Nonnodulating Bradyrhizobium spp. Modulate the Benefits of Legume-Rhizobium Mutualism

Abstract

Rhizobia 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 planta. IMPORTANCERhizobia 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. Rhizobia are heterotrophic soil bacteria with diverse lifestyles. Some rhizobial lineages have acquired the capacity to form nodules on legume roots and fix atmospheric nitrogen for these hosts (1). Nodulating rhizobia are attracted to flavonoids released by legumes. In response, t...

Plant microbiome analysis after Metarhizium amendment reveals increases in abundance of plant growth-promoting organisms and maintenance of disease-suppressive soil

“…Of note, it was found that Bradyrhizobium was significantly increased in roots after Metarhizium amendment (Fig 5). Bradyrhizobium are classically viewed as important PGPB that are capable of nodulation and nitrogen fixation for leguminous plants, however, the dominant ecotype in natural populations do not form these typical symbioses [78,79] and indeed no nodules were observed in this study (data not shown).…”

“…One hypothesis for the ecological importance of non-nodulating Bradyrhizobium species is the ability to increase plant host fitness by suppressing overproduction of nodules by prolific nodulating strains that would otherwise be energetically costly to the plant [79]. Co-inoculation of nodulating and non-nodulating strains of Bradyrhizobium isolated from Acmispon strigosus revealed that non-nodulating strains competitively colonized A. strigosus and depending on strain combination, could reduce the fitness of nodulating symbionts [79]. The plant growth promoting ability of Bradyrhizobium has also been shown for wild rice, Oryza breviligulata [80], and indicates that their ecological role is greater than their classical taxonomy indicates.…”

Legumes versus rhizobia: a model for ongoing conflict in symbiosis

“…Other genotypes of rhizobia dominate host nodules and rhizospheres through mechanisms correlated with antibiotic resistance and catabolic flexibility, which can promote persistence in the soil (Hollowell et al, , 2016a. Finally, some rhizobia evade host control over nodulation specificity by hitchhiking into the nodule alongside NF-secreting strains without themselves having any of the genes to encode NFs (Gano-Cohen et al, 2016). Soybeans have a unique mechanism to restrict nodulation by harmful rhizobia.…”

Interspecific conflict and the evolution of ineffective rhizobia

“…Isolates 140 and 161 were originally cultured from nodules, but might have coinfected the original host with a nodulating strain, as has been reported (Gano‐Cohen et al . ). Inoculated plants that did not form nodules were removed from remaining analyses, which focus on the 26 nodule‐forming isolates.…”