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Little is known about how community composition in the plant microbiome is affected by events in the life of a plant. For example, when the plant is exposed to soil, microbial communities may be an important factor in root community assembly. We conducted two experiments asking whether the composition of the root microbiota in mature plants could be determined by either the timing of root exposure to microbial communities or priority effects by early colonizing microbes. Timing of microbial exposure was manipulated through an inoculation experiment, where plants of different ages were exposed to a common soil inoculum. Priority effects were manipulated by challenging roots with established microbiota with an exogenous microbial community. Results show that even plants with existing microbial root communities were able to acquire new microbial associates, but that timing of soil exposure affected root microbiota composition for both bacterial and fungal communities in mature plants. Plants already colonized were only receptive to colonizers at 1 week post-germination. Our study shows that the timing of soil exposure in the early life stages of a plant is important for the development of the root microbiota in mature plants.
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Arbuscular mycorrhizal (AM) fungi play a key role in determining ecosystem functionality. Understanding how diversity in the fungal community affects plant productivity is therefore an important question in ecology. Current research has focused on understanding the role of functional complementarity in the fungal community when the host plant faces multiple stress factors. Fewer studies, however, have investigated how variation in traits affecting nutrient exchange can impact the plant growth dynamics, even in the absence of environmental stressors. Combining experimental data and a mathematical model based on ordinary differential equations, we investigate the role played by carbon sink strength on plant productivity. We simulate and measure plant growth over time when the plant is associated with two fungal isolates with different carbon sink strength, and when the plant is in pairwise association with each of the isolates alone. Overall, our theoretical as well as our experimental results show that co-inoculation with fungi with different carbon sink strength can induce positive non-additive effects (or synergistic effects) in plant productivity. Fungi with high carbon sink strength are able to quickly establish a fungal community and increase the nutrient supply to the plant, with a consequent positive impact on plant growth rate. On the other side, fungi with low carbon sink strength inflict lower carbon costs to the host plant, and support maximal plant productivity once plant biomass is large. As AM fungi are widely used as organic fertilizers worldwide, our findings have important implications for restoration ecology and agricultural management.
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Micorrizas , Biomasa , Carbono , Secuestro de Carbono , Ecosistema , Hongos , Raíces de Plantas , Suelo , Microbiología del SueloRESUMEN
That arbuscular mycorrhizal (AM) fungi covary with plant communities is clear, and many papers report nonrandom associations between symbiotic partners. However, these studies do not test the causal relationship, or 'codependency', whereby the composition of one guild affects the composition of the other. Here we outline underlying requirements for codependency, compare important drivers for both plant and AM fungal communities, and assess how host preference - a pre-requisite for codependency - changes across spatiotemporal scales and taxonomic resolution for both plants and AM fungi. We find few examples in the literature designed to test for codependency and those that do have been conducted within plots or mesocosms. Also, while plants and AM fungi respond similarly to coarse environmental filters, most variation remains unexplained, with host identity explaining less than 30% of the variation in AM fungal communities. These results combined question the likelihood of predictable co-occurrence, and therefore evolution of codependency, between plant and AM fungal taxa across locations. We argue that codependency is most likely to occur in homogeneous environments where specific plant - AM fungal pairings have functional consequences for the symbiosis. We end by outlining critical aspects to consider moving forward.
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Micobioma , Micorrizas , Codependencia Psicológica , Raíces de Plantas , Plantas , Microbiología del Suelo , SimbiosisRESUMEN
Biodiversity is an important component of healthy ecosystems, and thus understanding the mechanisms behind species coexistence is critical in ecology and conservation biology. In particular, few studies have focused on the dynamics resulting from the co-occurrence of mutualistic and competitive interactions within a group of species. Here we build a mathematical model to study the dynamics of a guild of competitors who are also engaged in mutualistic interactions with a common partner. We show that coexistence as well as competitive exclusion can occur depending on the competition strength and on strength of the mutualistic interactions, and we formulate concrete criteria for predicting invasion success of an alien mutualist based on propagule pressure, alien traits (such as its resource exchange ability) and composition of the recipient community. We find that intra guild diversity promotes the coexistence of species that would otherwise competitively exclude each other, and makes a guild less vulnerable to invasion. Our results can serve as a useful framework to predict the consequences of species manipulation in mutualistic communities.
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Biodiversidad , Especies Introducidas , Simbiosis , Ecología , Ecosistema , Dinámica PoblacionalRESUMEN
Estimating the abundance of arbuscular mycorrhizal fungi relies entirely on indirect methods, meaning all measures are associated with some variability. The most common methods use microscopic estimates of the relative proportion of root length colonized by fungal structures. These methods typically examine root subsamples. While such methods are inexpensive and relatively simple, significant variation within single root system means there is opportunity for sampling bias. We evaluated the two most common methods of percent root length colonization for AM fungi both as a subsample and for the entire root system of flax plants. We compared these measures to a novel technique that returns projected fungal surface area (fungal coverage), by using microphotography and imaging analysis. Both microscopic methods overestimated the colonization intensity compared to image analysis. Among the microscopic methods, the method which incorporated colonization intensity (Trouvelot) was significantly more similar to imaging method results, than the method that is based on the presence/absence of the fungus (McGonigle).
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Procesamiento de Imagen Asistido por Computador/métodos , Microscopía/métodos , Micorrizas/fisiología , Raíces de Plantas/microbiología , Lino/microbiología , Fotograbar/métodos , SimbiosisRESUMEN
In vitro propagation of AM fungi using transformed root cultures (TRC) is commonly used to obtain pure AM fungal propagules for use in research and industry. Early observations indicate that such an artificial environment can alter traits and function of AM fungi over time. We hypothesized that increased in vitro cultivation may promote ruderal strategies in fungi by enhancing propagule production and reducing mutualistic quality. To examine the effect of in vitro cultivation on the trait and function of AM fungi, we inoculated plants with 11 Rhizoglomus irregulare isolates which fell along a cultivation gradient spanning 80 generations. We harvested plants at 10, 20 and 30 d post inoculation to observe differences in fungal and plant traits post infection. In vitro cultivation led to increased spore production but reduced plant shoot phosphorus. Our results indicate that in vitro propagation may indirectly select for traits that affect symbiotic quality.
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Glomeromycota/fisiología , Micorrizas/fisiología , Raíces de Plantas/microbiología , Glomeromycota/crecimiento & desarrollo , Micorrizas/crecimiento & desarrollo , Fósforo/metabolismo , Raíces de Plantas/fisiología , Esporas Fúngicas/crecimiento & desarrollo , Esporas Fúngicas/fisiología , SimbiosisRESUMEN
We proposed a theoretical framework predicting mutualistic outcomes for the arbuscular mycorrhizal (AM) symbiosis based on host provenance (crop versus wild). To test the framework, we grew two isolates of Rhizoglomus irregulare (commercial versus an isolate locally isolated), with five crop plants and five wild plants endemic to the region that co-occur with the locally sourced fungus. While inoculation with either isolate had no effect on plant biomass, it decreased leaf P content, particularly for wild plants. All plants associating with the commercial fungus had lower leaf P. Overall, our data shows that wild plants may be more sensitive to differences in mutualistic quality among fungal isolates.
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Productos Agrícolas/microbiología , Micorrizas/fisiología , Biomasa , Glomeromycota/fisiología , Micelio/fisiología , Brotes de la Planta/microbiología , Esporas Fúngicas/fisiologíaRESUMEN
Cultivating arbuscular mycorrhizal (AM) fungi in vitro is an efficient way to produce material for industry and research. However, such artificial growing conditions may impose selective pressure on fungi grown in vitro over many generations. We hypothesized that isolates subjected to long term propagation in vitro may develop increasingly ruderal traits. We proposed a predictive framework for the effect of in vitro cultivation on asymbiotic AM fungal traits. Using photomicrography and image processing, we analyzed morphology and growth traits for 14 isolates representing an in vitro cultivation gradient from 0 to >80 generations in vitro. We investigated the range of trait variation among asymbiotic growth of arbuscular mycorrhizal (AM) fungus isolates (Rhizoglomus irregulare). Spore dormancy was strongly associated with in vitro cultivation. We observed extremely high levels of inter-isolate variation for most fungal traits, but this was not related to time in vitro. Our results indicate that intra-specific diversity may have a strong ecological role in AM fungal communities.
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Procesamiento de Imagen Asistido por Computador , Microscopía , Micorrizas/citología , Micorrizas/crecimiento & desarrollo , Variación Biológica Poblacional , Hifa/citología , Hifa/crecimiento & desarrollo , Esporas Fúngicas/citología , Esporas Fúngicas/crecimiento & desarrolloRESUMEN
Most plants engage in symbioses with mycorrhizal fungi in soils and net consequences for plants vary widely from mutualism to parasitism. However, we lack a synthetic understanding of the evolutionary and ecological forces driving such variation for this or any other nutritional symbiosis. We used meta-analysis across 646 combinations of plants and fungi to show that evolutionary history explains substantially more variation in plant responses to mycorrhizal fungi than the ecological factors included in this study, such as nutrient fertilization and additional microbes. Evolutionary history also has a different influence on outcomes of ectomycorrhizal versus arbuscular mycorrhizal symbioses; the former are best explained by the multiple evolutionary origins of ectomycorrhizal lifestyle in plants, while the latter are best explained by recent diversification in plants; both are also explained by evolution of specificity between plants and fungi. These results provide the foundation for a synthetic framework to predict the outcomes of nutritional mutualisms.
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[This corrects the article DOI: 10.1038/s42003-018-0120-9.].
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Plants interact simultaneously with each other and with soil biota, yet the relative importance of competition vs. plant-soil feedback (PSF) on plant performance is poorly understood. Using a meta-analysis of 38 published studies and 150 plant species, we show that effects of interspecific competition (either growing plants with a competitor or singly, or comparing inter- vs. intraspecific competition) and PSF (comparing home vs. away soil, live vs. sterile soil, or control vs. fungicide-treated soil) depended on treatments but were predominantly negative, broadly comparable in magnitude, and additive or synergistic. Stronger competitors experienced more negative PSF than weaker competitors when controlling for density (inter- to intraspecific competition), suggesting that PSF could prevent competitive dominance and promote coexistence. When competition was measured against plants growing singly, the strength of competition overwhelmed PSF, indicating that the relative importance of PSF may depend not only on neighbour identity but also density. We evaluate how competition and PSFs might interact across resource gradients; PSF will likely strengthen competitive interactions in high resource environments and enhance facilitative interactions in low-resource environments. Finally, we provide a framework for filling key knowledge gaps and advancing our understanding of how these biotic interactions influence community structure.
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Plantas , Microbiología del Suelo , Suelo , Biota , RetroalimentaciónRESUMEN
The ecological interactions that occur in and with soil are of consequence in many ecosystems on the planet. These interactions provide numerous essential ecosystem services, and the sustainable management of soils has attracted increasing scientific and public attention. Although soil ecology emerged as an independent field of research many decades ago, and we have gained important insights into the functioning of soils, there still are fundamental aspects that need to be better understood to ensure that the ecosystem services that soils provide are not lost and that soils can be used in a sustainable way. In this perspectives paper, we highlight some of the major knowledge gaps that should be prioritized in soil ecological research. These research priorities were compiled based on an online survey of 32 editors of Pedobiologia - Journal of Soil Ecology. These editors work at universities and research centers in Europe, North America, Asia, and Australia.The questions were categorized into four themes: (1) soil biodiversity and biogeography, (2) interactions and the functioning of ecosystems, (3) global change and soil management, and (4) new directions. The respondents identified priorities that may be achievable in the near future, as well as several that are currently achievable but remain open. While some of the identified barriers to progress were technological in nature, many respondents cited a need for substantial leadership and goodwill among members of the soil ecology research community, including the need for multi-institutional partnerships, and had substantial concerns regarding the loss of taxonomic expertise.
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Global comparisons reveal a decrease in gut microbiota diversity attributed to Western diets, lifestyle practices such as caesarian section, antibiotic use and formula-feeding of infants, and sanitation of the living environment. While gut microbial diversity is decreasing, the prevalence of chronic inflammatory diseases such as inflammatory bowel disease, diabetes, obesity, allergies and asthma is on the rise in Westernized societies. Since the immune system development is influenced by microbial components, early microbial colonization may be a key factor in determining disease susceptibility patterns later in life. Evidence indicates that the gut microbiota is vertically transmitted from the mother and this affects offspring immunity. However, the role of the external environment in gut microbiome and immune development is poorly understood. Studies show that growing up in microbe-rich environments, such as traditional farms, can have protective health effects on children. These health-effects may be ablated due to changes in the human lifestyle, diet, living environment and environmental biodiversity as a result of urbanization. Importantly, if early-life exposure to environmental microbes increases gut microbiota diversity by influencing patterns of gut microbial assembly, then soil biodiversity loss due to land-use changes such as urbanization could be a public health threat. Here, we summarize key questions in environmental health research and discuss some of the challenges that have hindered progress toward a better understanding of the role of the environment on gut microbiome development.
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Although arbuscular mycorrhizal (AM) fungi are obligate symbionts that can influence plant growth, the magnitude and direction of these effects are highly variable within fungal genera and even among isolates within species, as well as among plant taxa. To determine whether variability in AM fungal morphology and growth is correlated with AM fungal effects on plant growth, we established a common garden experiment with 56 AM fungal isolates comprising 17 genera and six families growing with three plant host species. Arbuscular mycorrhizal fungal morphology and growth was highly conserved among isolates of the same species and among species within a family. By contrast, plant growth response to fungal inoculation was highly variable, with the majority of variation occurring among different isolates of the same AM fungal species. Our findings show that host performance cannot be predicted from AM fungal morphology and growth traits. Divergent effects on plant growth among isolates within an AM fungal species may be caused by coevolution between co-occurring fungal and plant populations.
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Evolución Biológica , Glomeromycota/citología , Micorrizas/fisiología , Desarrollo de la Planta , Plantas/microbiología , Simbiosis , Filogenia , Carácter Cuantitativo Heredable , Especificidad de la EspecieRESUMEN
Arbuscular mycorrhizal fungi (AMF) are globally distributed, monophyletic root symbionts with ancient origins. Their contribution to carbon cycling and nutrient dynamics is ecologically important, given their obligate association with over 70% of vascular plant species. Current understanding of AMF species richness and community structure is based primarily on studies of grasses, herbs and agricultural crops, typically in disturbed environments. Few studies have considered AMF interactions with long-lived woody perennial species in undisturbed ecosystems. Here we examined AMF communities associated with roots and soils of young, mature and old western redcedar (Thuja plicata) at two sites in the old-growth temperate rainforests of British Columbia. Due to the unique biology of AMF, community richness and structure were assessed using a conservative, clade-based approach. We found 91 AMF OTUs across all samples, with significantly greater AMF richness in the southern site, but no differences in richness along the host chronosequence at either site. All host age classes harboured AMF communities that were overdispersed (more different to each other than expected by chance), with young tree communities most resembling old tree communities. A comparison with similar clade richness data obtained from the literature indicates that western redcedar AMF communities are as rich as those of grasses, tropical trees and palms. Our examination of undisturbed temperate old-growth rainforests suggests that priority effects, rather than succession, are an important aspect of AMF community assembly in this ecosystem.
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Micorrizas/clasificación , Microbiología del Suelo , Simbiosis , Thuja/microbiología , Biodiversidad , Colombia Británica , Hongos/clasificación , Raíces de Plantas/microbiología , Bosque Lluvioso , SueloRESUMEN
Feedback with soil biota is an important determinant of terrestrial plant diversity. However, the factors regulating plant-soil feedback, which varies from positive to negative among plant species, remain uncertain. In a large-scale study involving 55 species and 550 populations of North American trees, the type of mycorrhizal association explained much of the variation in plant-soil feedbacks. In soil collected beneath conspecifics, arbuscular mycorrhizal trees experienced negative feedback, whereas ectomycorrhizal trees displayed positive feedback. Additionally, arbuscular mycorrhizal trees exhibited strong conspecific inhibition at multiple spatial scales, whereas ectomycorrhizal trees exhibited conspecific facilitation locally and less severe conspecific inhibition regionally. These results suggest that mycorrhizal type, through effects on plant-soil feedbacks, could be an important contributor to population regulation and community structure in temperate forests.
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Retroalimentación Fisiológica , Bosques , Micorrizas/fisiología , Microbiología del Suelo , Árboles/fisiología , Dinámica Poblacional , Simbiosis , Árboles/microbiologíaRESUMEN
Despite the importance of arbuscular mycorrhizal (AM) fungi within terrestrial ecosystems, we know little about how natural AM fungal communities are structured. To date, the majority of studies examining AM fungal community diversity have focused on single habitats with similar environmental conditions, with relatively few studies having assessed the diversity of AM fungi over large-scale environmental gradients. In this study, we characterized AM fungal communities in the soil along a high-elevation gradient in the North American Rocky Mountains. We focused on phylogenetic patterns of AM fungal communities to gain insight into how AM fungal communities are naturally assembled. We found that alpine AM fungal communities had lower phylogenetic diversity relative to lower elevation communities, as well as being more heterogeneous in composition than either treeline or subalpine communities. AM fungal communities were phylogenetically clustered at all elevations sampled, suggesting that environmental filtering, either selection by host plants or fungal niches, is the primary ecological process structuring communities along the gradient.
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Micorrizas/clasificación , Análisis de Secuencia de ARN/métodos , Microbiología del Suelo , Aclimatación , Ecosistema , Micorrizas/genética , Filogenia , Filogeografía , ARN de Hongos/genética , Suelo/químicaRESUMEN
A better understanding of biogeography of Glomeromycota is essential for the conservation of arbuscular mycorrhizal (AM) fungal species and the ecosystem services that they provide worldwide. We examined the spatial dynamics of AM fungi along two slopes (4149 m a.s.l. to the summit at 5033 m a.s.l.) of Mount Mila on the Tibetan Plateau. Our hypothesis was that AM fungal communities at higher elevation would show distinct assemblages with lower diversity in conditions of increasing environmental harshness. A total of 52 operational taxonomic units (OTUs) spanning all four orders were detected and some OTUs were habitat specific. Nearly 30% of the OTUs were new phylotypes, including two family-like clades. Distinct communities of AM fungi were found at the higher elevation, demonstrating potential niche differentiation along the elevation gradient. Elevation patterns of taxon richness/diversity differed between the two transects, decreasing with increasing elevation on the eastern slope and being unimodal (or lacking a pattern) on the western slope. Taken together, our findings provide evidence of a significant spatial structure of AM fungi across the elevation gradient, with the distribution patterns of these fungi regulated simultaneously by the plant communities, soil properties and climatic conditions in this plateau montane ecosystem.
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Glomeromycota/clasificación , Pradera , Micorrizas/clasificación , Microbiología del Suelo , Estrés Fisiológico , ADN de Hongos/genética , TibetRESUMEN
Data generated from next generation sequencing (NGS) will soon comprise the majority of information about arbuscular mycorrhizal fungal (AMF) communities. Although these approaches give deeper insight, analysing NGS data involves decisions that can significantly affect results and conclusions. This is particularly true for AMF community studies, because much remains to be known about their basic biology and genetics. During a workshop in 2013, representatives from seven research groups using NGS for AMF community ecology gathered to discuss common challenges and directions for future research. Our goal was to improve the quality and accessibility of NGS data for the AMF research community. Discussions spanned sampling design, sample preservation, sequencing, bioinformatics and data archiving. With concrete examples we demonstrated how different approaches can significantly alter analysis outcomes. Failure to consider the consequences of these decisions may compound bias introduced at each step along the workflow. The products of these discussions have been summarized in this paper in order to serve as a guide for any researcher undertaking NGS sequencing of AMF communities.