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The teleos of metallo-reduction and metallo-oxidation in eukaryotic iron and copper trafficking.

ABSTRACT: Eukaryotic cells, whether free-living or organismal, rely on metallo-reductases to process environmental ferric iron and cupric copper prior to uptake. In addition, some free-living eukaryotes (e.g. fungi and algae) couple ferri-reduction to ferro-oxidation, a process catalyzed by a small cohort of multi-copper oxidases; in these organisms, the ferric iron product is a ligand for cell iron uptake via a ferric iron permease. In addition to their support of iron uptake in lower eukaryotes, ferroxidases support ferrous iron efflux in Chordata; in this process the release of the ferrous iron from the efflux transporter is catalyzed by its ferroxidation. Last, ferroxidases also catalyze the oxidation of cuprous copper and, as metallo-oxidases, mirror the dual activity of the metallo-reductases. This Perspective examines the teleos of the yin-yang of this redox cycling of iron and copper in their metabolism.

SUBMITTER: Kosman DJ

PROVIDER: S-EPMC5864563 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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The teleos of metallo-reduction and metallo-oxidation in eukaryotic iron and copper trafficking.

Kosman Daniel J DJ

Metallomics : integrated biometal science 20180227 3

Eukaryotic cells, whether free-living or organismal, rely on metallo-reductases to process environmental ferric iron and cupric copper prior to uptake. In addition, some free-living eukaryotes (e.g. fungi and algae) couple ferri-reduction to ferro-oxidation, a process catalyzed by a small cohort of multi-copper oxidases; in these organisms, the ferric iron product is a ligand for cell iron uptake via a ferric iron permease. In addition to their support of iron uptake in lower eukaryotes, ferroxi ...[more]

PMID: 29484341

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Project description:Fe(II)-oxidizing microorganisms and Fe(III)-reducing microorganisms, which drive the biogeochemical Fe cycle on the Earth's surface, are phylogenetically and ecologically diverse. However, no single organism capable of aerobic Fe(II) oxidation and anaerobic Fe(III) reduction at circumneutral pH have been reported so far. Here, we report a novel neutrophilic Fe(II)-oxidizing Rhodoferax bacterium, strain MIZ03, isolated from an iron-rich wetland in Japan. Our cultivation experiments demonstrate that MIZ03 represents a much more versatile metabolism for energy acquisition than previously recognized in the genus Rhodoferax. MIZ03 can grow chemolithoautotrophically at circumneutral pH by oxidation of Fe(II), H2, or thiosulfate as the sole electron donor under (micro)aerobic conditions (i.e., using O2 as the sole electron acceptor). In addition, it can reduce Fe(III) or nitrate under anaerobic conditions. Thus, this is the first report demonstrating the presence of a single bacterium capable of both Fe(II) oxidation and Fe(III) reduction at circumneutral pH. The observed physiology was consistent with its 4.9-Mbp complete genome encoding key genes for iron oxidation/reduction (foxEY and mtrABC), for nitrate reduction (narGHI), for thiosulfate oxidation (soxABCDXYZ), and for carbon fixation via the Calvin cycle. Our metagenomic survey suggests that there are more Rhodoferax members capable of Fe(II) oxidation and Fe(III) reduction. Such bifunctional Rhodoferax may have an ecological advantage in suboxic/anoxic environments at circumneutral pH by recycling of Fe as the electron donor and acceptor. IMPORTANCE The biogeochemical cycle of iron (Fe) via reactions of oxidation, reduction, precipitation, and dissolution is involved in the cycle of other ecologically relevant elements, such as C, N, P, S, As, Co, Ni, and Pb. The Fe cycle on the Earth's surface is driven by a variety of Fe(II)-oxidizing microorganisms and Fe(III)-reducing microorganisms. Here, we discovered a novel bacterium, Rhodoferax sp. strain MIZ03, capable of both Fe(II) oxidation and Fe(III) reduction at circumneutral pH, and we report its physiological characteristics and complete genome sequence. The unexpected capability of this bacterium provides novel insights into the Fe cycle in the environment. Moreover, this bacterium will help to better understand the molecular mechanisms of microbial Fe redox cycling as a model organism.

Dataset Information

The teleos of metallo-reduction and metallo-oxidation in eukaryotic iron and copper trafficking.

Publications

The teleos of metallo-reduction and metallo-oxidation in eukaryotic iron and copper trafficking.

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