Journal article
An ancient metalloenzyme evolves through metal preference modulation
Nature ecology & evolution, Vol.7(5), pp.732-744
05/01/2023
DOI: 10.1038/s41559-023-02012-0
PMCID: PMC10172142
PMID: 37037909
Abstract
The iron/manganese superoxide dismutases constitute a family of metalloenzymes that function as scavengers of reactive oxygen species. Here the authors use phylogenetics, biochemistry and structural biology to show how differential metal preference for Fe and Mn has been modulated throughout iron/manganese superoxide dismutases evolution.
Evolution creates functional diversity of proteins, the essential building blocks of all biological systems. However, studies of natural proteins sampled across the tree of life and evaluated in a single experimental system are lacking. Almost half of enzymes require metals, and metalloproteins tend to optimally utilize the physicochemical properties of a specific metal co-factor. Life must adapt to changes in metal bioavailability, including those during the transition from anoxic to oxic Earth or pathogens' exposure to nutritional immunity. These changes can challenge the ability of metalloenzymes to maintain activity, presumptively driving their evolution. Here we studied metal-preference evolution within the natural diversity of the iron/manganese superoxide dismutase (SodFM) family of reactive oxygen species scavengers. We identified and experimentally verified residues with conserved roles in determining metal preference that, when combined with an understanding of the protein's evolutionary history, improved prediction of metal utilization across the five SodFM subfamilies defined herein. By combining phylogenetics, biochemistry and structural biology, we demonstrate that SodFM metal utilization can be evolutionarily fine tuned by sliding along a scale between perfect manganese and iron specificities. Over the history of life, SodFM metal preference has been modulated multiple independent times within different evolutionary and ecological contexts, and can be changed within short evolutionary timeframes.
Details
- Title: Subtitle
- An ancient metalloenzyme evolves through metal preference modulation
- Creators
- K. M. Sendra - Newcastle UniversityA. Barwinska-Sendra - Newcastle UniversityE. S. Mackenzie - Newcastle UniversityA. Basle - Newcastle UniversityT. E. Kehl-Fie - University of Illinois Urbana-ChampaignK. J. Waldron - Newcastle University
- Resource Type
- Journal article
- Publication Details
- Nature ecology & evolution, Vol.7(5), pp.732-744
- Publisher
- NATURE PORTFOLIO
- DOI
- 10.1038/s41559-023-02012-0
- PMID
- 37037909
- PMCID
- PMC10172142
- ISSN
- 2397-334X
- eISSN
- 2397-334X
- Number of pages
- 26
- Grant note
- MR/V032151/1 / Medical Research Council; UK Research & Innovation (UKRI); Medical Research Council UK (MRC) National Science Centre, Poland 2021/42/A/NZ1/00214 / MAESTRO grant from the National Science Centre, Poland Biotechnology and Biological Sciences Research Council; UK Research & Innovation (UKRI); Biotechnology and Biological Sciences Research Council (BBSRC) R01 AI155611 / National Institutes of Health; United States Department of Health & Human Services; National Institutes of Health (NIH) - USA Newcastle University's Faculty of Medical Sciences
- Language
- English
- Date published
- 05/01/2023
- Academic Unit
- Microbiology and Immunology
- Record Identifier
- 9984618512502771
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