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Resource acquisition and allocation traits in symbiotic rhizobia with implications for life-history outside of legume hosts.

ABSTRACT: Resources that microbial symbionts obtain from hosts may enhance fitness during free-living stages when resources are comparatively scarce. For rhizobia in legume root nodules, diverting resources from nitrogen fixation to polyhydroxybutyrate (PHB) has been discussed as a source of host-symbiont conflict. Yet, little is known about natural variation in PHB storage and its implications for rhizobial evolution. We therefore measured phenotypic variation in natural rhizobia populations and investigated how PHB might contribute to fitness in the free-living stage. We found that natural populations of rhizobia from Glycine max and Chamaecrista fasciculata had substantial, heritable variation in PHB acquisition during symbiosis. A model simulating temperature-dependent metabolic activity showed that the observed range of stored PHB per cell could support survival for a few days, for active cells, or over a century for sufficiently dormant cells. Experiments with field-isolated Bradyrhizobium in starvation culture suggest PHB is partitioned asymmetrically in dividing cells, consistent with individual-level bet-hedging previously demonstrated in E. meliloti. High-PHB isolates used more PHB over the first month, yet still retained more PHB for potential long-term survival in a dormant state. These results suggest that stored resources like PHB may support both short-term and long-term functions that contribute to fitness in the free-living stage.

SUBMITTER: Muller KE

PROVIDER: S-EPMC6304121 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Resource acquisition and allocation traits in symbiotic rhizobia with implications for life-history outside of legume hosts.

Muller Katherine E KE Denison R Ford RF

Royal Society open science 20181212 12

Resources that microbial symbionts obtain from hosts may enhance fitness during free-living stages when resources are comparatively scarce. For rhizobia in legume root nodules, diverting resources from nitrogen fixation to polyhydroxybutyrate (PHB) has been discussed as a source of host-symbiont conflict. Yet, little is known about natural variation in PHB storage and its implications for rhizobial evolution. We therefore measured phenotypic variation in natural rhizobia populations and investig ...[more]

PMID: 30662731

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Project description:The stabilization of host-symbiont mutualism against the emergence of parasitic individuals is pivotal to the evolution of cooperation. One of the most famous symbioses occurs between legumes and their colonizing rhizobia, in which rhizobia extract nutrients (or benefits) from legume plants while supplying them with nitrogen resources produced by nitrogen fixation (or costs). Natural environments, however, are widely populated by ineffective rhizobia that extract benefits without paying costs and thus proliferate more efficiently than nitrogen-fixing cooperators. How and why this mutualism becomes stabilized and evolutionarily persists has been extensively discussed. To better understand the evolutionary dynamics of this symbiosis system, we construct a simple model based on the continuous snowdrift game with multiple interacting players. We investigate the model using adaptive dynamics and numerical simulations. We find that symbiotic evolution depends on the cost-benefit balance, and that cheaters widely emerge when the cost and benefit are similar in strength. In this scenario, the persistence of the symbiotic system is compatible with the presence of cheaters. This result suggests that the symbiotic relationship is robust to the emergence of cheaters, and may explain the prevalence of cheating rhizobia in nature. In addition, various stabilizing mechanisms, such as partner fidelity feedback, partner choice, and host sanction, can reinforce the symbiotic relationship by affecting the fitness of symbionts in various ways. This result suggests that the symbiotic relationship is cooperatively stabilized by various mechanisms. In addition, mixed nodule populations are thought to encourage cheater emergence, but our model predicts that, in certain situations, cheaters can disappear from such populations. These findings provide a theoretical basis of the evolutionary dynamics of legume-rhizobia symbioses, which is extendable to other single-host, multiple-colonizer systems.

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.

Dataset Information

Resource acquisition and allocation traits in symbiotic rhizobia with implications for life-history outside of legume hosts.

Publications

Resource acquisition and allocation traits in symbiotic rhizobia with implications for life-history outside of legume hosts.

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