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Evolutionary Relationships Between Low Potential Ferredoxin and Flavodoxin Electron Carriers.

ABSTRACT: Proteins from the ferredoxin (Fd) and flavodoxin (Fld) families function as low potential electrical transfer hubs in cells, at times mediating electron transfer between overlapping sets of oxidoreductases. To better understand protein electron carrier (PEC) use across the domains of life, we evaluated the distribution of genes encoding [4Fe-4S] Fd, [2Fe-2S] Fd, and Fld electron carriers in over 7,000 organisms. Our analysis targeted genes encoding small PEC genes encoding proteins having ?200 residues. We find that the average number of small PEC genes per Archaea (~13), Bacteria (~8), and Eukarya (~3) genome varies, with some organisms containing as many as 54 total PEC genes. Organisms fall into three groups, including those lacking genes encoding low potential PECs (3%), specialists with a single PEC gene type (20%), and generalists that utilize multiple PEC types (77%). Mapping PEC gene usage onto an evolutionary tree highlights the prevalence of [4Fe-4S] Fds in ancient organisms that are deeply rooted, the expansion of [2Fe-2S] Fds with the advent of photosynthesis and a concomitant decrease in [4Fe-4S] Fds, and the expansion of Flds in organisms that inhabit low-iron host environments. Surprisingly, [4Fe-4S] Fds present a similar abundance in aerobes as [2Fe-2S] Fds. This bioinformatic study highlights understudied PECs whose structure, stability, and partner specificity should be further characterized.

SUBMITTER: Campbell IJ

PROVIDER: S-EPMC7039249 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Evolutionary Relationships Between Low Potential Ferredoxin and Flavodoxin Electron Carriers.

Campbell Ian J IJ Bennett George N GN Silberg Jonathan J JJ

Frontiers in energy research 20190823

Proteins from the ferredoxin (Fd) and flavodoxin (Fld) families function as low potential electrical transfer hubs in cells, at times mediating electron transfer between overlapping sets of oxidoreductases. To better understand protein electron carrier (PEC) use across the domains of life, we evaluated the distribution of genes encoding [4Fe-4S] Fd, [2Fe-2S] Fd, and Fld electron carriers in over 7,000 organisms. Our analysis targeted genes encoding small PEC genes encoding proteins having ≤200 r ...[more]

PMID: 32095484

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Project description:UNLABELLED:The trxB2 gene, which is annotated as a thioredoxin reductase, was found to be essential for growth of Lactococcus lactis in the presence of oxygen. The corresponding protein (TrxB2) showed a high similarity with Bacillus subtilis YumC (E value = 4.0E-88), and YumC was able to fully complement the ΔtrxB2 mutant phenotype. YumC represents a novel type of ferredoxin (flavodoxin) reductase (FdR) with hitherto-unknown biological function. We adaptively evolved the ΔtrxB2 mutant under aerobic conditions to find suppressor mutations that could help elucidate the involvement of TrxB2 in aerobic growth. Genome sequencing of two independent isolates, which were able to grow as well as the wild-type strain under aerated conditions, revealed the importance of mutations in nrdI, encoding a flavodoxin involved in aerobic ribonucleotide reduction. We suggest a role for TrxB2 in nucleotide metabolism, where the flavodoxin (NrdI) serves as its redox partner, and we support this hypothesis by showing the beneficial effect of deoxynucleosides on aerobic growth of the ΔtrxB2 mutant. Finally, we demonstrate, by heterologous expression, that the TrxB2 protein functionally can substitute for YumC in B. subtilis but that the addition of deoxynucleosides cannot compensate for the lethal phenotype displayed by the B. subtilis yumC knockout mutant. IMPORTANCE:Ferredoxin (flavodoxin) reductase (FdR) is involved in many important reactions in both eukaryotes and prokaryotes, such as photosynthesis, nitrate reduction, etc. The recently identified bacterial YumC-type FdR belongs to a novel type, the biological function of which still remains elusive. We found that the YumC-like FdR (TrxB2) is essential for aerobic growth of Lactococcus lactis. We suggest that the YumC-type FdR is involved in the ribonucleotide reduction by the class Ib ribonucleotide reductase, which represents the workhorse for the bioconversion of nucleotides to deoxynucleotides in many prokaryotes and eukaryotic pathogens under aerobic conditions. As the partner of the flavodoxin (NrdI), the key FdR is missing in the current model describing the class Ib system in Escherichia coli. With this study, we have established a role for this novel type of FdR and in addition found the missing link needed to explain how ribonucleotide reduction is carried out under aerobic conditions.

Dataset Information

Evolutionary Relationships Between Low Potential Ferredoxin and Flavodoxin Electron Carriers.

Publications

Evolutionary Relationships Between Low Potential Ferredoxin and Flavodoxin Electron Carriers.

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