Priority effects alter interaction outcomes in a legume-rhizobium mutualism.
Ontology highlight
ABSTRACT:
SUBMITTER: Boyle JA
PROVIDER: S-EPMC7944086 | biostudies-literature |
REPOSITORIES: biostudies-literature
Similar Datasets
Project description:Legumes are high in protein and form a valuable part of human diets due to their interaction with symbiotic nitrogen-fixing bacteria known as rhizobia. Plants house rhizobia in specialized root nodules and provide the rhizobia with carbon in return for nitrogen. However, plants usually house multiple rhizobial strains that vary in their fixation ability, so the plant faces an investment dilemma. Plants are known to sanction strains that do not fix nitrogen, but nonfixers are rare in field settings, while intermediate fixers are common. Here, we modeled how plants should respond to an intermediate fixer that was otherwise isogenic and tested model predictions using pea plants. Intermediate fixers were only tolerated when a better strain was not available. In agreement with model predictions, nodules containing the intermediate-fixing strain were large and healthy when the only alternative was a nonfixer, but nodules of the intermediate-fixing strain were small and white when the plant was coinoculated with a more effective strain. The reduction in nodule size was preceded by a lower carbon supply to the nodule even before differences in nodule size could be observed. Sanctioned nodules had reduced rates of nitrogen fixation, and in later developmental stages, sanctioned nodules contained fewer viable bacteria than nonsanctioned nodules. This indicates that legumes can make conditional decisions, most likely by comparing a local nodule-dependent cue of nitrogen output with a global cue, giving them remarkable control over their symbiotic partners.
| S-EPMC8126861 | biostudies-literature
Project description:UnlabelledRhizobia are best known for nodulating legume roots and fixing atmospheric nitrogen for the host in exchange for photosynthates. However, the majority of the diverse strains of rhizobia do not form nodules on legumes, often because they lack key loci that are needed to induce nodulation. Nonnodulating rhizobia are robust heterotrophs that can persist in bulk soil, thrive in the rhizosphere, or colonize roots as endophytes, but their role in the legume-rhizobium mutualism remains unclear. Here, we investigated the effects of nonnodulating strains on the native Acmispon-Bradyrhizobium mutualism. To examine the effects on both host performance and symbiont fitness, we performed clonal inoculations of diverse nonnodulating Bradyrhizobium strains on Acmispon strigosus hosts and also coinoculated hosts with mixtures of sympatric nodulating and nonnodulating strains. In isolation, nonnodulating Bradyrhizobium strains did not affect plant performance. In most cases, coinoculation of nodulating and nonnodulating strains reduced host performance compared to that of hosts inoculated with only a symbiotic strain. However, coinoculation increased host performance only under one extreme experimental treatment. Nearly all estimates of nodulating strain fitness were reduced in the presence of nonnodulating strains. We discovered that nonnodulating strains were consistently capable of coinfecting legume nodules in the presence of nodulating strains but that the fitness effects of coinfection for hosts and symbionts were negligible. Our data suggest that nonnodulating strains most often attenuate the Acmispon-Bradyrhizobium mutualism and that this occurs via competitive interactions at the root-soil interface as opposed to in plantaImportanceRhizobia are soil bacteria best known for their capacity to form root nodules on legume plants and enhance plant growth through nitrogen fixation. Yet, most rhizobia in soil do not have this capacity, and their effects on this symbiosis are poorly understood. We investigated the effects of diverse nonnodulating rhizobia on a native legume-rhizobium symbiosis. Nonnodulating strains did not affect plant growth in isolation. However, compared to inoculations with symbiotic rhizobia, coinoculations of symbiotic and nonnodulating strains often reduced plant and symbiont fitness. Coinoculation increased host performance only under one extreme treatment. Nonnodulating strains also invaded nodule interiors in the presence of nodulating strains, but this did not affect the fitness of either partner. Our data suggest that nonnodulating strains may be important competitors at the root-soil interface and that their capacity to attenuate this symbiosis should be considered in efforts to use rhizobia as biofertilizers.
| S-EPMC4988196 | biostudies-literature
Project description:Species interactions play a critical role in biological invasions. For example, exotic plant and microbe mutualists can facilitate each other's spread as they co-invade novel ranges. Environmental context may influence the effect of mutualisms on invasions in heterogeneous environments, however these effects are poorly understood. We examined the mutualism between the legume, Medicago polymorpha, and the rhizobium, Ensifer medicae, which have both invaded California grasslands. Many of these invaded grasslands are composed of a patchwork of harsh serpentine and relatively benign non-serpentine soils. We grew legume genotypes collected from serpentine or non-serpentine soil in both types of soil in combination with rhizobium genotypes from serpentine or non-serpentine soils and in the absence of rhizobia. Legumes invested more strongly in the mutualism in the home soil type and trends in fitness suggested that this ecotypic divergence was adaptive. Serpentine legumes had greater allocation to symbiotic root nodules in serpentine soil than did non-serpentine legumes and non-serpentine legumes had greater allocation to nodules in non-serpentine soil than did serpentine legumes. Therefore, this invasive legume has undergone the rapid evolution of divergence for soil-specific investment in the mutualism. Contrary to theoretical expectations, the mutualism was less beneficial for legumes grown on the stressful serpentine soil than on the non-serpentine soil, possibly due to the inhibitory effects of serpentine on the benefits derived from the interaction. The soil-specific ability to allocate to a robust microbial mutualism may be a critical, and previously overlooked, adaptation for plants adapting to heterogeneous environments during invasion.
| S-EPMC3235091 | biostudies-literature
Project description:Background:Polyploidy is known to significantly alter plant genomes, phenotypes and interactions with the abiotic environment, yet the impacts of polyploidy on plant-biotic interactions are less well known. A particularly important plant-biotic interaction is the legume-rhizobia mutualism, in which rhizobia fix atmospheric nitrogen in exchange for carbon provided by legume hosts. This mutualism regulates nutrient cycles in natural ecosystems and provides nitrogen to agricultural environments. Despite the ecological, evolutionary and agricultural importance of plant polyploidy and the legume-rhizobia mutualism, it is not yet fully understood whether plant polyploidy directly alters mutualism traits or the consequences on plant growth. Scope:The aim was to propose a conceptual framework to understand how polyploidy might directly enhance the quantity and quality of rhizobial symbionts hosted by legume plants, resulting in increased host access to fixed nitrogen (N). Mechanistic hypotheses have been devised to examine how polyploidy can directly alter traits that impact the quantity (e.g. nodule number, nodule size, terminal bacteroid differentiation) and quality of symbionts (e.g. nodule environment, partner choice, host sanctions). To evaluate these hypotheses, an exhaustive review of studies testing the effects of plant polyploidy on the mutualism was conducted. In doing so, overall trends were synthesized, highlighting the limited understanding of the mechanisms that underlie variation in results achieved thus far, revealing striking gaps in knowledge and uncovering areas ripe for future research. Conclusions:Plant polyploidy can immediately alter nodule size, N fixation rate and the identity of rhizobial symbionts hosted by polyploid legumes, but many of the mechanistic hypotheses proposed here, such as bacteroid number and enhancements of the nodule environment, remain unexplored. Although current evidence supports a role of plant polyploidy in enhancing key aspects of the legume-rhizobia mutualism, the underlying mechanisms and effects on host benefit from the mutualism remain unresolved.
| S-EPMC5808787 | biostudies-other
Project description:Establishing mutualistic interactions in novel environments is important for the successful establishment of some non-native plant species. These associations may, in turn, impact native species interaction networks as non-natives become dominant in their new environments. Using phylogenetic and ecological interaction network approaches we provide the first report of the structure of belowground legume-rhizobium interaction networks and how they change along a gradient of invasion (uninvaded, semi invaded and heavily invaded sites) by Australian Acacia species in South Africa's Cape Floristic Region. We found that native and invasive legumes interact with distinct rhizobial lineages, most likely due to phylogenetic uniqueness of native and invasive host plants. Moreover, legume-rhizobium interaction networks are not nested, but significantly modular with high levels of specialization possibly as a result of legume-rhizobium co-evolution. Although network topology remained constant across the invasion gradient, composition of bacterial communities associated with native legumes changed dramatically as acacias increasingly dominated the landscape. In stark contrast to aboveground interaction networks (e.g. pollination and seed dispersal) we show that invasive legumes do not infiltrate existing native legume-rhizobium networks but rather form novel modules. This absence of mutualist overlap between native and invasive legumes suggests the importance of co-invading rhizobium-acacia species complexes for Acacia invasion success, and argues against a ubiquitous role for the formation and evolutionary refinement of novel interactions.
| S-EPMC4940501 | biostudies-literature
Project description:Theory suggests that communities should be more open to the establishment of regional species following disturbance because disturbance may make more resources available to dispersers. However, after an initial period of high invasibility, growth of the resident community may lead to the monopolization of local resources and decreased probability of successful colonist establishment. During press disturbances (i.e., directional environmental change), it remains unclear what effect regional dispersal will have on local community structure if the establishment of later arriving species is affected by early arriving species (i.e., if priority effects are important). To determine the relationship between time-since-disturbance and invasibility, we conducted a fully factorial field mesocosm experiment that exposed tundra zooplankton communities to two emerging stressors - nutrient and salt addition, and manipulated the arrival timing of regional dispersers. Our results demonstrate that invasibility decreases with increasing time-since-disturbance as abundance (nutrient treatments) or species richness (salt treatments) increases in the resident community. Results suggest that the relative timing of dispersal and environmental change will modify the importance of priority effects in determining species composition after a press disturbance.
| S-EPMC3936386 | biostudies-literature
Project description:Bacterial mutualists generate major fitness benefits for eukaryotes, reshaping the host phenotype and its interactions with the environment. Yet, microbial mutualist populations are predicted to generate mutants that defect from providing costly services to hosts while maintaining the capacity to exploit host resources. Here, we examined the mutualist service of symbiotic nitrogen fixation in a metapopulation of root-nodulating Bradyrhizobium spp. that associate with the native legume Acmispon strigosus. We quantified mutualism traits of 85 Bradyrhizobium isolates gathered from a 700 km transect in California spanning 10 sampled A. strigosus populations. We clonally inoculated each Bradyrhizobium isolate onto A. strigosus hosts and quantified nodulation capacity and net effects of infection, including host growth and isotopic nitrogen concentration. Six Bradyrhizobium isolates from five populations were categorized as ineffective because they formed nodules but did not enhance host growth via nitrogen fixation. Six additional isolates from three populations failed to form root nodules. Phylogenetic reconstruction inferred two types of mutualism breakdown, including three to four independent losses of effectiveness and five losses of nodulation capacity on A. strigosus. The evolutionary and genomic drivers of these mutualism breakdown events remain poorly understood.
| S-EPMC7015337 | biostudies-literature
Project description:Polymicrobial biofilms are a hallmark of chronic wound infection. The forces governing assembly and maturation of these microbial ecosystems are largely unexplored but the consequences on host response and clinical outcome can be significant. In the context of wound healing, formation of a biofilm and a stable microbial community structure is associated with impaired tissue repair resulting in a non-healing chronic wound. These types of wounds can persist for years simmering below the threshold of classically defined clinical infection (which includes heat, pain, redness, and swelling) and cycling through phases of recurrent infection. In the most severe outcome, amputation of lower extremities may occur if spreading infection ensues. Here we take an ecological perspective to study priority effects and competitive exclusion on overall biofilm community structure in a three-membered community comprised of strains of Staphylococcus aureus, Citrobacter freundii, and Candida albicans derived from a chronic wound. We show that both priority effects and inter-bacterial competition for binding to C. albicans biofilms significantly shape community structure on both abiotic and biotic substrates, such as ex vivo human skin wounds. We further show attachment of C. freundii to C. albicans is mediated by mannose-binding lectins. Co-cultures of C. freundii and C. albicans trigger the yeast-to-hyphae transition, resulting in a significant increase in neutrophil death and inflammation compared to either species alone. Collectively, the results presented here facilitate our understanding of fungal-bacterial interactions and their effects on host-microbe interactions, pathogenesis, and ultimately, wound healing.
| S-EPMC8245565 | biostudies-literature
Project description:Understanding the origins and evolutionary trajectories of symbiotic partnerships remains a major challenge. Why are some symbioses lost over evolutionary time whereas others become crucial for survival? Here, we use a quantitative trait reconstruction method to characterize different evolutionary stages in the ancient symbiosis between legumes (Fabaceae) and nitrogen-fixing bacteria, asking how labile is symbiosis across different host clades. We find that more than half of the 1,195 extant nodulating legumes analyzed have a high likelihood (>95%) of being in a state of high symbiotic persistence, meaning that they show a continued capacity to form the symbiosis over evolutionary time, even though the partnership has remained facultative and is not obligate. To explore patterns associated with the likelihood of loss and retention of the N2-fixing symbiosis, we tested for correlations between symbiotic persistence and legume distribution, climate, soil and trait data. We found a strong latitudinal effect and demonstrated that low mean annual temperatures are associated with high symbiotic persistence in legumes. Although no significant correlations between soil variables and symbiotic persistence were found, nitrogen and phosphorus leaf contents were positively correlated with legumes in a state of high symbiotic persistence. This pattern suggests that highly demanding nutrient lifestyles are associated with more stable partnerships, potentially because they "lock" the hosts into symbiotic dependency. Quantitative reconstruction methods are emerging as a powerful comparative tool to study broad patterns of symbiont loss and retention across diverse partnerships.
| S-EPMC4547229 | biostudies-literature
Project description:Background and aims:Arsenic (As) is one of the most widespread environmental contaminants. The aim of our study was to test a novel bioremediation system based on the symbiosis between leguminous plant and genetically engineered rhizobia. Methods:The arsenite [As(III)] S-adenosylmethionine methyltransferase gene (CrarsM) from the alga Chlamydomonas reinhardtii was inserted into the chromosome of Rhizobium leguminosarum bv. trifolii strain R3. The As methylation ability of the recombinant Rhizobium was tested under free living conditions and in symbiosis with red clover plants. Arsenic speciation was determined using high-performance liquid chromatography-inductively coupled plasma mass spectrometry. Results:Under free-living conditions, CrarsM-recombinant R. leguminosarum gained the ability to methylate As(III) to methylated arsenicals, including methylarsenate [MAs(V)], dimethylarsenate [DMAs(V)] and trimethylarsine oxide [TMAs(V)O]. Red clover plants were inoculated with either control (non-recombinant) or CrarsM-recombinant R. leguminosarum and exposed to 5 or 10 ?M arsenite. No methylated As species were detected in red clover plants inoculated with control R. leguminosarum. In contrast, all three methylated species were detected in both the nodules and the shoots when the recombinant Rhizobium established symbiosis with red clover, accounting for 74.7-75.1% and 29.1-42.4% of the total As in the two plant tissues, respectively. The recombinant symbiont also volatilized small amounts of As. Conclusions:The present study demonstrates that engineered rhizobia expressing an algal arsM gene can methylate and volatilize As, providing a proof of concept for potential future use of legume-rhizobia symbionts for As bioremediation.
| S-EPMC5889086 | biostudies-literature