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Quantifying structural relationships of metal-binding sites suggests origins of biological electron transfer.

ABSTRACT: Biological redox reactions drive planetary biogeochemical cycles. Using a novel, structure-guided sequence analysis of proteins, we explored the patterns of evolution of enzymes responsible for these reactions. Our analysis reveals that the folds that bind transition metal–containing ligands have similar structural geometry and amino acid sequences across the full diversity of proteins. Similarity across folds reflects the availability of key transition metals over geological time and strongly suggests that transition metal–ligand binding had a small number of common peptide origins. We observe that structures central to our similarity network come primarily from oxidoreductases, suggesting that ancestral peptides may have also facilitated electron transfer reactions. Last, our results reveal that the earliest biologically functional peptides were likely available before the assembly of fully functional protein domains over 3.8 billion years ago.Thus, life is a special, very complex form of motion of matter, but this form did not always exist, and it is not separated from inorganic nature by an impassable abyss; rather, it arose from inorganic nature as a new property in the process of evolution of the world. We must study the history of this evolution if we want to solve the problem of the origin of life. [A. I. Oparin (1)]

SUBMITTER: Bromberg Y

PROVIDER: S-EPMC8759750 | biostudies-literature | 2022 Jan

REPOSITORIES: biostudies-literature

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Quantifying structural relationships of metal-binding sites suggests origins of biological electron transfer.

Bromberg Yana Y Aptekmann Ariel A AA Mahlich Yannick Y Cook Linda L Senn Stefan S Miller Maximillian M Nanda Vikas V Ferreiro Diego U DU Falkowski Paul G PG

Science advances 20220114 2

Biological redox reactions drive planetary biogeochemical cycles. Using a novel, structure-guided sequence analysis of proteins, we explored the patterns of evolution of enzymes responsible for these reactions. Our analysis reveals that the folds that bind transition metal–containing ligands have similar structural geometry and amino acid sequences across the full diversity of proteins. Similarity across folds reflects the availability of key transition metals over geological time and strongly s ...[more]

PMID: 35030025

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Project description:A novel ArsR-SmtB family transcriptional repressor, KmtR, has been characterised from mycobacteria. Mutants of M. tuberculosis lacking kmtR show elevated expression of Rv2025c encoding a deduced CDF-family metal-exporter. KmtR-dependent repression of the cdf and kmtR operator-promoters was alleviated by nickel and cobalt in minimal medium. Electrophoretic mobility shift assays (EMSA) and fluorescence anisotropy (FA) show binding of purified KmtR to nucleotide sequences containing a region of dyad symmetry from the cdf and kmtR operator-promoters. A relatively large deltar(obs) in FA implies formation of high order apo-KmtR(n)-DNA and multiple complexes were detected by EMSA. Incubation of KmtR with cobalt inhibits DNA-complex assembly and metal-protein binding was confirmed by competition against 4-(2-pyridylazo)-resorcinol. KmtR is the second, to NmtR, characterised ArsR-SmtB sensor of nickel and cobalt from M. tuberculosis suggesting special significance for these ions in this pathogen. KmtR-dependent expression is elevated in complete medium with no increase in response to metals, while NmtR retains a response to nickel and cobalt under these conditions. Mixing equimolar apo-KmtR and apo-NmtR with 0.8 equivalents of nickel or cobalt gave nickel- and cobalt-dependent difference emission spectra similar to nickel(0.8)-KmtR and cobalt(0.8)-KmtR, respectively. Thus, KmtR has tighter affinities for nickel and cobalt than NmtR consistent with basal levels of these metals being sensed by KmtR but not NmtR in complete medium. More than a thousand genes encoding ArsR-SmtB related proteins are listed in databases and a proportion can be predicted to detect metals through known allosteric sites. KmtR has none of the previously defined sites. Substitution of His(88), Glu(101), His(102), His(110) or His(111) with Gln generated KmtR-variants that repress the cdf and kmtR operator-promoters even in elevated nickel and cobalt, revealing a new sensory site. Importantly, ArsR-SmtB sequence groupings do not correspond with the different sensory-motifs revealing that only the latter should be used to predict metal-sensing. Data is also available from http://bugs.sgul.ac.uk/E-BUGS-49

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Quantifying structural relationships of metal-binding sites suggests origins of biological electron transfer.

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Quantifying structural relationships of metal-binding sites suggests origins of biological electron transfer.

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