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Oxidation of cytochrome 605 is the rate limiting step when Ferrimicrobium ferriphilum respires aerobically on soluble iron

ABSTRACT: Proteins that oxidize extracellular substrates in Gram-positive bacteria are poorly understood. Ferrimicrobium acidiphilum is an actinobacterium that respires aerobically on extracellular ferrous ions at pH 1.5. In situ absorbance measurements were conducted on turbid suspensions of intact Fm. acidiphilum using an integrating cavity absorption meter designed for that purpose. Initial velocity kinetic studies monitored the appearance of product ferric ions in the presence of catalytic quantities of cells. Cell-catalyzed iron oxidation obeyed the Michaelis-Menten equation with values for KM and Vmax of 71 µM and 0.29 fmol/min/cell, respectively. Cell-monitored turnover kinetic studies conducted with higher concentrations of cells revealed that only a single cytochrome with reduced absorbance peaks at 448 and 605 nm was visible as the cells respired aerobically on iron. The reduced cytochrome 605 exhibited mathematical and correlational properties that were consistent with the hypothesis that oxidation of the cytochrome constituted the rate-limiting step in the aerobic respiratory process with a turnover number of 35 ± 2 s-1. Genomic and proteomic analyses showed that Fm. acidiphilum expressed two a-type heme copper terminal oxidases. Cytochrome 605 was associated with the terminal oxidase genes that occur earlier in the annotated circular genome of this bacterium.

INSTRUMENT(S): Orbitrap Fusion

ORGANISM(S): Ferrimicrobium Acidiphilum Dsm 19497

SUBMITTER: Jessie Guidry

LAB HEAD: Jessie J Guidry

PROVIDER: PXD019436 | Pride | 2020-09-07

REPOSITORIES: Pride

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Project description:Hydrogen can be an important source of energy for chemolithotrophic acidophiles, especially in the deep terrestrial subsurface. Nevertheless, the current knowledge of microbial hydrogen utilization in acidic environments is minimal. A multi-omics analysis was applied on Acidithiobacillus ferrooxidans growing aerobically and anaerobically (with ferric iron) on hydrogen as an electron donor, and a respiratory model proposed from the results obtained. In this model, both [NiFe] hydrogenases, cytoplasmic uptake and membrane-bound respiratory, oxidize molecular hydrogen to two protons and two electrons. The electrons are used to reduce membrane-soluble ubiquinone to ubiquinol. Genetically associated [FeS]-binding proteins mediate electron relay from the hydrogenases to the ubiquinone pool. Under aerobic conditions, reduced ubiquinol transfers electrons to either cytochrome aa3 oxidase via cytochrome bc1 complex and cytochrome c4 or the alternate directly to cytochrome bd oxidase, resulting in proton efflux together with the reduction of molecular oxygen to water. Under anaerobic conditions, reduced ubiquinol transfers electrons to outer membrane cytochrome c (ferric iron reductase) via cytochrome bc1 complex and a cascade of electron transporters (cytochrome c4, cytochrome c552, rusticyanin, and high potential iron-sulfur protein), resulting in proton efflux together with the reduction of ferric iron to ferrous iron. The proton gradient generated by molecular hydrogen oxidation maintains the membrane potential and allows the generation of ATP via ATP synthase and NADH via NADH-ubiquinone oxidoreductase. To a lesser extent, NADH can also be generated by another bidirectional cytoplasmic hydrogenase. ATP and NADH are further utilized in the Calvin–Benson–Bassham cycle for inorganic carbon uptake and assimilation. These results further clarify the role of extremophiles in biogeochemical processes and their impact on the composition and features of the deep terrestrial subsurface from the distant past to the present.

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Oxidation of cytochrome 605 is the rate limiting step when Ferrimicrobium ferriphilum respires aerobically on soluble iron

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