An Evolutionary Path to Altered Cofactor Specificity in a Metalloenzyme

Overview

Journal Nat Commun

Specialty Biology

Date 2020 Jun 3

PMID 32483131

Citations 13

Authors

Anna Barwinska-Sendra

Yuritzi M Garcia

Kacper M Sendra

Arnaud Basle

Eilidh S Mackenzie

Emma Tarrant

Patrick Card

Leandro C Tabares

Cedric Bicep

Sun Un

Thomas E Kehl-Fie

Kevin J Waldron

Affiliations

Soon will be listed here.

Abstract

Almost half of all enzymes utilize a metal cofactor. However, the features that dictate the metal utilized by metalloenzymes are poorly understood, limiting our ability to manipulate these enzymes for industrial and health-associated applications. The ubiquitous iron/manganese superoxide dismutase (SOD) family exemplifies this deficit, as the specific metal used by any family member cannot be predicted. Biochemical, structural and paramagnetic analysis of two evolutionarily related SODs with different metal specificity produced by the pathogenic bacterium Staphylococcus aureus identifies two positions that control metal specificity. These residues make no direct contacts with the metal-coordinating ligands but control the metal's redox properties, demonstrating that subtle architectural changes can dramatically alter metal utilization. Introducing these mutations into S. aureus alters the ability of the bacterium to resist superoxide stress when metal starved by the host, revealing that small changes in metal-dependent activity can drive the evolution of metalloenzymes with new cofactor specificity.

Citing Articles

Bacterial Metallostasis: Metal Sensing, Metalloproteome Remodeling, and Metal Trafficking.

Capdevila D, Rondon J, Edmonds K, Rocchio J, Villarruel Dujovne M, Giedroc D Chem Rev. 2024; 124(24):13574-13659.

PMID: 39658019 PMC: 11672702. DOI: 10.1021/acs.chemrev.4c00264.

Rational Design of a Flavoenzyme for Aerobic Nicotine Catabolism.

Hu H, Xu Z, Zhang Z, Song P, Stull F, Xu P bioRxiv. 2024; .

PMID: 39026806 PMC: 11257531. DOI: 10.1101/2024.07.11.603087.

Unveiling the Catalytic Mechanism of a Processive Metalloaminopeptidase.

Simpson M, Harding C, Czekster R, Remmel L, Bode B, Czekster C Biochemistry. 2023; 62(22):3188-3205.

PMID: 37924287 PMC: 10666288. DOI: 10.1021/acs.biochem.3c00420.

A Review of the Current State of Magnetic Force Microscopy to Unravel the Magnetic Properties of Nanomaterials Applied in Biological Systems and Future Directions for Quantum Technologies.

Winkler R, Ciria M, Ahmad M, Plank H, Marcuello C Nanomaterials (Basel). 2023; 13(18).

PMID: 37764614 PMC: 10536909. DOI: 10.3390/nano13182585.

An ancient metalloenzyme evolves through metal preference modulation.

Sendra K, Barwinska-Sendra A, Mackenzie E, Basle A, Kehl-Fie T, Waldron K Nat Ecol Evol. 2023; 7(5):732-744.

PMID: 37037909 PMC: 10172142. DOI: 10.1038/s41559-023-02012-0.

References

Waldron K, Rutherford J, Ford D, Robinson N . Metalloproteins and metal sensing. Nature. 2009; 460(7257):823-30. DOI: 10.1038/nature08300. View

Andreini C, Bertini I, Cavallaro G, Holliday G, Thornton J . Metal ions in biological catalysis: from enzyme databases to general principles. J Biol Inorg Chem. 2008; 13(8):1205-18. DOI: 10.1007/s00775-008-0404-5. View

Anjem A, Varghese S, Imlay J . Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol Microbiol. 2009; 72(4):844-58. PMC: 2776087. DOI: 10.1111/j.1365-2958.2009.06699.x. View

Gu M, Imlay J . Superoxide poisons mononuclear iron enzymes by causing mismetallation. Mol Microbiol. 2013; 89(1):123-34. PMC: 3731988. DOI: 10.1111/mmi.12263. View

Sobota J, Gu M, Imlay J . Intracellular hydrogen peroxide and superoxide poison 3-deoxy-D-arabinoheptulosonate 7-phosphate synthase, the first committed enzyme in the aromatic biosynthetic pathway of Escherichia coli. J Bacteriol. 2014; 196(11):1980-91. PMC: 4010980. DOI: 10.1128/JB.01573-14. View

Sheng Y, Abreu I, Cabelli D, Maroney M, Miller A, Teixeira M . Superoxide dismutases and superoxide reductases. Chem Rev. 2014; 114(7):3854-918. PMC: 4317059. DOI: 10.1021/cr4005296. View

Buvelot H, Posfay-Barbe K, Linder P, Schrenzel J, Krause K . Staphylococcus aureus, phagocyte NADPH oxidase and chronic granulomatous disease. FEMS Microbiol Rev. 2016; 41(2):139-157. DOI: 10.1093/femsre/fuw042. View

Garcia Y, Barwinska-Sendra A, Tarrant E, Skaar E, Waldron K, Kehl-Fie T . A Superoxide Dismutase Capable of Functioning with Iron or Manganese Promotes the Resistance of Staphylococcus aureus to Calprotectin and Nutritional Immunity. PLoS Pathog. 2017; 13(1):e1006125. PMC: 5245786. DOI: 10.1371/journal.ppat.1006125. View

Valderas M, Gatson J, Wreyford N, Hart M . The superoxide dismutase gene sodM is unique to Staphylococcus aureus: absence of sodM in coagulase-negative staphylococci. J Bacteriol. 2002; 184(9):2465-72. PMC: 134988. DOI: 10.1128/JB.184.9.2465-2472.2002. View

10.

Gregory E . Characterization of the O2-induced manganese-containing superoxide dismutase from Bacteroides fragilis. Arch Biochem Biophys. 1985; 238(1):83-9. DOI: 10.1016/0003-9861(85)90143-2. View

11.

Yamakura F, Sugio S, Hiraoka B, Ohmori D, Yokota T . Pronounced conversion of the metal-specific activity of superoxide dismutase from Porphyromonas gingivalis by the mutation of a single amino acid (Gly155Thr) located apart from the active site. Biochemistry. 2003; 42(36):10790-9. DOI: 10.1021/bi0349625. View

12.

Meier B, Barra D, Bossa F, Calabrese L, Rotilio G . Synthesis of either Fe- or Mn-superoxide dismutase with an apparently identical protein moiety by an anaerobic bacterium dependent on the metal supplied. J Biol Chem. 1982; 257(23):13977-80. View

13.

Martin M, Byers B, Olson M, Salin M, Arceneaux J, Tolbert C . A Streptococcus mutans superoxide dismutase that is active with either manganese or iron as a cofactor. J Biol Chem. 1986; 261(20):9361-7. View

14.

Kehl-Fie T, Chitayat S, Hood M, Damo S, Restrepo N, Garcia C . Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe. 2011; 10(2):158-64. PMC: 3157011. DOI: 10.1016/j.chom.2011.07.004. View

15.

Dupont C, Butcher A, Valas R, Bourne P, Caetano-Anolles G . History of biological metal utilization inferred through phylogenomic analysis of protein structures. Proc Natl Acad Sci U S A. 2010; 107(23):10567-72. PMC: 2890839. DOI: 10.1073/pnas.0912491107. View

16.

Kirschvink J, Gaidos E, Bertani L, Beukes N, Gutzmer J, Maepa L . Paleoproterozoic snowball earth: extreme climatic and geochemical global change and its biological consequences. Proc Natl Acad Sci U S A. 2000; 97(4):1400-5. PMC: 26445. DOI: 10.1073/pnas.97.4.1400. View

17.

Ji H, Chen L, Jiang Y, Zhang H . Evolutionary formation of new protein folds is linked to metallic cofactor recruitment. Bioessays. 2009; 31(9):975-80. DOI: 10.1002/bies.200800201. View

18.

Valasatava Y, Rosato A, Furnham N, Thornton J, Andreini C . To what extent do structural changes in catalytic metal sites affect enzyme function?. J Inorg Biochem. 2017; 179:40-53. PMC: 5760197. DOI: 10.1016/j.jinorgbio.2017.11.002. View

19.

Conant G, Wolfe K . Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet. 2008; 9(12):938-50. DOI: 10.1038/nrg2482. View

20.

Gregory E, Dapper C . Isolation of iron-containing superoxide dismutase from Bacteroides fragilis: reconstitution as a Mn-containing enzyme. Arch Biochem Biophys. 1983; 220(1):293-300. DOI: 10.1016/0003-9861(83)90413-7. View