Characterization of the N-ATPase, a distinct, laterally transferred Na+-translocating form of the bacterial F-type membrane ATPase

Dibrova, Daria V.; Galperin, Michael Y.; Mulkidjanian, Armen Y.

doi:10.1093/bioinformatics/btq234

Cited by 65 publications

(82 citation statements)

References 33 publications

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“…Bioinformatic investigation of the putative operon suggests that it encodes not the primary ATP synthase of R. palustris but a secondary complex present only in R. palustris TIE-1, not in related strains. The operon structure, as well as the presence of certain subunits, indicates that this complex belongs to the family of Na-dependent ATP synthases (44). In Archaea, these Na-ATP synthases function as the primary manufacturers of ATP.…”

Section: Discussionmentioning

confidence: 99%

Iron and Copper Act Synergistically To Delay Anaerobic Growth of Bacteria

Bird

Coleman

Newman

2013

Appl Environ Microbiol

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bTransition metals are known to cause toxic effects through their interaction with oxygen, but toxicity under anoxic conditions is poorly understood. Here we investigated the effects of iron (Fe) and copper (Cu) on the anaerobic growth and gene expression of the purple phototrophic bacterium Rhodopseudomonas palustris TIE-1. We found that Fe(II) and Cu(II) act synergistically to delay anaerobic growth at environmentally relevant metal concentrations. Cu(I) and Cu(II) had similar effects both alone and in the presence of ascorbate, a Cu(II) reductant, indicating that reduction of Cu(II) to Cu(I) by Fe(II) is not sufficient to explain the growth inhibition. Addition of Cu(II) increased the toxicity of Co(II) and Ni(II); in contrast, Ni(II) toxicity was diminished in the presence of Fe(II). The synergistic anaerobic toxicity of Fe(II) and Cu(II) was also observed for Escherichia coli MG1655, Shewanella oneidensis MR-1, and Rhodobacter capsulatus SB1003. Gene expression analyses for R. palustris identified three regulatory genes that respond to Cu(II) and not to Fe(II): homologs of cueR and cusR, two known proteobacterial copper homeostasis regulators, and csoR, a copper regulator recently identified in Mycobacterium tuberculosis. Two P-type ATPase efflux pumps, along with an F o F 1 ATP synthase, were also upregulated by Cu(II) but not by Fe(II). An Escherichia coli mutant deficient in copA, cus, and cueO showed a smaller synergistic effect, indicating that iron might interfere with one or more of the copper homeostasis systems. Our results suggest that interactive effects of transition metals on microbial physiology may be widespread under anoxic conditions, although the molecular mechanisms remain to be more fully elucidated.

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Section: Discussionmentioning

confidence: 99%

Iron and Copper Act Synergistically To Delay Anaerobic Growth of Bacteria

Bird

Coleman

Newman

2013

Appl Environ Microbiol

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“…These enzyme complexes are reversible, rotary molecular machines that couple ion transfer across the membrane with the synthesis or hydrolysis of ATP (see [109–115] and references therein). The rotary ATPases fall into two distinct types, namely the F/N-type that is present in bacteria, a few archaea, mitochondria, and chloroplasts, and A/V-type, which is represented in archaea, some bacteria, and in the cytoplasmic and vacuolar membranes of eukaryotes.…”

Section: Emergence Of Membrane Bioenergeticsmentioning

confidence: 99%

“…Considering the revealed evolutionary primacy of Na + -dependent membrane energetics, we hypothesized that the function of the first ion-translocating rotary ATPase was to expel sodium ions out of the cell [10, 12]. In a search for relics of such primordial rotary Na + export pump, we have identified, by means of phylogenomic analysis, a distinct family of rotary ATPases (N-ATPases), almost all members of which, as judged from the sequence of their proteolipid subunits, appeared to be Na + -translocating ATPases [115]. These enzymes are encoded by a highly mobile operon, which always co-occurs with the operon coding for the “main” F-type or A/V-type ATP synthase typical of the respective prokaryotic group.…”

Section: Emergence Of Membrane Bioenergeticsmentioning

confidence: 99%

Ancient systems of sodium/potassium homeostasis as predecessors of membrane bioenergetics

Dibrova

Galperin

Koonin

et al. 2015

Biochemistry Moscow

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Cell cytoplasm of archaea, bacteria, and eukaryotes contains substantially more potassium than sodium, and potassium cations are specifically required for many key cellular processes, including protein synthesis. This distinct ionic composition and requirements have been attributed to the emergence of the first cells in potassium-rich habitats. Different, albeit complementary, scenarios have been proposed for the primordial potassium-rich environments based on experimental data and theoretical considerations. Specifically, building on the observation that potassium prevails over sodium in the vapor of inland geothermal systems, we have argued that the first cells could emerge in the pools and puddles at the periphery of primordial anoxic geothermal fields, where the elementary composition of the condensed vapor would resemble the internal milieu of modern cells. Marine and freshwater environments generally contain more sodium than potassium. Therefore, to invade such environments, while maintaining excess of potassium over sodium in the cytoplasm, primordial cells needed means to extrude sodium ions. The foray into new, sodium-rich habitats was the likely driving force behind the evolution of diverse redox-, light-, chemically-, or osmotically-dependent sodium export pumps and the increase of membrane tightness. Here we present a scenario that details how the interplay between several, initially independent sodium pumps might have triggered the evolution of sodium-dependent membrane bioenergetics, followed by the separate emergence of the proton-dependent bioenergetics in archaea and bacteria. We also discuss the development of systems that utilize the sodium/potassium gradient across the cell membranes.

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“…Both these clusters showed a decreased expression at sample point II (mRNA ratio of 0.4 to 0.5). The genes of the third cluster, GOX2167 to GOX 2175, might code for an Na ϩ -translocating F 1 F 0 -ATP synthase (33) and showed an increased expression at sample point II (mRNA ratio of 1.4 to 3.3).…”

Section: Intracellular Carbon Fluxes Of Phosphorylated Compoundsmentioning

confidence: 99%

Combined Fluxomics and Transcriptomics Analysis of Glucose Catabolism via a Partially Cyclic Pentose Phosphate Pathway in Gluconobacter oxydans 621H

Hanke¹,

Nöh²,

Noack³

et al. 2013

Appl Environ Microbiol

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In this study, the distribution and regulation of periplasmic and cytoplasmic carbon fluxes in Gluconobacter oxydans 621H with glucose were studied by 13 C-based metabolic flux analysis ( 13 C-MFA) in combination with transcriptomics and enzyme assays. For 13 C-MFA, cells were cultivated with specifically 13 C-labeled glucose, and intracellular metabolites were analyzed for their labeling pattern by liquid chromatography-mass spectrometry (LC-MS). In growth phase I, 90% of the glucose was oxidized periplasmically to gluconate and partially further oxidized to 2-ketogluconate. Of the glucose taken up by the cells, 9% was phosphorylated to glucose 6-phosphate, whereas 91% was oxidized by cytoplasmic glucose dehydrogenase to gluconate. Additional gluconate was taken up into the cells by transport. Of the cytoplasmic gluconate, 70% was oxidized to 5-ketogluconate and 30% was phosphorylated to 6-phosphogluconate. In growth phase II, 87% of gluconate was oxidized to 2-ketogluconate in the periplasm and 13% was taken up by the cells and almost completely converted to 6-phosphogluconate. Since G. oxydans lacks phosphofructokinase, glucose 6-phosphate can be metabolized only via the oxidative pentose phosphate pathway (PPP) or the Entner-Doudoroff pathway (EDP).13 C-MFA showed that 6-phosphogluconate is catabolized primarily via the oxidative PPP in both phases I and II (62% and 93%) and demonstrated a cyclic carbon flux through the oxidative PPP. The transcriptome comparison revealed an increased expression of PPP genes in growth phase II, which was supported by enzyme activity measurements and correlated with the increased PPP flux in phase II. Moreover, genes possibly related to a general stress response displayed increased expression in growth phase II.

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Characterization of the N-ATPase, a distinct, laterally transferred Na+-translocating form of the bacterial F-type membrane ATPase

Cited by 65 publications

References 33 publications

Iron and Copper Act Synergistically To Delay Anaerobic Growth of Bacteria

Iron and Copper Act Synergistically To Delay Anaerobic Growth of Bacteria

Ancient systems of sodium/potassium homeostasis as predecessors of membrane bioenergetics

Combined Fluxomics and Transcriptomics Analysis of Glucose Catabolism via a Partially Cyclic Pentose Phosphate Pathway in Gluconobacter oxydans 621H

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