Origin and phylogenetic relationships of [4Fe–4S]‐containing O<sub>2</sub> sensors of bacteria

Barth, C. A.; Weiss, Madeline C.; Roettger, Mayo; Martin, William; Unden, Gottfried

doi:10.1111/1462-2920.14411

Cited by 13 publications

(17 citation statements)

References 162 publications

(263 reference statements)

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“…The [Fe]-HYD homologues IOP1/NAR1 repress the hypoxia-inducible factor-1α subunit (HIF1-α) in humans [32] and, furthermore, possess conserved functions in cytosolic FeS cluster assembly in the human and yeast [33,34]. Prokaryotes employ O 2 -labile FeS clusters for O 2 -sensing and signalling [35]. In land plants, the [Fe]-HYD homologue has relinquished enzymatic activity to become the oxygen sensor GOLLUM [36].…”

Section: Distribution Of Enzymes For Anaerobic Metabolism In Eukaryotesmentioning

confidence: 99%

Adaptation to life on land at high O₂via transition from ferredoxin-to NADH-dependent redox balance

Gould

Handrich

et al. 2019

Proc. R. Soc. B.

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Pyruvate : ferredoxin oxidoreductase (PFO) and iron only hydrogenase ([Fe]-HYD) are common enzymes among eukaryotic microbes that inhabit anaerobic niches. Their function is to maintain redox balance by donating electrons from food oxidation via ferredoxin (Fd) to protons, generating H 2 as a waste product. Operating in series, they constitute a soluble electron transport chain of one-electron transfers between FeS clusters. They fulfil the same function—redox balance—served by two electron-transfers in the NADH- and O 2 -dependent respiratory chains of mitochondria. Although they possess O 2 -sensitive FeS clusters, PFO, Fd and [Fe]-HYD are also present among numerous algae that produce O 2 . The evolutionary persistence of these enzymes among eukaryotic aerobes is traditionally explained as adaptation to facultative anaerobic growth. Here, we show that algae express enzymes of anaerobic energy metabolism at ambient O 2 levels (21% v/v), Chlamydomonas reinhardtii expresses them with diurnal regulation. High O 2 environments arose on Earth only approximately 450 million years ago. Gene presence/absence and gene expression data indicate that during the transition to high O 2 environments and terrestrialization, diverse algal lineages retained enzymes of Fd-dependent one-electron-based redox balance, while the land plant and land animal lineages underwent irreversible specialization to redox balance involving the O 2 -insensitive two-electron carrier NADH.

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Section: Distribution Of Enzymes For Anaerobic Metabolism In Eukaryotesmentioning

confidence: 99%

Adaptation to life on land at high O₂via transition from ferredoxin-to NADH-dependent redox balance

Gould

Handrich

et al. 2019

Proc. R. Soc. B.

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“…Sequences were aligned using Unipro UGENE Version 1.31.1 (Okonechnikov, Golosova, & Fursov, ). The HisKA_3 sequence logo in Figure b is derived from the sequence of S. carnosus NreB and 70 homologous proteins (Barth et al, ) using MEME Suite Version 5.0.5. (Bailey, Williams, Misleh, & Li, ).…”

Section: Methodsmentioning

confidence: 99%

“…The HisKA_3 sequence logo in Figure 1b is derived from the sequence of S. carnosus NreB and 70 homologous proteins (Barth et al, 2018) using MEME Suite Version 5.0.5. (Bailey, Williams, Misleh, & Li, 2006).…”

Section: Sequence Comparisonsmentioning

confidence: 99%

“…Sensitivity to O 2 resides in the sensor kinase NreB, which contains an O 2 ‐sensitive iron–sulfur cluster in the sensory PAS domain (Kamps, Achebach, Fedtke, Unden, & Götz, ; Müllner et al, ) of the FNR type (Crack, Green, Cheesman, Le Brun, & Thomson, ; Crack, Thomson, Brun, & Nick, ; Khoroshilova, Popescu, Münck, Beinert, & Kiley, ; Kiley & Beinert, ). Under anoxic conditions, the cluster prevails as a [4Fe‐4S] 2+ cluster that is decomposed in the presence of O 2 to the [2Fe‐2Fe] 2+ form (Barth, Weiss, Roettger, Martin, & Unden, ; Müllner et al, ; Unden, Nilkens, & Singenstreu, ). The cluster conversion is linked to decreased kinase (or autophosphorylation) activity of NreB (Müllner et al, ), and the resulting expression of narG is decreased by a factor of >5 in the anaerobic/aerobic transition (Nilkens et al, ).…”

Section: Introductionmentioning

confidence: 99%

“…that is decomposed in the presence of O 2 to the [2Fe-2Fe] 2+ form (Barth, Weiss, Roettger, Martin, & Unden, 2018;Müllner et al, 2008;Unden, Nilkens, & Singenstreu, 2013). The cluster conversion is linked to decreased kinase (or autophosphorylation) activity of NreB (Müllner et al, 2008), and the resulting expression of narG is decreased by a factor of >5 in the anaerobic/aerobic transition .…”

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Control of the bifunctional O₂‐sensor kinase NreB of Staphylococcus carnosus by the nitrate sensor NreA: Switching from kinase to phosphatase state

Klein

Kretzschmar

Unden

2019

Molecular Microbiology

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The NreB–NreC two‐component system of Staphylococcus carnosus for O2 sensing cooperates with the accessory nitrate sensor NreA in the NreA–NreB–NreC system for coordinated sensing and regulation of nitrate respiration by O2 and nitrate. ApoNreA (NreA in the absence of nitrate) interacts with NreB and inhibits NreB autophosphorylation (and activation). NreB contains the phosphatase motif DxxxQ. The present study shows that NreB on its own was inactive for the dephosphorylation of the phosphorylated response regulator NreC (NreC‐P), but co‐incubation with NreB and NreA stimulated NreC‐P dephosphorylation. Either the presence of NreA·NO3- instead of apoNreA or mutation of the phosphatase motif (D160 or Q164) of NreB abrogated phosphatase activity of NreB. Phosphatase activity was observed for anoxic (active) NreB as well as oxic NreB, therefore the functional state of NreB is not relevant for phosphatase activity. Thus, NreB is a bifunctional sensor kinase with an integral cryptic phosphatase activity. Activation of phosphatase activity and dephosphorylation of NreC‐P requires NreA as a cofactor. Accordingly, NreA and nitrate have major and dual roles in NreA–NreB–NreC regulation by (i) inhibiting NreB phosphorylation and (ii) triggering a kinase/phosphatase switch of NreB when present as apoNreA.

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Sepsis, pyruvate, and mitochondria energy supply chain shortage

McCall

Zhu

Zabalawi

et al. 2022

Journal of Leukocyte Biology

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Balancing high energy-consuming danger resistance and low energy supply of disease tolerance is a universal survival principle that often fails during sepsis. Our research supports the concept that sepsis phosphorylates and deactivates mitochondrial pyruvate dehydrogenase complex control over the tricarboxylic cycle and the electron transport chain. StimulatIng mitochondrial energetics in septic mice and human sepsis cell models can be achieved by inhibiting pyruvate dehydrogenase kinases with the pyruvate structural analog dichloroacetate. Stimulating the pyruvate dehydrogenase complex by dichloroacetate reverses a disruption in the tricarboxylic cycle that induces itaconate, a key mediator of the disease tolerance pathway. Dichloroacetate treatment increases mitochondrial respiration and ATP synthesis, decreases oxidant stress, overcomes metabolic paralysis, regenerates tissue, organ, and innate and adaptive immune cells, and doubles the survival rate in a murine model of sepsis.

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Origin and phylogenetic relationships of [4Fe–4S]‐containing O₂ sensors of bacteria

Cited by 13 publications

References 162 publications

Adaptation to life on land at high O₂via transition from ferredoxin-to NADH-dependent redox balance

Adaptation to life on land at high O₂via transition from ferredoxin-to NADH-dependent redox balance

Control of the bifunctional O₂‐sensor kinase NreB of Staphylococcus carnosus by the nitrate sensor NreA: Switching from kinase to phosphatase state

Sepsis, pyruvate, and mitochondria energy supply chain shortage

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Origin and phylogenetic relationships of [4Fe–4S]‐containing O2 sensors of bacteria

Cited by 13 publications

References 162 publications

Adaptation to life on land at high O2via transition from ferredoxin-to NADH-dependent redox balance

Adaptation to life on land at high O2via transition from ferredoxin-to NADH-dependent redox balance

Control of the bifunctional O2‐sensor kinase NreB of Staphylococcus carnosus by the nitrate sensor NreA: Switching from kinase to phosphatase state

Sepsis, pyruvate, and mitochondria energy supply chain shortage

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Origin and phylogenetic relationships of [4Fe–4S]‐containing O₂ sensors of bacteria

Adaptation to life on land at high O₂via transition from ferredoxin-to NADH-dependent redox balance

Adaptation to life on land at high O₂via transition from ferredoxin-to NADH-dependent redox balance

Control of the bifunctional O₂‐sensor kinase NreB of Staphylococcus carnosus by the nitrate sensor NreA: Switching from kinase to phosphatase state