Manganese transport is essential for N<sub>2</sub>‐fixation by <i>Rhizobium leguminosarum</i> in bacteroids from galegoid but not phaseoloid nodules

Hood, Graham A.; Ramachandran, Vinoy K.; East, Alison K.; Downie, J. Allan; Poole, Philip S.

doi:10.1111/1462-2920.13773

Cited by 16 publications

(13 citation statements)

References 66 publications

(91 reference statements)

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“…During early root hair infection, S. meliloti is exposed to the reactive oxygen species (ROS) released by the plant host as a defense response ( Soto et al, 2009 ). Manganese has been shown to be important to counteract ROS effects, whereas Mg 2+ transport is essential for microaerobic nitrogen-fixation in late symbiotic stages ( Davies and Walker, 2007 ; Hood et al, 2015 ; Hood et al, 2017 ). It is therefore tempting to speculate on a key role of divalent metal ions in the control of Sm RNase III activity in vivo .…”

Section: Discussionmentioning

confidence: 99%

Sinorhizobium meliloti RNase III: Catalytic Features and Impact on Symbiosis

et al. 2018

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Members of the ribonuclease (RNase) III family of enzymes are metal-dependent double-strand specific endoribonucleases. They are ubiquitously found and eukaryotic RNase III-like enzymes include Dicer and Drosha, involved in RNA processing and RNA interference. In this work, we have addressed the primary characterization of RNase III from the symbiotic nitrogen-fixing α-proteobacterium Sinorhizobium meliloti. The S. meliloti rnc gene does encode an RNase III-like protein (SmRNase III), with recognizable catalytic and double-stranded RNA (dsRNA)-binding domains that clusters in a branch with its α–proteobacterial counterparts. Purified SmRNase III dimerizes, is active at neutral to alkaline pH and behaves as a strict metal cofactor-dependent double-strand endoribonuclease, with catalytic features distinguishable from those of the prototypical member of the family, the Escherichia coli ortholog (EcRNase III). SmRNase III prefers Mn2+ rather than Mg2+ as metal cofactor, cleaves the generic structured R1.1 substrate at a site atypical for RNase III cleavage, and requires higher cofactor concentrations and longer dsRNA substrates than EcRNase III for optimal activity. Furthermore, the ultraconserved E125 amino acid was shown to play a major role in the metal-dependent catalysis of SmRNase III. SmRNase III degrades endogenous RNA substrates of diverse biogenesis with different efficiency, and is involved in the maturation of the 23S rRNA. SmRNase III loss-of-function neither compromises viability nor alters morphology of S. meliloti cells, but influences growth, nodulation kinetics, the onset of nitrogen fixation and the overall symbiotic efficiency of this bacterium on the roots of its legume host, alfalfa, which ultimately affects plant growth. Our results support an impact of SmRNase III on nodulation and symbiotic nitrogen fixation in plants.

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Section: Discussionmentioning

confidence: 99%

Sinorhizobium meliloti RNase III: Catalytic Features and Impact on Symbiosis

et al. 2018

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“…Higher DCu concentrations could support denitrification in the coastal sediment and anoxic waters, removing bioavailable nitrogen and creating conditions favorable to N 2 fixation. Manganese has been shown to be essential for some terrestrial N 2 -fixing bacteria [76,77], but the physiological requirement for manganese in marine diazotrophs is not well understood.…”

Section: Factors Controlling the Distribution Of N 2 Fixationmentioning

confidence: 99%

New insights into the distributions of nitrogen fixation and diazotrophs revealed by high-resolution sensing and sampling methods

et al. 2020

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Nitrogen availability limits marine productivity across large ocean regions. Diazotrophs can supply new nitrogen to the marine environment via nitrogen (N 2 ) fixation, relieving nitrogen limitation. The distributions of diazotrophs and N 2 fixation have been hypothesized to be generally controlled by temperature, phosphorus, and iron availability in the global ocean.However, even in the North Atlantic where most research on diazotrophs and N 2 fixation has taken place, environmental controls remain contentious. Here we measure diazotroph composition, abundance, and activity at high resolution using newly developed underway sampling and sensing techniques. We capture a diazotrophic community shift from Trichodesmium to UCYN-A between the oligotrophic, warm (25-29°C) Sargasso Sea and relatively nutrient-enriched, cold (13-24°C) subpolar and eastern American coastal waters. Meanwhile, N 2 fixation rates measured in this study are among the highest ever recorded globally and show significant increase with phosphorus availability across the transition from the Gulf Stream into subpolar and coastal waters despite colder temperatures and higher nitrate concentrations. Transcriptional patterns in both Trichodesmium and UCYN-A indicate phosphorus stress in the subtropical gyre. Over this iron-replete transect spanning the western North Atlantic, our results suggest that temperature is the major factor controlling the diazotrophic community structure while phosphorous drives N 2 fixation rates. Overall, the occurrence of record-high UCYN-A abundance and peak N 2 fixation rates in the cold coastal region where nitrate concentrations are highest (~200 nM) challenges current paradigms on what drives the distribution of diazotrophs and N 2 fixation.

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“…In young nodules of galegoid-clade legumes, mntH and mntABC were found to be highly expressed in the plant symbiont Rhizobium leguminosarum (Hood et al . 2017 ). Interestingly, both genes appeared essential for nitrogen fixation, and their expression was only upregulated in galegoid-clade and not in phaseloid-clade legumes.…”

Section: Roles Effects and Functional Origin Of Mn 2+ Transport And Homeostasis In Bacteriamentioning

confidence: 99%

“…It was suggested that this host effect is related to a difference in Mn 2+ availability and/or ROS concentration in the different plant species (Hood et al . 2017 ).…”

Section: Roles Effects and Functional Origin Of Mn 2+ Transport And Homeostasis In Bacteriamentioning

confidence: 99%

Regulation and distinct physiological roles of manganese in bacteria

Bosma

Rau

Gijtenbeek

et al. 2021

FEMS Microbiology Reviews

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Manganese (Mn2+) is an essential trace element within organisms spanning the entire tree of life. In this review, we provide an overview of Mn2+ transport and the regulation of its homeostasis in bacteria, with a focus on its functions beyond being a co-factor for enzymes. Crucial differences in Mn2+ homeostasis exist between bacterial species that can be characterized to have iron- or manganese-centric metabolism. Highly iron-centric species require minimal Mn2+ and mostly use it as a mechanism to cope with oxidative stress. As a consequence, tight regulation of Mn2+ uptake is required, while organisms that use both Fe2+ and Mn2+ need other layers of regulation for maintaining homeostasis. We will focus in detail on manganese-centric bacterial species, in particular lactobacilli, that require little to no Fe2+ and use Mn2+ for a wider variety of functions. These organisms can accumulate extraordinarily high amounts of Mn2+ intracellularly, enabling the non-enzymatic use of Mn2+ for decomposition of reactive oxygen species while simultaneously functioning as a mechanism of competitive exclusion. We further discuss how Mn2+ accumulation can provide both beneficial and pathogenic bacteria with advantages in thriving in their niches.

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Manganese transport is essential for N₂‐fixation by Rhizobium leguminosarum in bacteroids from galegoid but not phaseoloid nodules

Cited by 16 publications

References 66 publications

Sinorhizobium meliloti RNase III: Catalytic Features and Impact on Symbiosis

Sinorhizobium meliloti RNase III: Catalytic Features and Impact on Symbiosis

New insights into the distributions of nitrogen fixation and diazotrophs revealed by high-resolution sensing and sampling methods

Regulation and distinct physiological roles of manganese in bacteria

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Manganese transport is essential for N2‐fixation by Rhizobium leguminosarum in bacteroids from galegoid but not phaseoloid nodules

Cited by 16 publications

References 66 publications

Sinorhizobium meliloti RNase III: Catalytic Features and Impact on Symbiosis

Sinorhizobium meliloti RNase III: Catalytic Features and Impact on Symbiosis

New insights into the distributions of nitrogen fixation and diazotrophs revealed by high-resolution sensing and sampling methods

Regulation and distinct physiological roles of manganese in bacteria

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Manganese transport is essential for N₂‐fixation by Rhizobium leguminosarum in bacteroids from galegoid but not phaseoloid nodules