Trends in Legume-Rhizobia Symbiosis in Remediation of Mercury-Contaminated Agricultural Soils

Raghupathy, Shwetha; Arunachalam, Sathiavelu

doi:10.1080/00103624.2023.2285516

Cited by 5 publications

(4 citation statements)

References 77 publications

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“…While the majority of molecular research in legume host-plants and symbiotic rhizobia has focused on nitrogen xation mechanisms, which provide obvious bene ts to both partners through nitrogen and carbon exchange, more recognition of overlapping stress responses in rhizobia and host plant signaling has been realized to be essential for establishing symbiosis and improved resilience in legume-rhizobia systems [18]. Symbiotic interactions between legume host plants and nitrogen-xing rhizobia have profound impacts on soil quality and plant health, and soil microbes in symbiosis with legumes have potential for bioremediation of toxic soils [19,20], particularly if one or both symbiotic partners becomes adapted to a novel stress condition such as heavy metals in the environment.…”

Section: Introductionmentioning

confidence: 99%

“…Transcriptomics studies have identi ed candidate genes that respond to the predominant heavy metals in mining sites by enhanced ion transport mechanisms (e.g., ATPase e ux activity using cadA), but genome wide studies in rhizobia have been mostly focused on adaptations to Cd, Cu, Pb and Zn [19,[28][29][30]. Studies of adaptive evolution and tolerance to Hg in rhizobia have been limited to a small number of genes [20], rather than whole genome evolution or genome-wide responses in the transcriptome.…”

Section: Introductionmentioning

confidence: 99%

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Adaptation to mercury stress by nitrogen-fixing bacteria is driven by horizontal gene transfer and enhanced gene expression of the Mer operon

Paape,

Bhat,

Sharma

et al. 2024

Preprint

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Background: Mercury (Hg) is highly toxic and has the potential to cause severe health problems for humans and foraging animals when transported into edible plant parts. Soil rhizobia that form symbiosis with legumes may possess mechanisms to prevent heavy metal translocation from roots to shoots in plants by exporting metals from nodules or compartmentalizing metal ions inside nodules. We sequenced the genomes of Sinorhizobium medicae and Rhizobium leguminosarum with high variation in Hg-tolerance to identify differences between low and high Hg-tolerant strains. While independent mercury reductase A (merA) genes are prevalent in a-proteobacteria, Mer operons are rare and often vary in their gene organization. Results: Our analyses identified multiple structurally conserved merA homologs in the genomes of S. medicae, but only the strains that possessed a Mer operon exhibited hypertolerance to Hg. RNAseq analysis revealed nearly all genes in the Mer operon were significantly up-regulated in response to Hg stress in free-living conditions and in nodules. In both free-living and nodule environments, we found the Hg-tolerant strains with a Mer operon exhibited the fewest number of differentially expressed genes (DEGs) in the genome, indicating a rapid and efficient detoxification of Hg2+ from the cells that reduced general stress responses to the Hg-treatment. Expression changes in S. medicae while inside of nodules showed that both rhizobia strain and host-plant tolerance affected the number of DEGs. Aside from Mer operon genes, nif genes which are involved in nitrogenase activity in S. medicae showed significant up-regulation in the most Hg-tolerant strain while inside the most Hg-accumulating host-plant, indicating a genotype-by-genotype interaction that influences nitrogen-fixation under stress conditions. Transfer of the Mer operon to low-tolerant strains resulted in an immediate increase in Hg tolerance, indicating that the operon is solely necessary to confer hypertolerance to Hg, despite paralogous merA genes present elsewhere in the genome. Conclusions: Mercury reductase operons (Mer) have not been previously reported in nitrogen-fixing rhizobia. This study demonstrates a pivotal role of the Mer operon in effective mercury detoxification and hypertolerance in nitrogen-fixing rhizobia. This finding has major implications not only for soil bioremediation, but also host plants growing in mercury contaminated soils.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Adaptation to mercury stress by nitrogen-fixing bacteria is driven by horizontal gene transfer and enhanced gene expression of the Mer operon

Paape,

Bhat,

Sharma

et al. 2024

Preprint

View full text Add to dashboard Cite

show abstract

“…While the majority of molecular research in legume host-plants and symbiotic rhizobia has focused on nitrogen fixation mechanisms, which provide obvious benefits to both partners through nitrogen and carbon exchange, more recognition of overlapping stress responses in rhizobia and host plant signaling has been realized to be essential for establishing symbiosis and improved resilience in legume-rhizobia systems (Hawkins and Oresnik, 2022). Symbiotic interactions between legume host plants and nitrogen-fixing rhizobia have profound impacts on soil quality and plant health, and soil microbes in symbiosis with legumes have potential for bioremediation of toxic soils (Fagorzi et al, 2018; Raghupathy and Arunachalam, 2023), particularly if one or both symbiotic partners becomes adapted to a novel stress condition such as heavy metals in the environment.…”

Section: Introductionmentioning

confidence: 99%

“…Transcriptomics studies have identified candidate genes that respond to the predominant heavy metals in mining sites by enhanced ion transport mechanisms (e.g., ATPase efflux activity using cadA), but genome wide studies in rhizobia have been mostly focused on adaptations to Cd, Cu, Pb and Zn (Rossbach et al, 2008; Maynaud et al, 2013; Lu et al, 2017; Fagorzi et al, 2018). Studies of adaptive evolution and tolerance to Hg in rhizobia have been limited to a small number of genes (Raghupathy and Arunachalam, 2023), rather than whole genome evolution or genome-wide responses in the transcriptome.…”

Section: Introductionmentioning

confidence: 99%

Local adaptation to mercury contamination by nitrogen-fixing rhizobia is driven by horizontal gene transfer, copy number, and enhanced gene expression

Bhat,

Sharma,

Lucas

et al. 2023

Preprint

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Mercury (Hg) is highly toxic and has the potential to cause severe health problems for foraging animals and humans when transported into edible plant parts. Soil rhizobia that form symbiosis with legumes may possess mechanisms to prevent heavy metal translocation from roots to shoots in plants by exporting metals from nodules or compartmentalizing metal ions inside nodules. Using long-read sequencing, we assembled the genomes ofSinorhizobium medicaeandRhizobium leguminosarumfrom the Almadén mercury mine in Spain with high variation in Hg-tolerance to identify structural and transcriptomic differences between low and high Hg-tolerant strains. While independent mercury reductase A (merA) genes are prevalent in α-proteobacteria, Mer operons are rare and often vary in their gene organization. Our analyses identified multiple structurally conserved merA homologs in the genomes ofS. medicae, including a dihydrolipoamide 2-oxoglutarate dehydrogenase (D2OD), but only the strains that possessed a Mer operon exhibited hypertolerance to Hg. Using RNAseq reads mapped to the unique genome assemblies, we found the Hg-tolerant strains which possessed a Mer operon, that nearly all genes within the operon were significantly up-regulated in response to Hg stress in free-living conditions and in nodules. In both free-living and nodule environments, we found the Hg-tolerant strains with a Mer operon exhibited the fewest number of DEGs in the genome, indicating a rapid and efficient detoxification of Hg2+from the cells that reduced general stress responses to the Hg-treatment. Expression changes inS. medicaewhile inside of nodules showed that both rhizobia strain and host-plant tolerance affected the number of DEGs. Aside from Mer operon genes,nifgenes which are involved in nitrogenase activity inS. medicaeshowed significant up-regulation in the most Hg-tolerant strain while inside the most Hg-accumulating host-plant, indicating a genotype-by-genotype interaction that influences nitrogen-fixation under stress conditions. Transfer of the Mer operon to non-tolerant strains resulted in an immediate increase in Hg tolerance, indicating that the operon is solely necessary to confer hypertolerance to Hg, despite paralogous merA genes present elsewhere in the genome. This study demonstrated that the Mer operon can be exchanged via horizontal gene transfer into non-tolerant rhizobia strains naturally and experimentally.

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Sulfur availability and nodulation modify the response of Robinia pseudoacacia L. to lead (Pb) exposure

Xue,

Liu,

Xia

et al. 2024

Journal of Hazardous Materials

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Trends in Legume-Rhizobia Symbiosis in Remediation of Mercury-Contaminated Agricultural Soils

Cited by 5 publications

References 77 publications

Adaptation to mercury stress by nitrogen-fixing bacteria is driven by horizontal gene transfer and enhanced gene expression of the Mer operon

Adaptation to mercury stress by nitrogen-fixing bacteria is driven by horizontal gene transfer and enhanced gene expression of the Mer operon

Local adaptation to mercury contamination by nitrogen-fixing rhizobia is driven by horizontal gene transfer, copy number, and enhanced gene expression

Sulfur availability and nodulation modify the response of Robinia pseudoacacia L. to lead (Pb) exposure

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