Modular origins of biological electron transfer chains

Raanan, Hagai; Pike, Douglas H.; Moore, E. Colleen; Falkowski, Paul G.; Nanda, Vikas

doi:10.1073/pnas.1714225115

Cited by 34 publications

(52 citation statements)

References 49 publications

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“…One avenue to unraveling this question may be to examine the PEC "fossil record" from a structural perspective. A recent study using the structural database to study oxidoreductase evolution observed a modular origin of biological ET chains (Raanan et al, 2018). An additional way to elucidate this question is to use protein design to test ideas about ancestral PECs that are no longer observed in nature (Mutter et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Evolutionary Relationships Between Low Potential Ferredoxin and Flavodoxin Electron Carriers

2019

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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.

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Section: Discussionmentioning

confidence: 99%

Evolutionary Relationships Between Low Potential Ferredoxin and Flavodoxin Electron Carriers

2019

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“…Shuttling of electrons between life's macro-elements has had an evolutionary history at least as long as life itself, culminating in the tightly linked global metabolic network seen today. The genes encoding the enzymes responsible for oxidation and reduction reactions evolved, duplicated and mutated, and have been shared across many branches on the canonical tree of life (David and Alm, 2011;Raanan et al, 2018). An overarching driver for the evolution of life's electron transfer machinery has been the progressive oxidation, both abiotic and biological, of Earth's oceans and atmosphere (Catling et al, 2001;Jelen et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Elemental sulfur reduction in the deep‐sea vent thermophile, Thermovibrio ammonificans

Jelen

Giovannelli

Falkowski

et al. 2018

Environmental Microbiology

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The reduction of elemental sulfur is an important energy-conserving pathway in prokaryotes inhabiting geothermal environments, where sulfur respiration contributes to sulfur biogeochemical cycling. Despite this, the pathways through which elemental sulfur is reduced to hydrogen sulfide remain unclear in most microorganisms. We integrated growth experiments using Thermovibrio ammonificans, a deep-sea vent thermophile that conserves energy from the oxidation of hydrogen and reduction of both nitrate and elemental sulfur, with comparative transcriptomic and proteomic approaches, coupled with scanning electron microscopy. Our results revealed that two members of the FAD-dependent pyridine nucleotide disulfide reductase family, similar to sulfide-quinone reductase and to NADH-dependent sulfur reductase (NSR), respectively, are over-expressed during sulfur respiration. Scanning electron micrographs and sulfur sequestration experiments indicated that direct access of T. ammonificans to sulfur particles strongly promoted growth. The sulfur metabolism of T. ammonificans appears to require abiotic transition from bulk elemental sulfur to polysulfide to nanoparticulate sulfur at an acidic pH, coupled to biological hydrogen oxidation. A coupled biotic-abiotic mechanism for sulfur respiration is put forward, mediated by an NSR-like protein as the terminal reductase.

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“…Identifying Oxidoreductase Modules. To identify the building blocks of oxidoreductases, we applied a comparative structural alignment approach described previously (10) to a larger dataset of proteins encompassing both metal-containing and organic redox cofactors. Briefly, we isolated local cofactor-binding protein motifs (microenvironments) from deposited high-resolution structures from the Protein Data Bank (PDB) at http://wwpdb.org (13).…”

Section: Resultsmentioning

confidence: 99%

“…Previously, we published a network analysis of over 30,000 metal-coordination sites in high-resolution protein structures and discovered a small number of metal-binding modules that were recurrent across many proteins (10). Modules that bound transition metals often occurred in pairs or larger chains, making paths for electron transfer through the protein matrix.…”

Section: Rossmann Foldmentioning

confidence: 99%

Small protein folds at the root of an ancient metabolic network

Raanan

Poudel

Pike

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Life on Earth is driven by electron transfer reactions catalyzed by a suite of enzymes that comprise the superfamily of oxidoreductases (Enzyme Classification EC1). Most modern oxidoreductases are complex in their structure and chemistry and must have evolved from a small set of ancient folds. Ancient oxidoreductases from the Archean Eon between ca. 3.5 and 2.5 billion years ago have been long extinct, making it challenging to retrace evolution by sequence-based phylogeny or ancestral sequence reconstruction. However, three-dimensional topologies of proteins change more slowly than sequences. Using comparative structure and sequence profile-profile alignments, we quantify the similarity between proximal cofactor-binding folds and show that they are derived from a common ancestor. We discovered that two recurring folds were central to the origin of metabolism: ferredoxin and Rossmann-like folds. In turn, these two folds likely shared a common ancestor that, through duplication, recruitment, and diversification, evolved to facilitate electron transfer and catalysis at a very early stage in the origin of metabolism.

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Modular origins of biological electron transfer chains

Cited by 34 publications

References 49 publications

Evolutionary Relationships Between Low Potential Ferredoxin and Flavodoxin Electron Carriers

Evolutionary Relationships Between Low Potential Ferredoxin and Flavodoxin Electron Carriers

Elemental sulfur reduction in the deep‐sea vent thermophile, Thermovibrio ammonificans

Small protein folds at the root of an ancient metabolic network

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