Average oxidation state of carbon in proteins

Journal of the Royal Society Interface

Volumn 11, Issue 100, 2014, Pages

  Dick, Jeffrey M ^a  

^a CURTIN UNIVERSITY   (Australia)

Author keywords

Oxidation state; Protein evolution; Protein metabolism; Redox potential; Subcellular location

Indexed keywords

CARBON; CELL MEMBRANES; CYTOLOGY; METABOLISM; ORGANIC CARBON; OXIDATION; PHYSIOLOGY; REDOX REACTIONS;

OXIDATION STATE; PROTEIN EVOLUTION; PROTEIN METABOLISM; REDOX POTENTIALS; SUBCELLULAR LOCATION;

PROTEINS;

AMINO ACID; CARBON; DNA BASE; MEMBRANE PROTEIN; PROTEIN; RNA; BACTERIAL PROTEIN;

ARTICLE; CHEMICAL REACTION; CHEMICAL STRUCTURE; CODON; MICROORGANISM; MOLECULE; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; PROTEIN METABOLISM; BACTERIUM; CHEMISTRY; OXIDATION REDUCTION REACTION;

BACTERIA; BACTERIAL PROTEINS; CARBON; OXIDATION-REDUCTION;

EID: 84908172796     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2013.1095     Document Type: Article

References (88)

1. Hewitt LF. 1950 Oxidation-reduction potentials in bacteriology and biochemistry, 6th edn. Edinburgh, UK: E. and S. Livingstone Ltd.
2. Baas Becking LGM, Kaplan IR, Moore D. 1960 Limits of the natural environment in terms of pH and oxidation-reduction potentials. J. Geol. 68, 243-284. (doi:10.1086/626659)
3. Ziegler DM. 1985 Role of reversible oxidationreduction of enzyme thiols-disulfides in metabolic regulation. Annu. Rev. Biochem. 54, 305-329. (doi:10.1146/annurev.bi.54.070185.001513)
4. Bindoli A, Rigobello MP. 2013 Principles in redox signaling: From chemistry to functional significance. Antioxid. Redox Signal. 18, 1557-1593. (doi:10. 1089/ars.2012.4655)
5. Knecht E, Aguado C, Cárcel J, Esteban I, Esteve JM, Ghislat G, Moruno JF, Vidal JM, Sáez R. 2009 Intracellular protein degradation in mammalian cells: Recent developments. Cell. Mol. Life Sci. 66, 2427-2443. (doi:10.1007/s00018-009-0030-6)
6. Dawes EA, Ribbons DW. 1962 The endogenous metabolism of microorganisms. Annu. Rev. Microbiol. 16, 241-264. (doi:10.1146/annurev.mi. 16.100162.001325)
7. Amend JP, Shock EL. 2001 Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol. Rev. 25, 2175-2243. (doi:10.1016/S0168-6445(00)00062-0)
8. Sleep NH, Bird DK. 2008 Evolutionary ecology during the rise of dioxygen in the Earth's atmosphere. Phil. Trans. R. Soc. B 363, 2651-2664. (doi:10.1098/rstb.2008.0018)
9. Amend JP, Shock EL. 1998 Energetics of amino acid synthesis in hydrothermal ecosystems. Science 281, 1659-1662. (doi:10.1126/science.281. 5383.1659)
10. Dick JM, LaRowe DE, Helgeson HC. 2006 Temperature, pressure, and electrochemical constraints on protein speciation: Group additivity calculation of the standard molal thermodynamic properties of ionized unfolded proteins. Biogeosciences 3, 311-336. (doi:10.5194/bg-3-311-2006)
11. Dick JM, Shock EL. 2011 Calculation of the relative chemical stabilities of proteins as a function of temperature and redox chemistry in a hot spring. PLoS ONE 8, e22782. (doi:10.1371/journal.pone. 0022782)
12. Harms MJ, Thornton JW. 2013 Evolutionary biochemistry: Revealing the historical and physical causes of protein properties. Nat. Rev. Genet. 14, 559-571. (doi:10.1038/nrg3540)
13. Sterner R, Liebl W. 2001 Thermophilic adaptation of proteins. Crit. Rev. Biochem. Mol. Biol. 36, 39-106. (doi:10.1080/20014091074174)
14. Cornish-Bowden A, Cárdenas ML, Letelier J-C, Soto-Andrade J. 2007 Beyond reductionism: Metabolic circularity as a guiding vision for a real biology of systems. Proteomics 7, 839-845. (doi:10.1002/pmic.200600431)
15. Helgeson HC. 1991 Organic/inorganic reactions in metamorphic processes. Can. Mineral. 29, 707-739. (http://canmin.geoscienceworld.org/content/29/4.toc)
16. Masiello CA, Gallagher ME, Randerson JT, Deco RM, Chadwick OA. 2008 Evaluating two experimental approaches for measuring ecosystem carbon oxidation state and oxidative ratio. J. Geophys. Res. Biogeosci. 113, G03010. (doi:10.1029/2007JG000534)
17. Kroll JH et al. 2011 Carbon oxidation state as a metric for describing the chemistry of atmospheric organic aerosol. Nat. Chem. 3, 133-139. (doi:10. 1038/NCHEM.948)
18. R Core Team. 2013 R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. (http://www. R-project.org)
19. Dick JM. 2008 Calculation of the relative metastabilities of proteins using the CHNOSZ software package. Geochem. Trans. 9, 10. (doi:10. 1186/1467-4866-9-10)
20. Wong JT-F. 1981 Coevolution of genetic code and amino acid biosynthesis. Trends Biochem. Sci. 6, 33-36. (doi:10.1016/0968-0004(81)90013-X)
21. Woese CR, Dugre DH, Saxinger WC, Dugre SA. 1966 The molecular basis for the genetic code. Proc. Natl Acad. Sci. USA 55, 966-974. (doi:10.1073/pnas.55.4.966)
22. Kyte J, Doolittle RF. 1982 A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132. (doi:10.1016/0022-2836(82)90515-0)
23. Shock EL. 1990 Do amino acids equilibrate in hydrothermal fluids? Geochim. Cosmochim. Acta 54, 1185-1189. (doi:10.1016/0016-7037(90) 90450-Y)
24. LaRowe DE, Helgeson HC. 2006 Biomolecules in hydrothermal systems: Calculation of the standard molal thermodynamic properties of nucleic-acid bases, nucleosides, and nucleotides at elevated temperatures and pressures. Geochim. Cosmochim. Acta 70, 4680-4724. (doi:10.1016/j.gca.2006.04. 010)
25. Amend JP, LaRowe DE, McCollom TM, Shock EL. 2013 The energetics of organic synthesis inside and outside the cell. Phil. Trans. R. Soc. B 368, 20120255. (doi:10.1098/rstb.2012.0255)
26. The UniProt Consortium. 2012 Reorganizing the protein space at the universal protein resource (UniProt). Nucleic Acids Res. 40, D71-D75. (doi:10. 1093/nar/gkr981)
27. Almén M, Nordström KJV, Fredriksson R, Schiöth HB. 2009 Mapping the human membrane proteome: A majority of the human membrane proteins can be classified according to function and evolutionary origin. BMC Biol. 7, 50. (doi:10.1186/1741-7007-7-50)
28. Frank SA. 2009 The common patterns of nature. J. Evol. Biol. 22, 1563-1585. (doi:10.1111/j.1420-9101.2009.01775.x)
29. Dick JM. 2009 Calculation of the relative metastabilities of proteins in subcellular compartments of Saccharomyces cerevisiae. BMC Syst. Biol. 3, 75. (doi:10.1186/1752-0509-3-75)
30. Huh W-K, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK. 2003 Global analysis of protein localization in budding yeast. Nature 425, 686-691. (doi:10.1038/nature02026)
31. Cherry JM et al. 2012 Saccharomyces genome database: The genomics resource of budding yeast. Nucleic Acids Res. 40, D700-D705. (doi:10.1093/nar/gkr1029)
32. Ashburner M et al. 2000 Gene ontology: Tool for the unification of biology. Nat. Genet. 25, 25-29. (doi:10.1038/75556)
33. Hanson GT, Aggeler R, Oglesbee D, Cannon M, Capaldi RA, Tsien RY, Remington SJ. 2004 Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J. Biol. Chem. 279, 13 044-13 053. (doi:10.1074/jbc.M312846200)
34. Hu JJ, Dong LX, Outten CE. 2008 The redox environment in the mitochondrial intermembrane space is maintained separately from the cytosol and matrix. J. Biol. Chem. 283, 29 126-29 134. (doi:10. 1074/jbc.M803028200)
35. Schafer FQ, Buettner GR. 2001 Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 30, 1191-1212. (doi:10.1016/S0891-5849(01)00480-4)
36. Morgan B, Ezeriņa D, Amoako TNE, Riemer J, Seedorf M, Dick TP. 2013 Multiple glutathione disulfide removal pathways mediate cytosolic redox homeostasis. Nat. Chem. Biol. 9, 119-125. (doi:10. 1038/nchembio.1142)
37. Hwang C, Sinskey AJ, Lodish HF. 1992 Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257, 1496-1502. (doi:10.1126/science.1523409)
38. Birk J, Meyer M, Aller I, Hansen HG, Odermatt A, Dick TP, Meyer AJ, Appenzeller-Herzog C. 2013 Endoplasmic reticulum: Reduced and oxidized glutathione revisited. J. Cell Sci. 126, 1604-1617. (doi:10.1242/jcs.117218)
39. Lin Y-H, Chien W-S, Duan K-J. 2010 Correlations between reduction-oxidation potential profiles and growth patterns of Saccharomyces cerevisiae during very-high-gravity fermentation. Process Biochem. 45, 765-770. (doi:10.1016/j.procbio. 2010.01.018)
40. Go Y-M, Jones DP. 2008 Redox compartmentalization in eukaryotic cells. Biochim. Biophys. Acta 1780, 1271-1290. (doi:10.1016/j. bbagen.2008.01.011)
41. Queval G, Jaillard D, Zechmann B, Noctor G. 2011 Increased intracellular H2O2 availability preferentially drives glutathione accumulation in vacuoles and chloroplasts. Plant Cell Environ. 34, 21-32. (doi:10. 1111/j.1365-3040.2010.02222.x)
42. Singh A, Kaur N, Kosman DJ. 2007 The metalloreductase Fre6p in Fe-efflux from the yeast vacuole. J. Biol. Chem. 282, 28 619-28 626. (doi:10.1074/jbc.M703398200)
43. van Lith M, Tiwari S, Pediani J, Milligan G, Bulleid NJ. 2011 Real-time monitoring of redox changes in the mammalian endoplasmic reticulum. J. Cell Sci. 124, 2349-2356. (doi:10. 1242/jcs.085530)
44. Araújo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR. 2011 Protein degradation: An alternative respiratory substrate for stressed plants. Trends Plant Sci. 16, 489-498. (doi:10.1016/j.tplants.2011.05.008)
45. Pruitt KD, Tatusova T, Brown GR, Maglott DR. 2012 NCBI reference sequences (RefSeq): Current status, new features and genome annotation policy. Nucleic Acids Res. 40, D130-D135. (doi:10.1093/nar/gkr1079)
46. Vreeland RH, Straight S, Krammes J, Dougherty K, Rosenzweig WD, Kamekura M. 2002 Halosimplex carlsbadense gen. nov., sp. nov., a unique halophilic archaeon, with three 16S rRNA genes, that grows only in defined medium with glycerol and acetate or pyruvate. Extremophiles 6, 445-452. (doi:10. 1007/s00792-002-0278-3)
47. Tindall BJ, Trüper HG. 1986 Ecophysiology of the aerobic halophilic archaebacteria. Syst. Appl. Microbiol. 7, 202-212. (doi:10.1016/S0723-2020(86)80007-8)
48. Cayol J-L, Ollivier B, Patel BKC, Prensier G, Guezennec J, Garcia J-L. 1994 Isolation and characterization of Halothermothrix orenii gen. nov., sp. nov., a halophilic, thermophilic, fermentative, strictly anaerobic bacterium. Int. J. Syst. Bacteriol. 44, 534-540. (doi:10.1099/00207713-44-3-534)
49. Oren A, Weisburg WG, Kessel M, Woese CR. 1984 Halobacteroides halobius gen. nov., sp. nov., a moderately halophilic anaerobic bacterium from the bottom sediments of the Dead Sea. Syst. Appl. Microbiol. 5, 58-70. (doi:10.1016/S0723-2020 (84)80051-X)
50. Pérez-Brocal V, Gil R, Ramos S, Lamelas A, Postigo M, Michelena JM, Silva FJ, Moya A, Latorre A. 2006 A small microbial genome: The end of a long symbiotic relationship? Science 314, 312-313. (doi:10.1126/science.1130441)
51. Rogers MJ et al. 1985 Construction of the mycoplasma evolutionary tree from 5S rRNA sequence data. Proc. Natl Acad. Sci. USA 82, 1160-1164. (doi:10.1073/pnas.82.4.1160)
52. Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, Hattori M. 2006 The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314, 267. (doi:10.1126/science. 1134196)
53. McCutcheon JP, Moran NA. 2011 Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10, 13-26. (doi:10.1038/nrmicro2670)
54. Tabita FR, Satagopan S, Hanson TE, Kreel NE, Scott SS. 2008 Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships. J. Exp. Bot. 59, 1515-1524. (doi:10.1093/jxb/erm361)
55. Nisbet EG, Grassineau NV, Howe CJ, Abell PI, Regelous M, Nisbet RER. 2007 The age of Rubisco: The evolution of oxygenic photosynthesis. Geobiology 5, 311-335. (doi:10.1111/j.1472-4669. 2007.00127.x)
56. Wang XD, Tang KW, Wang Y, Smith Jr. WO. 2010 Temperature effects on growth, colony development and carbon partitioning in three Phaeocystis species. Aquat. Biol. 9, 239-249. (doi:10.3354/ab00256)
57. Gosink JJ, Herwig RP, Staley JT. 1997 Octadecabacter arcticus gen. nov., sp. nov., and O. antarcticus, sp. nov., nonpigmented, psychrophilic gas vacuolate bacteria from polar sea ice and water. Syst. Appl. Microbiol. 20, 356-365. (doi:10.1016/S0723-2020(97)80003-3)
58. Zhang GS, Jiang N, Liu XL, Dong XZ. 2008 Methanogenesis from methanol at low temperatures by a novel psychrophilic methanogen, 'Methanolobus psychrophilus' sp. nov., prevalent in Zoige wetland of the Tibetan plateau. Appl. Environ. Microbiol. 74, 6114-6120. (doi:10.1128/AEM.01146-08)
59. Franzmann PD, Springer N, Ludwig W, Demacario EC, Rohde M. 1992 A methanogenic archaeon from Ace Lake, Antarctica: Methanococcoides burtonii sp. nov. Syst. Appl. Microbiol. 15, 573-581. (doi:10. 1016/S0723-2020(11)80117-7)
60. Jordan DC. 1982 Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants. Int. J. Syst. Bacteriol. 32, 136-139. (doi:10.1099/00207713-32-1-136)
61. Hallmann R, Friedrich A, Koops H-P, Pommerening-Röser A, Rohde K, Zenneck C, Sand W. 1992 Physiological characteristics of Thiobacillus ferrooxidans and Leptospirillum ferrooxidans and physicochemical factors influence microbial metal leaching. Geomicrobiol. J. 10, 193-206. (doi:10. 1080/01490459209377920)
62. Miedema P. 1982 The effects of low temperature on Zea mays. Adv. Agron. 35, 93-128. (doi:10.1016/S0065-2113(08)60322-3)
63. Emerson D, Rentz JA, Lilburn TG, Davis RE, Aldrich H, Chan C, Moyer CL. 2007 A novel lineage of Proteobacteria involved in formation of marine Feoxidizing microbial mat communities. PLoS ONE 2, e667. (doi:10.1371/journal.pone.0000667)
64. Alazard D, Dukan S, Urios A, Verhé F, Bouabida N, Morel F, Thomas P, Garcia J-L, Ollivier B. 2003 Desulfovibrio hydrothermalis sp. nov., a novel sulfate-reducing bacterium isolated from hydrothermal vents. Int. J. Syst. Evol. Microbiol. 53, 173-178. (doi:10.1099/ijs.0.02323-0)
65. Sowers KR, Baron SF, Ferry JG. 1984 Methanosarcina acetivorans sp. nov., an acetotrophic methaneproducing bacterium isolated from marine sediments. Appl. Environ. Microbiol. 47, 971-978.
66. Hallberg KB, Lindström EB. 1994 Characterization of Thiobacillus caldus sp. nov., a moderately thermophilic acidophile. Microbiology 140, 3451-3456. (doi:10.1099/13500872-140-12-3451)
67. Doemel WN, Brock TD. 1970 The upper temperature limit of Cyanidium caldarium. Arch. Mikrobiol. 72, 326-332. (doi:10.1007/BF00409031)
68. Norris PR, Clark DA, Owen JP, Waterhouse S. 1996 Characteristics of Sulfobacillus acidophilus sp. nov. and other moderately thermophilic mineralsulphide-oxidizing bacteria. Microbiology 142, 775-783. (doi:10.1099/00221287-142-4-775)
69. Goto E, Kodama T, Minoda Y. 1977 Studies on hydrogen utilizing microorganisms. 5. Isolation and culture conditions of thermophilic hydrogen bacteria. Agric. Biol. Chem. 41, 685-690. (doi:10. 1271/bbb1961.41.685)
70. Allewalt JP, Bateson MM, Revsbech NP, Slack K, Ward DM. 2006 Effect of temperature and light on growth of and photosynthesis by Synechococcus isolates typical of those predominating in the Octopus Spring microbial mat community of Yellowstone National Park. Appl. Environ. Microbiol. 72, 544-550. (doi:10.1128/AEM.72.1. 544-550.2006)
71. Kamagata Y, Kawasaki H, Oyaizu H, Nakamura K, Mikami E, Endo G, Koga Y, Yamasato K. 1992 Characterization of three thermophilic strains of Methanothrix ('Methanosaeta') thermophila sp. nov. and rejection of Methanothrix ('Methanosaeta') thermoacetophila. Int. J. Syst. Bacteriol. 42, 463-468. (doi:10.1099/00207713-42-3-463)
72. Yamaoka T, Satoh K, Katoh S. 1978 Photosynthetic activities of a thermophilic blue-green alga. Plant Cell Physiol. 19, 943-954.
73. Shiratori H, Sasaya K, Ohiwa H, Ikeno H, Ayame S, Kataoka N, Miya A, Beppu T, Ueda K. 2009 Clostridium clariflavum sp. nov. and Clostridium caenicola sp. nov., moderately thermophilic, cellulose-/cellobiose-digesting bacteria isolated from methanogenic sludge. Int. J. Syst. Evol. Microbiol. 59, 1764-1770. (doi:10.1099/ijs.0. 003483-0)
74. Darland G, Brock TD. 1971 Bacillus acidocaldarius sp.nov., an acidophilic thermophilic spore-forming bacterium. J. Gen. Microbiol. 67, 9-15. (doi:10. 1099/00221287-67-1-9)
75. Balk M, Weijma J, Stams AJM. 2002 Thermotoga lettingae sp nov., a novel thermophilic, methanoldegrading bacterium isolated from a thermophilic anaerobic reactor. Int. J. Syst. Evol. Microbiol. 52, 1361-1368. (doi:10.1099/ijs.0.02165-0)
76. Wu DY et al. 2009 Complete genome sequence of the aerobic CO-oxidizing thermophile Thermomicrobium roseum. PLoS ONE 4, e4207. (doi:10.1371/journal.pone.0004207)
77. Beeder J, Nilsen RK, Rosnes JT, Torsvik T, Lien T. 1994 Archaeoglobus fulgidus isolated from hot North Sea oil field waters. Appl. Environ. Microbiol. 60, 1227-1231.
78. Jones WJ, Leigh JA, Mayer F, Woese CR, Wolfe RS. 1983 Methanococcus jannaschii sp. nov., an extremely thermophilic methanogen from a submarine hydrothermal vent. Arch. Microbiol. 136, 254-261. (doi:10.1007/BF00425213)
79. Zillig W, Gierl A, Schreiber G, Wunderl S, Janekovic D, Stetter KO, Klenk HP. 1983 The archaebacterium Thermofilum pendens represents a novel genus of the thermophilic, anaerobic sulfur respiring Thermoproteales. Syst. Appl. Microbiol. 4, 79-87. (doi:10.1016/S0723-2020(83)80035-6)
80. Fiala G, Stetter KO, Jannasch HW, Langworthy TA, Madon J. 1986 Staphylothermus marinus sp. nov. represents a novel genus of extremely thermophilic submarine heterotrophic archaebacteria growing up to 988C. Syst. Appl. Microbiol. 8, 106-113. (doi:10. 1016/S0723-2020(86)80157-6)
81. González JM, Masuchi Y, Robb FT, Ammerman JW, Maeder DL, Yanagibayashi M, Tamaoka J, Kato C. 1998 Pyrococcus horikoshii sp. nov., a hyperthermophilic archaeon isolated from a hydrothermal vent at the Okinawa Trough. Extremophiles 2, 123-130. (doi:10.1007/s007920050051)
82. Fiala G, Stetter KO. 1986 Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 1008C. Arch. Microbiol. 145, 56-61. (doi:10.1007/BF00413027)
83. Wicken JS. 1987 Evolution, thermodynamics, and information. New York, NY: Oxford University Press.
84. Akashi H, Gojobori T. 2002 Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc. Natl Acad. Sci. USA 99, 3695-3700. (doi:10.1073/pnas. 062526999)
85. Sella G, Hirsh AE. 2005 The application of statistical physics to evolutionary biology. Proc. Natl Acad. Sci. USA 102, 9541-9546. (doi:10.1073/pnas. 0501865102)
86. Lombardi AT, Garcia Jr. O. 2002 Biological leaching of Mn, Al, Zn, Cu and Ti in an anaerobic sewage sludge effectuated by Thiobacillus ferrooxidans and its effect on metal partitioning. Water Res. 36, 3193-3202. (doi:10.1016/S0043-1354(02) 00008-8)
87. Miller SR. 2003 Evidence for the adaptive evolution of the carbon fixation gene rbcL during diversification in temperature tolerance of a clade of hot spring cyanobacteria. Mol. Ecol. 12, 1237-1246. (doi:10.1046/j.1365-294X.2003.01831.x)
88. McDonald JH. 2010 Temperature adaptation at homologous sites in proteins from nine thermophile-mesophile species pairs. Genome Biol. Evol. 2, 267-276. (doi:10.1093/gbe/evq017)