The metabolic acclimation of <i>Arabidopsis thaliana</i> to arsenate is sensitized by the loss of mitochondrial LIPOAMIDE DEHYDROGENASE2, a key enzyme in oxidative metabolism

Taylor, Nicolas L.; Chi, Yingjun; Millar, A. Harvey; Lambers, Hans; Finnegan, Patrick M.

doi:10.1111/pce.12187

Cited by 27 publications

(16 citation statements)

References 54 publications

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“…As(III) is known to inhibit pyruvate dehydrogenase and 2-oxoglutarate dehydrogenase multienzyme complexes since it binds to the lipoic acid and dithiol moieties of these enzymes (45)(46)(47)(48). In addition, ROS generated by arsenic degrades Fe-S clusters, which are components of aconitase, succinate dehydrogenase, and fumarase.…”

Section: Resultsmentioning

confidence: 99%

Expression of Genes and Proteins Involved in Arsenic Respiration and Resistance in Dissimilatory Arsenate-Reducing Geobacter sp. Strain OR-1

Tsuchiya

Ehara

Kasahara

et al. 2019

Appl Environ Microbiol

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The reduction of arsenate [As(V)] to arsenite [As(III)] by dissimilatory As(V)-reducing bacteria, such as Geobacter spp., may play a significant role in arsenic release from anaerobic sediments into groundwater. The biochemical and molecular mechanisms by which these bacteria cope with this toxic element remain unclear. In this study, the expression of several genes involved in arsenic respiration (arr) and resistance (ars) was determined using Geobacter sp. strain OR-1, the only cultured Geobacter strain capable of As(V) respiration. In addition, proteins expressed differentially under As(V)-respiring conditions were identified by semiquantitative proteomic analysis. Dissimilatory As(V) reductase (Arr) of strain OR-1 was localized predominantly in the periplasmic space, and the transcription of its gene (arrA) was upregulated under As(V)-respiring conditions. The transcription of the detoxifying As(V) reductase gene (arsC) was also upregulated, but its induction required 500 times higher concentration of As(III) (500 M) than did the arrA gene. Comparative proteomic analysis revealed that in addition to the Arr and Ars proteins, proteins involved in the following processes were upregulated under As(V)-respiring conditions: (i) protein folding and assembly for rescue of proteins with oxidative damage, (ii) DNA replication and repair for restoration of DNA breaks, (iii) anaplerosis and gluconeogenesis for sustainable energy production and biomass formation, and (iv) protein and nucleotide synthesis for the replacement of damaged proteins and nucleotides. These results suggest that strain OR-1 copes with arsenic stress by orchestrating pleiotropic processes that enable this bacterium to resist and actively metabolize arsenic. IMPORTANCE Dissimilatory As(V)-reducing bacteria, such as Geobacter spp., play significant roles in arsenic release and contamination in groundwater and threaten the health of people worldwide. However, the biochemical and molecular mechanisms by which these bacteria cope with arsenic toxicity remain unclear. In this study, it was found that both respiratory and detoxifying As(V) reductases of a dissimilatory As(V)-reducing bacterium, Geobacter sp. strain OR-1, were upregulated under As(V)respiring conditions. In addition, various proteins expressed specifically or more abundantly in strain OR-1 under arsenic stress were identified. Strain OR-1 actively metabolizes arsenic while orchestrating various metabolic processes that repair oxidative damage caused by arsenic. Such information is useful in assessing and identifying possible countermeasures for the prevention of microbial arsenic release in nature.

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Section: Resultsmentioning

confidence: 99%

Expression of Genes and Proteins Involved in Arsenic Respiration and Resistance in Dissimilatory Arsenate-Reducing Geobacter sp. Strain OR-1

Tsuchiya

Ehara

Kasahara

et al. 2019

Appl Environ Microbiol

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“…Specific examples relevant to the current study include documented inhibition of pyruvate dehydrogenase (PDH), α‐ketoglutarate dehydrogenase (KGDH) and branched‐chain α‐ketoacid dehydrogenase (BCKDH) enzymes. These enzymes all contain a dihydrolipoamide dehydrogenase subunit that is sensitive to As(III) inactivation across organisms (Bergquist et al ., ; Afzal et al ., ; Chen et al ., ). Inhibition of these specific enzymes is consistent with the measured increase in abundance of several metabolites observed in As(III) exposed A. tumefaciens 5A (Fig.…”

Section: Discussionmentioning

confidence: 97%

Metabolic response of Agrobacterium tumefaciens 5A to arsenite

Tokmina‐Lukaszewska

Shi

Tripet

et al. 2017

Environmental Microbiology

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Wide-spread abundance in soil and water, coupled with high toxicity have put arsenic at the top of the list of environmental contaminants. Early studies demonstrated that both concentration and the valence state of inorganic arsenic (arsenite, As(III) vs. arsenate As(V)) can be modulated by microbes. Using genetics, transcriptomic and proteomic techniques, microbe-arsenic detoxification, respiratory As(V) reduction and As(III) oxidation have since been examined. The effect of arsenic exposure on whole-cell intracellular microbial metabolism, however, has not been extensively studied. We combined LC-MS and H NMR to quantify metabolic changes in Agrobacterium tumefaciens (strain 5A) upon exposure to sub-lethal concentrations of As(III). Metabolomics analysis reveals global differences in metabolite concentrations between control and As(III) exposure groups, with significant perturbations to intermediates shuttling into and cycling within the TCA cycle. These data are most consistent with the disruption of two key TCA cycle enzymes, pyruvate dehydrogenase and α-ketoglutarate dehydrogenase. Glycolysis also appeared altered following As(III) stress, with carbon accumulating as complex saccharides. These observations suggest that an important consequence of As(III) contamination in nature will be to alter microbial carbon metabolism at the microbial community level and thus has the potential to foundationally impact all biogeochemical cycles in the environment.

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“…The cytoplasmic redox potential of root cells strongly increased within a few hours upon addition of As and HpxAs; the increase was slightly delayed and of lower magnitude in Hpx (Figure ). The likely reason is the decrease in cell energization (ATP/ADP) by inhibition of mitochondrial respiration and disturbance of mitochondrial redox homeostasis in the presence of As (Chen et al, ). The partial recovery of the cytosolic redox potential under As during the prolonged 7‐day exposure indicates acclimation presumably by vacuolar compartmentation mediated by ABCC1 and ABCC2 (Sharma, Dietz, & Mimura, ; Song et al, ).…”

Section: Discussionmentioning

confidence: 99%

Interference between arsenic‐induced toxicity and hypoxia

Kumar

Vogelsang

Seidel

et al. 2018

Plant Cell & Environment

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Plants often face combinatorial stresses in their natural environment. Here, arsenic (As) toxicity was combined with hypoxia (Hpx) in the roots of Arabidopsis thaliana as it often occurs in nature. Arsenic inhibited growth of both roots and leaves, whereas root growth almost entirely ceased in Hpx. Growth efficiently resumed, and Hpx marker transcripts decreased upon reaeration. Compromised recovery from HpxAs treatment following reaeration indicated some persistent effects of combined stresses despite lower As accumulation. Root glutathione redox potential turned more oxidized in Hpx and most strongly in HpxAs. The more oxidizing root cell redox potential and the lowered glutathione amounts may be conducive to the growth arrest of plants exposed to HpxAs. The stresses elicited changes in elemental and transcriptomic composition. Thus, calcium, magnesium, and phosphorous amounts decreased in rosettes, but the strongest decline was seen for potassium. The reorganized potassium-related transcriptome supports the conclusion that disturbed potassium homeostasis contributes to the growth phenotype. In a converse manner, photosynthesis-related parameters were hardly affected, whereas accumulated carbohydrates under all stresses and anthocyanins under Hpx exclude carbohydrate limitation. The study demonstrates the existence of both synergistic since mutually aggravating effects and antagonistic effects of single and combined stresses.

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The metabolic acclimation of Arabidopsis thaliana to arsenate is sensitized by the loss of mitochondrial LIPOAMIDE DEHYDROGENASE2, a key enzyme in oxidative metabolism

Cited by 27 publications

References 54 publications

Expression of Genes and Proteins Involved in Arsenic Respiration and Resistance in Dissimilatory Arsenate-Reducing Geobacter sp. Strain OR-1

Expression of Genes and Proteins Involved in Arsenic Respiration and Resistance in Dissimilatory Arsenate-Reducing Geobacter sp. Strain OR-1

Metabolic response of Agrobacterium tumefaciens 5A to arsenite

Interference between arsenic‐induced toxicity and hypoxia

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