number of environmental factors potentially influencing the relationship between orchids and trees. Difference in bark features, such as water holding capacity and pH were recorded between Q. yiwuensis and P. weinmannifolia, which could influence both orchid seed germination and fungal diversity on the two phorophytes. Morphological and molecular culture-based methods, combined with metabarcoding analyses, were used to assess fungal communities associated with studied orchids and trees. A total of 162 fungal species in 74 genera were isolated from bark samples. Only two genera, Acremonium and Verticillium, were shared by the two phorophyte species. Metabarcoding analysis confirmed the presence of significantly different fungal communities on the investigated tree and orchid species, with considerable similarity between each orchid species and its host tree, suggesting that the orchid-host tree association is influenced by the fungal communities of the host tree bark.
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Micorrizas/classificação , Orchidaceae/microbiologia , Casca de Planta/microbiologia , China , Ecossistema , Fungos/genética , Fungos/patogenicidade , Micobioma , Micorrizas/metabolismo , Projetos Piloto , Simbiose , ÁrvoresRESUMO
A new study shows that a plant gives less carbon to its root-associated mycorrhizal fungus when targeted by herbivores, but the fungus doesn't retaliate.
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Afídeos , Micorrizas , Animais , Carbono , Herbivoria , Nutrientes , SimbioseRESUMO
Organic farming is increasingly promoted as a means to reduce the environmental impact of artificial fertilizers, pesticides, herbicides, and antibiotics in conventional dairy systems. These factors potentially affect the microbial communities of the production stages (soil, silage, dung, and milk) of the entire farm cycle. However, understanding whether the microbiota representative of different production stages reflects different agricultural practices - such as conventional versus organic farming - is unknown. Furthermore, the translocation of the microbial community across production stages is scarcely studied. We sequenced the microbial communities of soil, silage, dung, and milk samples from organic and conventional dairy farms in the Netherlands. We found that community structure of soil fungi and bacteria significantly differed among soil types, but not between organic versus conventional farming systems. The microbial communities of silage also did not differ among conventional and organic systems. Nevertheless, the dung microbiota of cows and the fungal communities in the milk were significantly structured by agricultural practice. We conclude that, while the production stages of dairy farms seem to be disconnected in terms of microbial transfer, certain practices specific for each agricultural system, such as the content of diet and the use of antibiotics, are potential drivers of shifts in the cow's microbiota, including the milk produced. This may reflect differences in farm animal health and quality of dairy products depending on farming practices.
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BACKGROUND: Insect-associated microorganisms can provide a wide range of benefits to their host, but insect dependency on these microbes varies greatly. The origin and functionality of insect microbiomes is not well understood. Many caterpillars can harbor symbionts in their gut that impact host metabolism, nutrient uptake and pathogen protection. Despite our lack of knowledge on the ecological factors driving microbiome assemblages of wild caterpillars, they seem to be highly variable and influenced by diet and environment. Several recent studies have shown that shoot-feeding caterpillars acquire part of their microbiome from the soil. Here, we examine microbiomes of a monophagous caterpillar (Tyria jacobaeae) collected from their natural host plant (Jacobaea vulgaris) growing in three different environments: coastal dunes, natural inland grasslands and riverine grasslands, and compare the bacterial communities of the wild caterpillars to those of soil samples collected from underneath each of the host plants from which the caterpillars were collected. RESULTS: The microbiomes of the caterpillars were dominated by Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes. Only 5% of the total bacterial diversity represented 86.2% of the total caterpillar's microbiome. Interestingly, we found a high consistency of dominant bacteria within the family Burkholderiaceae in all caterpillar samples across the three habitats. There was one amplicon sequence variant belonging to the genus Ralstonia that represented on average 53% of total community composition across all caterpillars. On average, one quarter of the caterpillar microbiome was shared with the soil. CONCLUSIONS: We found that the monophagous caterpillars collected from fields located more than 100 km apart were all dominated by a single Ralstonia. The remainder of the bacterial communities that were present resembled the local microbial communities in the soil in which the host plant was growing. Our findings provide an example of a caterpillar that has just a few key associated bacteria, but that also contains a community of low abundant bacteria characteristic of soil communities.
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Fungi have crucial roles in ecosystems, and are important associates for many organisms. They are adapted to a wide variety of habitats, however their global distribution and diversity remains poorly documented. The exponential growth of DNA barcode information retrieved from the environment is assisting considerably the traditional ways for unraveling fungal diversity and detection. The raw DNA data in association to environmental descriptors of metabarcoding studies are made available in public sequence read archives. While this is potentially a valuable source of information for the investigation of Fungi across diverse environmental conditions, the annotation used to describe environment is heterogenous. Moreover, a uniform processing pipeline still needs to be applied to the available raw DNA data. Hence, a comprehensive framework to analyses these data in a large context is still lacking. We introduce the MycoDiversity DataBase, a database which includes public fungal metabarcoding data of environmental samples for the study of biodiversity patterns of Fungi. The framework we propose will contribute to our understanding of fungal biodiversity and aims to become a valuable source for large-scale analyses of patterns in space and time, in addition to assisting evolutionary and ecological research on Fungi.
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Código de Barras de DNA Taxonômico , Ecossistema , Biodiversidade , Fungos/genéticaRESUMO
Biological invasions can have various impacts on the diversity of important microbial mutualists such as mycorrhizal fungi, but few studies have tested whether the effects of invasions on mycorrhizal diversity are consistent across spatial gradients. Furthermore, few of these studies have taken place in tropical ecosystems that experience an inordinate rate of invasions into native habitats. Here, we examined the effects of plant invasions dominated by non-native tree species on the diversity of arbuscular mycorrhizal (AM) fungi in Hawaii. To test the hypothesis that invasions result in consistent changes in AM fungal diversity across spatial gradients relative to native forest habitats, we sampled soil in paired native and invaded sites from three watersheds and used amplicon sequencing to characterize AM fungal communities. Whether our analyses considered phylogenetic relatedness or not, we found that invasions consistently increased the richness of AM fungi. However, AM fungal species composition was not related to invasion status of the vegetation nor local environment, but stratified by watershed. Our results suggest that while invasions can lead to an overall increase in the diversity of microbial mutualists, the effects of plant host identity or geographic structuring potentially outweigh those of invasive species in determining the community membership of AM fungi. Thus, host specificity and spatial factors such as dispersal need to be taken into consideration when examining the effects of biological invasions on symbiotic microbes.
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The vast majority of plants obtain an important proportion of vital resources from soil through mycorrhizal fungi. Generally, this happens in exchange of photosynthetically fixed carbon, but occasionally the interaction is mycoheterotrophic, and plants obtain carbon from mycorrhizal fungi. This process results in an antagonistic interaction between mycoheterotrophic plants and their fungal hosts. Importantly, the fungal-host diversity available for plants is restricted as mycoheterotrophic interactions often involve narrow lineages of fungal hosts. Unfortunately, little is known whether fungal-host diversity may be additionally modulated by plant-plant interactions through shared hosts. Yet, this may have important implications for plant competition and coexistence. Here, we use DNA sequencing data to investigate the interaction patterns between mycoheterotrophic plants and arbuscular mycorrhizal fungi. We find no phylogenetic signal on the number of fungal hosts nor on the fungal hosts shared among mycoheterotrophic plants. However, we observe a potential trend toward increased phylogenetic diversity of fungal hosts among mycoheterotrophic plants with increasing overlap in their fungal hosts. While these patterns remain for groups of plants regardless of location, we do find higher levels of overlap and diversity among plants from the same location. These findings suggest that species coexistence cannot be fully understood without attention to the two sides of ecological interactions.