Restricted access
Variation among species in proteomic sulphur content is related to environmental conditions
Published:14 February 2006https://doi.org/10.1098/rspb.2005.3441
Abstract
The elemental composition of proteins influences the quantities of different elements required by organisms. Here, we considered variation in the sulphur content of whole proteomes among 19 Archaea, 122 Eubacteria and 10 eukaryotes whose genomes have been fully sequenced. We found that different species vary greatly in the sulphur content of their proteins, and that average sulphur content of proteomes and genome base composition are related. Forces contributing to variation in proteomic sulphur content appear to operate quite uniformly across the proteins of different species. In particular, the sulphur content of orthologous proteins was frequently correlated with mean proteomic sulphur contents. Among prokaryotes, proteomic sulphur content tended to be greater in anaerobes, relative to non-anaerobes. Thermophiles tended to have lower proteomic sulphur content than non-thermophiles, consistent with the thermolability of cysteine and methionine residues. This work suggests that persistent environmental growth conditions can influence the evolution of elemental composition of whole proteomes in a manner that may have important implications for the amount of sulphur used by living organisms to build proteins. It extends previous studies that demonstrated links between transient changes in environmental conditions and the elemental composition of subsets of proteins expressed under these conditions.
Footnotes
References
-
Akashi H& Gojobori T . 2002 Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilus. Proc. Natl Acad. Sci. USA. 99, 3695–3700.doi:10.1073/pnas.062526999. . Crossref, PubMed, Web of Science, Google Scholar -
Barton L.L& Tomei F.A Characteristics and activities of sulfate-reducing bacteria. Sulfate-reducing bacteriavol. 8& Barton L.L . 1995pp. 1–32. Eds. New York, NY:Plenum Press. Google Scholar -
Baudouin-Cornu P, Surdin-Kerjan Y, Marlière P& Thomas D . 2001 Molecular evolution of protein atomic composition. Science. 293, 297–300.doi:10.1126/science.1061052. . Crossref, PubMed, Web of Science, Google Scholar -
Baudouin-Cornu P, Schuerer K, Marlière P& Thomas D . 2004 Intimate evolution of proteins: proteome atomic content correlates with genome base composition. J. Biol. Chem. 279, 5421–5428.doi:10.1074/jbc.M306415200. . Crossref, PubMed, Web of Science, Google Scholar -
Beeby M, O'Connor B.D, Ryttersgaard C, Boutz D.R, Perry L.J& Yeates T.O . 2005 The genomics of disulfide bonding and protein stabilization in thermophiles. PLoS Biol. 3, e309 doi:10.1371/journal.pbio.0030309. . Crossref, PubMed, Web of Science, Google Scholar -
Berlett B.S& Stadtman E.R . 1997 Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272, 20 313–20 316.doi:10.1074/jbc.272.33.20313. . Crossref, Web of Science, Google Scholar -
Bragg J.G& Hyder C.L . 2004 Nitrogen versus carbon use in prokaryotic genomes and proteomes. Proc. R. Soc. B. 271, Suppl. 5, S374–S377.doi:10.1098/rsbl.2004.0193. . Link, Web of Science, Google Scholar -
Creevey C.J, Fitzpatrick D.A, Philip G.K, Kinsella R.J, O'Connell M.J, Pentony M.M, Travers S.A, Wilkinson M& McInerney J.O . 2004 Does a tree-like phylogeny only exist at the tips in the prokaryotes?. Proc. R. Soc. B. 271, 2551–2558.doi:10.1098/rspb.2004.2864. . Link, Web of Science, Google Scholar -
Fauchon M, 2002 Sulfur sparing in the yeast proteome in response to sulfur demand. Mol. Cell. 9, 713–723.doi:10.1016/S1097-2765(02)00500-2. . Crossref, PubMed, Web of Science, Google Scholar -
Felsenstein J . 1985 Phylogenies and the comparative method. Am. Nat. 125, 1–15.doi:10.1086/284325. . Crossref, Web of Science, Google Scholar -
Ghaemmaghami S, Huh W.-K, Bower K, Howson R.W, Belle A, Dephoure N, O'Shea E.K& Weissman J.S . 2003 Global analysis of protein expression in yeast. Nature. 425, 737–741.doi:10.1038/nature02046. . Crossref, PubMed, Web of Science, Google Scholar -
Harvey P.H& Pagel M.D The comparative method in evolutionary biology. 1991 Oxford, UK:Oxford University Press. Google Scholar -
Heidelberg J.F, 2004 The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat. Biotechnol. 22, 554–559.doi:10.1038/nbt959. . Crossref, PubMed, Web of Science, Google Scholar -
Hickey D.A& Singer G.A.C . 2004 Genomic and proteomic adaptations to growth at high temperature. Genome Biol. 5, 1171–1177.doi:10.1186/gb-2004-5-10-117. . Crossref, Web of Science, Google Scholar -
Holt J.G Bergey's manual of systematic bacteriology vol. 1 1984 Baltimore, MD:Williams & Wilkins. Google Scholar -
Holt J.G Bergey's manual of systematic bacteriology vol. 2 1986 Baltimore, MD:Williams & Wilkins. Google Scholar -
Holt J.G Bergey's manual of systematic bacteriology vol. 4 1989a Baltimore, MD:Williams & Wilkins. Google Scholar -
Holt J.G Bergey's manual of systematic bacteriology vol. 3 1989b Baltimore, MD:Williams & Wilkins. Google Scholar -
Karlin S& Brendel V . 1992 Chance and statistical significance in protein and DNA sequence analysis. Science. 257, 39–49. Crossref, PubMed, Web of Science, Google Scholar -
Klenk H.P, 1997 The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature. 390, 364–370.doi:10.1038/37052. . Crossref, PubMed, Web of Science, Google Scholar -
Lambros R.J, Mortimer J.R& Forsdyke D.R . 2003 Optimum growth temperature and the base composition of open reading frames in prokaryotes. Extremophiles. 7, 443–450.doi:10.1007/s00792-003-0353-4. . Crossref, PubMed, Web of Science, Google Scholar -
Major T.A, Burd H& Whitman W.B . 2004 Abundance of 4Fe-4S motifs in the genomes of methanogens and other prokaryotes. FEMS Microbiol. Lett. 239, 117–123.doi:10.1016/j.femsle.2004.08.027. . Crossref, PubMed, Web of Science, Google Scholar -
Mazel D& Marlière P . 1989 Adaptive eradication of methionine and cysteine from cyanobacterial light-harvesting proteins. Nature. 341, 245–248.doi:10.1038/341245a0. . Crossref, PubMed, Web of Science, Google Scholar -
McEwan C, Gatherer D& McEwan N . 1998 Nitrogen-fixing aerobic bacteria have higher genomic GC content than non-fixing species within the same genus. Hereditas. 128, 173–178.doi:10.1111/j.1601-5223.1998.00173.x. . Crossref, PubMed, Web of Science, Google Scholar -
Meinnel T, Mechulam Y& Blanquet S . 1993 Methionine as translation start signal: a review of the enzymes of the pathway in Escherichia coli. Biochimie. 75, 1061–1075.doi:10.1016/0300-9084(93)90005-D. . Crossref, PubMed, Web of Science, Google Scholar -
Naya H, Romero H, Zavala A, Alvarez B& Musto H . 2002 Aerobiosis increases the genomic guanine plus cytosine content (GC%) in prokaryotes. J. Mol. Evol. 55, 260–264.doi:10.1007/s00239-002-2323-3. . Crossref, PubMed, Web of Science, Google Scholar -
Rabus R, 2004 The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments. Environ. Microbiol. 6, 887–902.doi:10.1111/j.1462-2920.2004.00665.x. . Crossref, PubMed, Web of Science, Google Scholar -
Russell R.J.M, Ferguson J.M.C, Hough D.W, Danson M.J& Taylor G.L . 1997 The crystal structure of citrate synthase from the hyperthermophilic Archaeon Pyrococcus furiosus at 1.9 angstrom resolution. Biochemistry. 36, 9983–9994.doi:10.1021/bi9705321. . Crossref, PubMed, Web of Science, Google Scholar -
Schultes E, Hraber P.T& LaBean T.H . 1997 Global similarities in nucleotide base composition among disparate functional classes of single-stranded RNA imply adaptive evolutionary convergence. RNA. 3, 792–806. PubMed, Web of Science, Google Scholar -
Singer G.A.C& Hickey D.A . 2003 Thermophilic prokaryotes have characteristic patterns of codon usage, amino acid composition and nucleotide content. Gene. 317, 39–47.doi:10.1016/S0378-1119(03)00660-7. . Crossref, PubMed, Web of Science, Google Scholar -
Sterner R.W& Elser J.J Ecological stoichiometry. 2002 Princeton, NJ:Princeton University Press. Google Scholar -
Tatusov R.L, Koonin E.V& Lipman D.J . 1997 A genomic perspective on protein families. Science. 278, 631–637.doi:10.1126/science.278.5338.631. . Crossref, PubMed, Web of Science, Google Scholar -
Tekaia F, Yeramian E& Dujon B . 2002 Amino acid composition of genomes, lifestyles of organisms, and evolutionary trends: a global picture with correspondence analysis. Gene. 297, 51–60.doi:10.1016/S0378-1119(02)00871-5. . Crossref, PubMed, Web of Science, Google Scholar
