Trait-based assembly of arbuscular mycorrhizal fungal communities determines soil carbon formation and retention.

Fungi are crucial for soil organic carbon (SOC) formation, especially for the more persistent mineral-associated organic C (MAOC) pool. Yet, evidence for this often overlooks arbuscular mycorrhizal fungi (AMF) communities and how their composition and traits impact SOC accumulation. We grew sudangrass with AMF communities representing different traits conserved at the family level: competitors, from the Gigasporaceae family; ruderals, from the Glomeraceae family; or both families combined. We labeled sudangrass with 13 C-CO2 to assess AMF contributions to SOC, impacts on SOC priming, and fungal biomass persistence in MAOC. Single-family AMF communities decreased total SOC by 13.8%, likely due to fungal priming. Despite net SOC losses, all AMF communities contributed fungal C to soil but only the Glomeraceae community initially contributed to MAOC. After a month of decomposition, both the Glomeraceae and mixed-family communities contributed to MAOC formation. Plant phosphorus uptake, but not hyphal chemistry, was positively related to AMF soil C and MAOC accumulation. Arbuscular mycorrhizal fungi contribution to MAOC is dependent on the specific traits of the AMF community and related to phosphorus uptake. These findings provide insight into how variations in AMF community composition and traits, and thus processes like environmental filtering of AMF, may impact SOC accumulation.

Arbuscular mycorrhizal fungal communities with contrasting life-history traits influence host nutrient acquisition.

Life-history traits differ substantially among arbuscular mycorrhizal (AM) fungal families, potentially affecting hyphal nutrient acquisition efficiency, host nutrition, and thereby plant health and ecosystem function. Despite these implications, AM fungal community life-history strategies and community trait diversity effects on host nutrient acquisition are poorly understood. To address this knowledge gap, we grew sudangrass with AM fungal communities representing contrasting life-history traits and diversity: either (1) five species in the AM family Gigasporaceae, representing competitor traits, (2) five Glomerales species, representing ruderal traits, or (3) a mixed-trait community combining all ten AM fungal species. After 12 weeks, we measured above and belowground plant biomass and aboveground nutrient uptake and concentration. Overall, AM fungal colonization increased host nutrition, biomass, and foliar δ5nitrogen enrichment compared to the uncolonized control. Between the single-trait communities, the Glomeraceae community generally outperformed the Gigasporaceae community in host nutrition and plant growth, increasing plant phosphorus (P) uptake 1.5 times more than the Gigasporaceae community. We saw weak evidence for a synergistic effect of the mixed community, which was only higher for plant P concentration (1.26 times higher) and root colonization (1.26 times higher) compared to the single-trait communities. However, this higher P concentration did not translate to more P uptake or the highest plant biomass for the mixed community. These findings demonstrate that the AM symbiosis is affected by community differences at high taxonomic levels and provide insight into how different AM fungal communities and their associated traits affect host nutrition for fast-growing plant species.

Application of plant-soil feedbacks in the selection of crop rotation sequences.

Plant-soil feedback (PSF) can be a major driver of plant performance in communities, and this concept can be used in selecting crop rotation sequences to maximize agricultural yields. Potential benefits of using PSF in this context include nutrient use optimization, pathogen reduction, and enhancement of mutualisms between crops and microbes. Yet the contributions of these combined mechanisms are poorly understood. Here we investigated the relative contributions of these mechanisms using five major crops commonly cultivated in rotation (alfalfa, canola, maize, soybean, and wheat) under controlled conditions. We trained soil by growing each of the five crops in a "training phase," and then reciprocally planted the five crops in the trained soils in a "feedback phase." To tease out soil biota from nutrient effects, we established three treatments: "control" (trained unsterilized soil used in the feedback phases), "biota" (sterilized soil in the feedback phase inoculated with soil biota from the control treatment after the training phase), and "nutrient" (sterilized soils in both phases). Plant-soil feedback for each crop was calculated by comparing the total biomass of each crop grown in soils trained by each of the four other crops (i.e., in rotation) against total biomass in self-trained soil (i.e., monocropping). We found that PSF values varied among crop combinations in all the treatments, but such variation was the greatest in the nutrient treatment. Overall, soil biota feedback tended to be lower, whereas nutrient feedback tended to be greater compared to the unsterilized control soil, suggesting that effects of antagonistic biota outweighed those of beneficial microbes in the biota treatment, and that plants optimized nutrient uptake when the soil microbiome was absent in the nutrient treatment. Furthermore, soils in the nutrient treatment trained by the legume crops (alfalfa and soybean) tended to provide the greatest positive feedback, emphasizing the important legacy of N2 fixers in crop rotation. Taken together, our data demonstrate how nutrients and soil biota can be integral to PSFs among crops, and that assessing PSFs under controlled conditions can serve as a basis to determine the most productive crop rotation sequences prior to field testing.

Codependency between plant and arbuscular mycorrhizal fungal communities: what is the evidence?

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.

Plant communities mediate the interactive effects of invasion and drought on soil microbial communities.

Soil microbiomes could play a major role in ecosystem responses to escalating anthropogenic global change. However, we currently have a poor understanding of how soil microbes will respond to interacting global change factors and if responses will be mediated by changes in plant community structure. We used a field experiment to assess changes in soil fungal and bacterial communities in response to plant invasion, experimental drought, and their combination. In addition, we evaluated the relative importance of direct versus indirect pathways of invasion and drought through changes in associated plant communities with structural equation models. We found that fungal communities were interactively structured by invasion and drought, where fungal richness was lowest with invasion under ambient conditions but highest with invasion under drought conditions. Bacterial richness was lower under drought but unaffected by invasion. Changes in the plant community, including lower plant richness and higher root biomass, moderated the direct effects of invasion on microbial richness. Fungal and bacterial functional groups, including pathogens, mutualists, and nitrogen metabolizers, were also influenced by plant community changes. In sum, plant communities mediated the effects of interacting global change drivers on soil microbial community structure, with significant potential consequences for community dynamics and ecosystem functions.

Accounting for local adaptation in ectomycorrhizas: a call to track geographical origin of plants, fungi, and soils in experiments.

Local adaptation, the differential success of genotypes in their native versus foreign environments, can influence ecological and evolutionary processes, yet its importance is difficult to estimate because it has not been widely studied, particularly in the context of interspecific interactions. Interactions between ectomycorrhizal (EM) fungi and their host plants could serve as model system for investigations of local adaptation because they are widespread and affect plant responses to both biotic and abiotic selection pressures. Furthermore, because EM fungi cycle nutrients and mediate energy flow into food webs, their local adaptation may be critical in sustaining ecological function. Despite their ecological importance and an extensive literature on their relationships with plants, the vast majority of experiments on EM symbioses fail to report critical information needed to assess local adaptation: the geographic origin of the plant, fungal inocula, and soil substrate used in the experiment. These omissions limit the utility of such studies and restrict our understanding of EM ecology and evolution. Here, we illustrate the potential importance of local adaptation in EM relationships and call for consistent reporting of the geographic origin of plant, soil, and fungi as an important step towards a better understanding of the ecology and evolution of EM symbioses.

Priorities for research in soil ecology.

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.

An empirical investigation of the possibility of adaptability of arbuscular mycorrhizal fungi to new hosts.

Little is known about the adaptive capacity of arbuscular mycorrhizal (AM) fungi to novel hosts. Here we assessed the possibility of two heterospecific AM fungal isolates to adaptively change, in terms of host biomass response, as a function of host plant identity, over the course of a growing season. First, we produced pure inocula of Rhizophagus clarus and Rhizophagus intraradices, each starting from a single spore. Second, we "trained" each isolate individually in a community with two plants, sudangrass (Sorgum bicolour subsp. drummondii) and leek (Aliium ampeloprasum var. porrum), using a dual-compartment system to allow the establishment of a common mycorrhizal network between the two hosts. Third, we conducted a greenhouse experiment to reciprocally test each "trained" clone, obtained from each compartment, either with the same (home), or the other host (away) under two contrasting phosphorus levels. Overall, results did not support adaptive responses of the AM fungi to their hosts (i.e., greater host biomass under "home" relative to "away" conditions), but the opposite (i.e., greater host biomass under "away" relative to "home" conditions) was more frequently observed. These changes in AM fungal symbiotic functioning open the possibility for relatively rapid genetic change of arbuscular mycorrhizal fungi in response to new hosts, which represents one step forward from in vitro experiments.

Evolutionary asymmetry in the arbuscular mycorrhizal symbiosis: conservatism in fungal morphology does not predict host plant growth.

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.

Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis.

BACKGROUND: Local adaptation, the differential success of genotypes in their native versus foreign environment, arises from various evolutionary processes, but the importance of concurrent abiotic and biotic factors as drivers of local adaptation has only recently been investigated. Local adaptation to biotic interactions may be particularly important for plants, as they associate with microbial symbionts that can significantly affect their fitness and may enable rapid evolution. The arbuscular mycorrhizal (AM) symbiosis is ideal for investigations of local adaptation because it is globally widespread among most plant taxa and can significantly affect plant growth and fitness. Using meta-analysis on 1170 studies (from 139 papers), we investigated the potential for local adaptation to shape plant growth responses to arbuscular mycorrhizal inoculation. RESULTS: The magnitude and direction for mean effect size of mycorrhizal inoculation on host biomass depended on the geographic origin of the soil and symbiotic partners. Sympatric combinations of plants, AM fungi, and soil yielded large increases in host biomass compared to when all three components were allopatric. The origin of either the fungi or the plant relative to the soil was important for explaining the effect of AM inoculation on plant biomass. If plant and soil were sympatric but allopatric to the fungus, the positive effect of AM inoculation was much greater than when all three components were allopatric, suggesting potential local adaptation of the plant to the soil; however, if fungus and soil were sympatric (but allopatric to the plant) the effect of AM inoculation was indistinct from that of any allopatric combinations, indicating maladaptation of the fungus to the soil. CONCLUSIONS: This study underscores the potential to detect local adaptation for mycorrhizal relationships across a broad swath of the literature. Geographic origin of plants relative to the origin of AM fungal communities and soil is important for describing the effect of mycorrhizal inoculation on plant biomass, suggesting that local adaptation represents a powerful factor for the establishment of novel combinations of fungi, plants, and soils. These results highlight the need for subsequent investigations of local adaptation in the mycorrhizal symbiosis and emphasize the importance of routinely considering the origin of plant, soil, and fungal components.

Composition of fungal soil communities varies with plant abundance and geographic origin.

Interactions of belowground fungal communities with exotic and native plant species may be important drivers of plant community structure in invaded grasslands. However, field surveys linking plant community structure with belowground fungal communities are missing. We investigated whether a selected number of abundant and relatively rare plants, either native or exotic, from an old-field site associate with different fungal communities. We also assessed whether these plants showed different symbiotic relationships with soil biota through their roots. We characterized the plant community and collected roots to investigate fungal communities using 454 pyrosequencing and assessed arbuscular mycorrhizal colonization and enemy-induced lesions. Differences in fungal communities were considered based on the assessment of α- and ß diversity depending on plant 'abundance' and 'origin'. Plant abundance and origin determined the fungal community. Fungal richness was higher for native abundant as opposed to relatively rare native plant species. However, this was not observed for exotics of contrasting abundance. Regardless of their origin, ß diversity was higher for rare than for abundant species. Abundant exotics in the community, which happen to be grasses, were the least mycorrhizal whereas rare natives were most susceptible to enemy attack. Our results suggest that compared with exotics, the relative abundance of remnant native plant species in our old-field site is still linked to the structure of belowground fungal communities. In contrast, exotic species may act as a disturbing agent contributing towards the homogenization of soil fungal communities, potentially changing feedback interactions.

High functional diversity within species of arbuscular mycorrhizal fungi is associated with differences in phosphate and nitrogen uptake and fungal phosphate metabolism.

Plant growth responses following colonization with different isolates of a single species of an arbuscular mycorrhizal (AM) fungus can range from highly beneficial to detrimental, but the reasons for this high within-species diversity are currently unknown. To examine whether differences in growth and nutritional benefits are related to the phosphate (P) metabolism of the fungal symbiont, the effect of 31 different isolates from 10 AM fungal morphospecies on the P and nitrogen (N) nutrition of Medicago sativa and the P allocation among different P pools was examined. Based on differences in the mycorrhizal growth response, high, medium, and low performance isolates were distinguished. Plant growth benefit was positively correlated to the mycorrhizal effect on P and N nutrition. High performance isolates increased plant biomass by more than 170 % and contributed substantially to both P and N nutrition, whereas the effect of medium performance isolates particularly on the N nutrition of the host was significantly lower. Roots colonized by high performance isolates were characterized by relatively low tissue concentrations of inorganic P and short-chain polyphosphates and a high ratio between long- to short-chain polyphosphates. The high performance isolates belonged to different morphospecies and genera, indicating that the ability to contribute to P and N nutrition is widespread within the Glomeromycota and that differences in symbiotic performance and P metabolism are not specific for individual fungal morphospecies.

Accounting for soil biotic effects on soil health and crop productivity in the design of crop rotations.

There is an urgent need for novel agronomic improvements capable of boosting crop yields while alleviating environmental impacts. One such approach is the use of optimized crop rotations. However, a set of measurements that can serve as guiding principles for the design of crop rotations is lacking. Crop rotations take advantage of niche complementarity, enabling the optimization of nutrient use and the reduction of pests and specialist pathogen loads. However, despite the recognized importance of plant-soil microbial interactions and feedbacks for crop yield and soil health, this is ignored in the selection and management of crops for rotation systems. We review the literature and propose criteria for the design of crop rotations focusing on the roles of soil biota and feedback on crop productivity and soil health. We consider that identifying specific key organisms or consortia capable of influencing plant productivity is more important as a predictor of soil health and crop productivity than assessing the overall soil microbial diversity per se. As such, we propose that setting up soil feedback studies and applying genetic sequencing tools towards the development of soil biotic community databases has a strong potential to enable the establishment of improved soil health indicators for optimized crop rotations.

Isolate identity determines plant tolerance to pathogen attack in assembled mycorrhizal communities.

Arbuscular mycorrhizal fungi (AMF) are widespread soil microorganisms that associate mutualistically with plant hosts. AMF receive photosynthates from the host in return for various benefits. One of such benefits is in the form of enhanced pathogen tolerance. However, this aspect of the symbiosis has been understudied compared to effects on plant growth and its ability to acquire nutrients. While it is known that increased AMF species richness positively correlates with plant productivity, the relationship between AMF diversity and host responses to pathogen attack remains obscure. The objective of this study was to test whether AMF isolates can differentially attenuate the deleterious effects of a root pathogen on plant growth, whether the richest assemblage of AMF isolates provides the most tolerance against the pathogen, and whether AMF-induced changes to root architecture serve as a mechanism for improved plant disease tolerance. In a growth chamber study, we exposed the plant oxeye daisy (Leucanthemum vulgare) to all combinations of three AMF isolates and to the plant root pathogen Rhizoctonia solani. We found that the pathogen caused an 81% reduction in shoot and a 70% reduction in root biomass. AMF significantly reduced the highly deleterious effect of the pathogen. Mycorrhizal plants infected with the pathogen produced 91% more dry shoot biomass and 72% more dry root biomass relative to plants solely infected with R. solani. AMF isolate identity was a better predictor of AMF-mediated host tolerance to the pathogen than AMF richness. However, the enhanced tolerance response did not result from AMF-mediated changes to root architecture. Our data indicate that AMF communities can play a major role in alleviating host pathogen attack but this depends primarily on the capacity of individual AMF isolates to provide this benefit.

Diversity effects on productivity are stronger within than between trophic groups in the arbuscular mycorrhizal symbiosis.

BACKGROUND: The diversity of plants and arbuscular mycorrhizal fungi (AMF) has been experimentally shown to alter plant and AMF productivity. However, little is known about how plant and AMF diversity interact to shape their respective productivity. METHODOLOGY/PRINCIPAL FINDINGS: We co-manipulated the diversity of both AMF and plant communities in two greenhouse studies to determine whether the productivity of each trophic group is mainly influenced by plant or AMF diversity, respectively, and whether there is any interaction between plant and fungal diversity. In both experiments we compared the productivity of three different plant species monocultures, or their respective 3-species mixtures. Similarly, in both studies these plant treatments were crossed with an AMF diversity gradient that ranged from zero (non-mycorrhizal controls) to a maximum of three and five taxonomically distinct AMF taxa, respectively. We found that within both trophic groups productivity was significantly influenced by taxon identity, and increased with taxon richness. These main effects of AMF and plant diversity on their respective productivities did not depend on each other, even though we detected significant individual taxon effects across trophic groups. CONCLUSIONS/SIGNIFICANCE: Our results indicate that similar ecological processes regulate diversity-productivity relationships within trophic groups. However, productivity-diversity relationships are not necessarily correlated across interacting trophic levels, leading to asymmetries and possible biotic feedbacks. Thus, biotic interactions within and across trophic groups should be considered in predictive models of community assembly.

Indigenous arbuscular mycorrhizal fungal assemblages protect grassland host plants from pathogens.

Plant roots can establish associations with neutral, beneficial and pathogenic groups of soil organisms. Although it has been recognized from the study of individual isolates that these associations are individually important for plant growth, little is known about interactions of whole assemblages of beneficial and pathogenic microorganisms associating with plants.We investigated the influence of an interaction between local arbuscular mycorrhizal (AM) fungal and pathogenic/saprobic microbial assemblages on the growth of two different plant species from semi-arid grasslands in NE Germany (Mallnow near Berlin). In a greenhouse experiment each plant species was grown for six months in either sterile soil or in sterile soil with one of three different treatments: 1) an AM fungal spore fraction isolated from field soil from Mallnow; 2) a soil pathogen/saprobe fraction consisting of a microbial community prepared with field soil from Mallnow and; 3) the combined AM fungal and pathogen/saprobe fractions. While both plant species grew significantly larger in the presence of AM fungi, they responded negatively to the pathogen/saprobe treatment. For both plant species, we found evidence of pathogen protection effects provided by the AM fungal assemblages. These results indicate that interactions between assemblages of beneficial and pathogenic microorganisms can influence the growth of host plants, but that the magnitude of these effects is plant species-specific.

Prevailing negative soil biota effect and no evidence for local adaptation in a widespread Eurasian grass.

BACKGROUND: Soil biota effects are increasingly accepted as an important driver of the abundance and distribution of plants. While biogeographical studies on alien invasive plant species have indicated coevolution with soil biota in their native distribution range, it is unknown whether adaptation to soil biota varies among populations within the native distribution range. The question of local adaptation between plants and their soil biota has important implications for conservation of biodiversity and may justify the use of seed material from local provenances in restoration campaigns. METHODOLOGY/PRINCIPAL FINDINGS: We studied soil biota effects in ten populations of the steppe grass Stipa capillata from two distinct regions, Europe and Asia. We tested for local adaptation at two different scales, both within (ca. 10-80 km) and between (ca. 3300 km) regions, using a reciprocal inoculation experiment in the greenhouse for nine months. Generally, negative soil biota effects were consistent. However, we did not find evidence for local adaptation: both within and between regions, growth of plants in their 'home soil' was not significantly larger relative to that in soil from other, more distant, populations. CONCLUSIONS/SIGNIFICANCE: Our study suggests that negative soil biota effects can prevail in different parts of a plant species' range. Absence of local adaptation points to the possibility of similar rhizosphere biota composition across populations and regions, sufficient gene flow to prevent coevolution, selection in favor of plasticity, or functional redundancy among different soil biota. From the point of view of plant--soil biota interactions, our findings indicate that the current practice of using seeds exclusively from local provenances in ecosystem restoration campaigns may not be justified.