Abstract
Methionine sulfoxide reductases, enzymes that reverse the oxidation of methionine residues, have been described in a wide range of species. The reduction of the diastereoisomers of oxidized methionine is catalyzed by two different monomeric methionine sulfoxide reductases (MsrA and MsrB) and is best understood as an evolutionary response to high levels of oxygen either in the Earth’s atmosphere or possibly in more localized environments. Phylogenetic analyses of these proteins suggest that their distribution is the outcome of a complex history including many paralogy and lateral gene transfer events.
Similar content being viewed by others
References
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Boschi-Muller S, Olry A, Antoine M, Branlant G (2005) The enzymology and biochemistry of methionine sulfoxide reductases. Biochim Biophys Acta 1703:231–238
Brock TD (ed) (1986) Thermophiles: general, molecular, and applied microbiology. John Wiley & Sons, New York
Brown JR, Douady CJ, Italia MJ, Marshall WE, Stanhope MJ (2001) Universal trees based on large combined protein sequence data sets. Nature Genetics 28:281–285
Daubin V, Gouy M, Perriere G (2002) A phylogenomic approach to bacterial phylogeny: evidence of a core of genes sharing a common history. Genome Res 12:1080–1090
Delaye L, Becerra A, Lazcano A (2005) The last common ancestor: What’s in a name? Origins Life Evol Biosph 35:537–554
Dhandayuthapani S, Blaylock MW, Bebear CM, Rasmussen WG, Baseman JB (2001) Peptide methionine sulfoxide reductase (MsrA) is a virulence determinant in Mycoplasma genitalium. J Bacteriol 183:5645–5650
El Hassouni M, Chambost JP, Expert D, van Gijsegem F, Barras F (1999) The minimal gene set member msrA, encoding peptide methionine sulfoxide reductase, is a virulence determinant of the peptide of the plant pathogen Erwinia chrysanthemi. Proc Natl Acad Sci USA 96:887–892
Ezraty B, Aussel B, Barras F (2005) Methionine sulfoxide reductases in prokaryotes. Biochim Biophys Acta 1703:221–229
Falkowski PG (2006) Tracing oxygen’s imprint on Earth’s metabolic evolution. Science 311:1724–1725
Felsenstein J (1989) PHYLIP—phylogeny inference package (version 3.2). Cladistics 5:164–166
Gladyshev VN (2002) Thioredoxin and peptide methionine sulfoxide reductase: convergence of similar structure and function in distinct structural folds. Proteins 46:149–152
Grimaud R, Ezraty B, Mitchell JK, Lafitte D, Briand C, Derrick PJ, Barras F (2001) Repair of oxidized proteins. J Biol Chem 276:48915–48920
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hansel A, Heinemann SH, Hoshi T (2005) Heterogeneity and function of mammalian MSRs: enzymes for repair, protection and regulation. Biochim Biophys Acta 1703:239–247
Harris JK, Kelley ST, Spiegelman GB, Pace NR (2003) The genetic core of the universal ancestor. Genome Res 13:407–412
Jannasch HW, Mottl MJ (1985) Geomicrobiology of deep-sea hydrothermal vents. Science 229:717–725
Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28:27–30
Kantorow M, Hawse JR, Cowell TL, Benhamed S, Pizarro GO, Redd VN, Hejtmancik JF (2004). Methionine sulfoxide reductase A is important for lens cell viability and resistance to oxidative stress. Proc Natl Acad Sci USA 101:9654–9659
Kryukov GD, Kumar RA, Koc A, Sun Z, Gladyshev VM (2002) Selenoprotein R is a zinc-containing stereo-specific methionine sulfoxide reductase. Proc Natl Acad Sci USA 99:4245–4250
Kültz D (2005) Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 67:225–257
Kumar RA, Koc A, Cerny RL, Gladyshev VN (2002) Reaction mechanism, evolutionary analysis, and the role of zinc in Drosophila methionine-R-sulfoxide reductase. J Biol Chem 277:37527–37535
Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5:150–163
Lowther WT, Weissbach H, Etienne F, Brot N, Matthews BW (2002) The mirrowed methionine sulfoxidase reductases of Neisseria gonorrhoeae pilB. Nat Struct Biol 9:348–352
Margulis L (1993) Symbiosis in cell evolution: microbial communities in the archean and proterozoiceons. Freeman, San Francisco
Moskovitz J, Berlett BS, Poston JM, Stadtman ER (1997) The yeast peptide-methionine sulfoxide reductase functions as an antioxidant in vivo. Proc Natl Acad Sci USA 94:985–9589
Murzin AG, Brenner SE, Hubbard T, Chothia C (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247:536–540
Mushegian AR, Koonin EV (1996) A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc Natl Acad Sci USA 93:10268–10273
Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798–804
Ruan H, Tang XD, Chen ML, Joiner ML, Sun G, Brot N, Weissbach H, Heinemann SH, Iverson L, Wu CF, Toshinori H (2002) High-quality life extension by the enzyme peptide methionine sulfoxide reductase. Proc Natl Acad Sci USA 99:2748–2753
Sharov VS, Schoneich C (2000) Diastereoselective protein methionine oxidation by reactive oxygen species and diastereoselective repair by methionine sulfoxide reductase. Free Radic Biol Med 29:986–994
Sharov VS, Ferrington DA, Squier TC, Schoneich C (1999) Diastereoselective reduction of protein-bound methionine sulfoxide by methionine sulfoxide reductase. FEBS Lett 455:247–250
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Wiedenheft B, Mosolf J, Willits D, Yeager M, Dryden KA, Young M, Douglas T (2005) An archaeal antioxidant: characterization of a Dps-like protein from Sulfolobus solfataricus. Proc Natl Acad Sci USA 102:10551–10556
Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4580
Yang S, Doolittle RF, Bourke PE (2005) Phylogeny determined by protein domain content. Proc Natl Acad Sci USA 102:373–378
Acknowledgments
We are indebted to Professor Russell Doolittle for his critical reading of the manuscript and to Drs. David DesMarais and David E. Graham for several useful exchanges and for providing us with important references.
Author information
Authors and Affiliations
Corresponding author
Additional information
[Reviewing Editor: Dr. Martin Kreitman]
Electronic Supplementary Material
Rights and permissions
About this article
Cite this article
Delaye, L., Becerra, A., Orgel, L. et al. Molecular Evolution of Peptide Methionine Sulfoxide Reductases (MsrA and MsrB): On the Early Development of a Mechanism That Protects Against Oxidative Damage. J Mol Evol 64, 15–32 (2007). https://doi.org/10.1007/s00239-005-0281-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-005-0281-2