Dataset Information

The Non-Legume Parasponia andersonii Mediates the Fitness of Nitrogen-Fixing Rhizobial Symbionts Under High Nitrogen Conditions.

ABSTRACT: Organisms rely on symbiotic associations for metabolism, protection, and energy. However, these intimate partnerships can be vulnerable to exploitation. What prevents microbial mutualists from parasitizing their hosts? In legumes, there is evidence that hosts have evolved sophisticated mechanisms to manage their symbiotic rhizobia, but the generality and evolutionary origins of these control mechanisms are under debate. Here, we focused on the symbiosis between Parasponia hosts and N2-fixing rhizobium bacteria. Parasponia is the only non-legume lineage to have evolved a rhizobial symbiosis and thus provides an evolutionary replicate to test how rhizobial exploitation is controlled. A key question is whether Parasponia hosts can prevent colonization of rhizobia under high nitrogen conditions, when the contribution of the symbiont becomes nonessential. We grew Parasponia andersonii inoculated with Bradyrhizobium elkanii under four ammonium nitrate concentrations in a controlled growth chamber. We measured shoot and root dry weight, nodule number, nodule fresh weight, nodule volume. To quantify viable rhizobial populations in planta, we crushed nodules and determined colony forming units (CFU), as a rhizobia fitness proxy. We show that, like legumes and actinorhizal plants, P. andersonii is able to control nodule symbiosis in response to exogenous nitrogen. While the relative host growth benefits of inoculation decreased with nitrogen fertilization, our highest ammonium nitrate concentration (3.75 mM) was sufficient to prevent nodule formation on inoculated roots. Rhizobial populations were highest in nitrogen free medium. While we do not yet know the mechanism, our results suggest that control mechanisms over rhizobia are not exclusive to the legume clade.

SUBMITTER: Dupin SE

PROVIDER: S-EPMC7019102 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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The Non-Legume Parasponia andersonii Mediates the Fitness of Nitrogen-Fixing Rhizobial Symbionts Under High Nitrogen Conditions.

Dupin Simon E SE Geurts René R Kiers E Toby ET

Frontiers in plant science 20200207

Organisms rely on symbiotic associations for metabolism, protection, and energy. However, these intimate partnerships can be vulnerable to exploitation. What prevents microbial mutualists from parasitizing their hosts? In legumes, there is evidence that hosts have evolved sophisticated mechanisms to manage their symbiotic rhizobia, but the generality and evolutionary origins of these control mechanisms are under debate. Here, we focused on the symbiosis between Parasponia hosts and N ...[more]

PMID: 32117343

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Project description:The environmental context of the nitrogen-fixing mutualism between leguminous plants and rhizobial bacteria varies over space and time. Variation in resource availability, population density, and composition likely affect the ecology and evolution of rhizobia and their symbiotic interactions with hosts. We examined how host genotype, nitrogen addition, rhizobial density, and community complexity affected selection on 68 rhizobial strains in the Sinorhizobium meliloti-Medicago truncatula mutualism. As expected, host genotype had a substantial effect on the size, number, and strain composition of root nodules (the symbiotic organ). The understudied environmental variable of rhizobial density had a stronger effect on nodule strain frequency than the addition of low nitrogen levels. Higher inoculum density resulted in a nodule community that was less diverse and more beneficial but only in the context of the more selective host genotype. Higher density resulted in more diverse and less beneficial nodule communities with the less selective host. Density effects on strain composition deserve additional scrutiny as they can create feedback between ecological and evolutionary processes. Finally, we found that relative strain rankings were stable across increasing community complexity (2, 3, 8, or 68 strains). This unexpected result suggests that higher-order interactions between strains are rare in the context of nodule formation and development. Our work highlights the importance of examining mechanisms of density-dependent strain fitness and developing theoretical predictions that incorporate density dependence. Furthermore, our results have translational relevance for overcoming establishment barriers in bioinoculants and motivating breeding programs that maintain beneficial plant-microbe interactions across diverse agroecological contexts. IMPORTANCE Legume crops establish beneficial associations with rhizobial bacteria that perform biological nitrogen fixation, providing nitrogen to plants without the economic and greenhouse gas emission costs of chemical nitrogen inputs. Here, we examine the influence of three environmental factors that vary in agricultural fields on strain relative fitness in nodules. In addition to manipulating nitrogen, we also use two biotic variables that have rarely been examined: the rhizobial community's density and complexity. Taken together, our results suggest that (i) breeding legume varieties that select beneficial strains despite environmental variation is possible, (ii) changes in rhizobial population densities that occur routinely in agricultural fields could drive evolutionary changes in rhizobial populations, and (iii) the lack of higher-order interactions between strains will allow the high-throughput assessments of rhizobia winners and losers during plant interactions.

Project description:BackgroundRhizobia are soil bacteria that establish symbiotic relationships with legumes and fix nitrogen in root nodules. We recently reported that several nitrogen-fixing rhizobial strains, belonging to Rhizobium phaseoli, R. trifolii, R. grahamii and Sinorhizobium americanum, were able to colonize Phaseolus vulgaris (common bean) seeds. To gain further insight into the traits that support this ability, we analyzed the genomic sequences and proteomes of R. phaseoli (CCGM1) and S. americanum (CCGM7) strains from seeds and compared them with those of the closely related strains CIAT652 and CFNEI73, respectively, isolated only from nodules.ResultsIn a fine structural study of the S. americanum genomes, the chromosomes, megaplasmids and symbiotic plasmids were highly conserved and syntenic, with the exception of the smaller plasmid, which appeared unrelated. The symbiotic tract of CCGM7 appeared more disperse, possibly due to the action of transposases. The chromosomes of seed strains had less transposases and strain-specific genes. The seed strains CCGM1 and CCGM7 shared about half of their genomes with their closest strains (3353 and 3472 orthologs respectively), but a large fraction of the rest also had homology with other rhizobia. They contained 315 and 204 strain-specific genes, respectively, particularly abundant in the functions of transcription, motility, energy generation and cofactor biosynthesis. The proteomes of seed and nodule strains were obtained and showed a particular profile for each of the strains. About 82 % of the proteins in the comparisons appeared similar. Forty of the most abundant proteins in each strain were identified; these proteins in seed strains were involved in stress responses and coenzyme and cofactor biosynthesis and in the nodule strains mainly in central processes. Only 3 % of the abundant proteins had hypothetical functions.ConclusionsFunctions that were enriched in the genomes and proteomes of seed strains possibly participate in the successful occupancy of the new niche. The genome of the strains had features possibly related to their presence in the seeds. This study helps to understand traits of rhizobia involved in seed adaptation.

Project description:Numerous reforestation projects have been conducted to improve soil fertility in degraded forests, often causing alterations to the soil microbial communities. However, it remains unclear whether microbial functional groups are affected and how these groups correlate with an increase in the nutrient contents during reforestation. We investigated the abundance and composition of free-living nitrogen-fixing microorganisms (diazotrophs) by quantifying and sequencing the marker gene nifH in bulk soils from five reforestation approaches, including legumes and non-legumes, in subtropical China. The relationships between diazotrophic community attributes and soil nitrogen (N) content [NO3 -, NH4 +, and microbial biomass N (MBN)] were examined under various approaches. Abundance of diazotrophs was highest in the native tree plantation (Schima spp. and Michelia macclurei) and Acacia mangium monoculture (AM), and lowest in the Pinus massoniana monoculture. The diazotrophic abundance correlated positively with soil organic matter and water content while there was a negative correlation to pH. The composition of diazotrophic community differed significantly among the five reforestation approaches examined and was closely correlated with variations in soil pH, NH4 + and water content. Diazotrophic community composition was closely related to soil NH4 + content, whereas abundance was not. The AM contained higher NH4 +, NO3 - and MBN contents than the other reforestation approaches, which may be associated with the indicator species of diazotrophs (Actinobacteria, Proteobacteria, and Firmicutes). However, there were more indicator species of Proteobacteria in the mixed Acacia plantation (Acacia mangium and Acacia crassicarpa) than in AM, which might have contributed to the remarkedly lower N content compared to AM. Overall, the soil N content under reforestation appeared to be more related to the composition of diazotroph community than to the abundance of diazotrophs.

Dataset Information

The Non-Legume Parasponia andersonii Mediates the Fitness of Nitrogen-Fixing Rhizobial Symbionts Under High Nitrogen Conditions.

Publications

The Non-Legume <i>Parasponia andersonii</i> Mediates the Fitness of Nitrogen-Fixing Rhizobial Symbionts Under High Nitrogen Conditions.

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