SORGOdb: Superoxide Reductase Gene Ontology curated DataBase
© Lucchetti-Miganeh et al; licensee BioMed Central Ltd. 2011
Received: 15 December 2010
Accepted: 16 May 2011
Published: 16 May 2011
Superoxide reductases (SOR) catalyse the reduction of superoxide anions to hydrogen peroxide and are involved in the oxidative stress defences of anaerobic and facultative anaerobic organisms. Genes encoding SOR were discovered recently and suffer from annotation problems. These genes, named sor, are short and the transfer of annotations from previously characterized neelaredoxin, desulfoferrodoxin, superoxide reductase and rubredoxin oxidase has been heterogeneous. Consequently, many sor remain anonymous or mis-annotated.
SORGOdb is an exhaustive database of SOR that proposes a new classification based on domain architecture. SORGOdb supplies a simple user-friendly web-based database for retrieving and exploring relevant information about the proposed SOR families. The database can be queried using an organism name, a locus tag or phylogenetic criteria, and also offers sequence similarity searches using BlastP. Genes encoding SOR have been re-annotated in all available genome sequences (prokaryotic and eukaryotic (complete and in draft) genomes, updated in May 2010).
SORGOdb contains 325 non-redundant and curated SOR, from 274 organisms. It proposes a new classification of SOR into seven different classes and allows biologists to explore and analyze sor in order to establish correlations between the class of SOR and organism phenotypes. SORGOdb is freely available at http://sorgo.genouest.org/index.php.
Two and a half billion years ago, the intense photosynthetic activity of cyanobacteria caused the largest environmental change in Earth's history: the oxygenation of the atmosphere and the oceans, which were hitherto largely anoxic [1, 2]. This profound transformation of the biosphere exerted an evolutionary selection pressure on organisms and led to the development of new pathways, including the highly exergonic respiratory chain based on O2 as the terminal electron acceptor. Currently, most living organisms, except anaerobic microbes, require oxygen. O2 is used as a substrate by many enzymes involved metabolizing amines, purines and amino acids. Oxygen is a relatively inert molecule due to its spin triplet ground state. However, it can be activated by photons or by one electron oxidation or reduction processes to generate reactive oxygen species (called reactive oxygen species or ROS), particularly hydroxyl radicals (•OH), hydrogen peroxide (H2O2) and superoxide anion radicals (O2-).
The superoxide anion is generated fortuitously by flavoenzymes such as NADH dehydrogenase II, succinate dehydrogenase, fumarate reductase, and sulphite reductase [3, 4]. The superoxide anion is one of the deleterious reactive oxygen species: it can damage DNA, proteins and lipids indirectly by releasing iron from damaged dehydratase clusters [4, 5]. In anaerobes, most of the essential "central metabolic" redox enzymes (for example aconitase, fumarase, dihydroxyacid dehydratase, and pyruvate:ferredoxin oxidoreductase) contain iron sulphur [Fe-S] clusters that are rapidly inactivated when exposed to oxygen [5–8].
To survive and protect themselves from the toxicity of superoxide anion, many species, and especially anaerobes, have developed defence mechanisms .
Superoxide dismutase (SOD) was first isolated by Mann and Keilis (1938) and its catalytic function, which consists to dismutate O2- into molecular oxygen and hydrogen peroxide, was discovered in 1969 by McCord and Fridovich . Mammals have two forms of SOD isozymes: the manganese SOD (Mn-SOD), present in the mitochondria, and the copper/zinc SOD (Cu/Zn-SO), present in the cytoplasm [10, 11]. In plants, SOD have been classified into three distinct types on the basis of their metal cofactor: Cu/Zn-SOD (in the cytosol and chloroplasts), Mn-SOD (in mitochondria), and Fe-SOD (often in chloroplasts) [12–14]. There are three known SOD in E. coli: MnSOD, FeSOD and CuZnSOD. The two first are located in the cytoplasm and the last in the periplasmic space . A distinct additional fourth class of SOD containing nickel (NiSOD) was recently discovered in Streptomyces [16, 17] and cyanobacteria . SOD-driven dismutation was the only biological mechanism identified for scavenging superoxide anion radicals until the early 1990's. McCord et al.  established a correlation between oxygen tolerance and SOD production and suggested that SOD was the single most important enzyme for enabling organisms to survive in the presence of molecular oxygen. They proposed that the hypersensitivity of obligate anaerobes to oxygen was a consequence of SOD deficiency. However, most anaerobic organisms, which indeed lack SOD, show various degrees of tolerance to oxygen when they are occasionally exposed to this molecule in their environments.
Two novel iron-sulphur-containing proteins that detoxify superoxide molecules were then discovered in sulphate-reducing and hyperthermophilic anaerobes: desulfoferrodoxin (Dfx) in Desulfovibrio desulfuricans, Desulfovibrio vulgaris Hildenbourgh  and Desulfoarculus baarsii , neelaredoxin (Nlr) in Desulfovibrio gigas  and superoxide reductase (SOR) in Pyrococcus furiosus . This revealed the existence of alternative mechanisms for ROS detoxification in anaerobes. The function of these proteins was first studied in 1996 by Dfx complementation of superoxide detoxication activity in E. coli SOD mutants . Later, Nlr from Treponema pallidum  and D. gigas  were also shown to complement such SOD mutants. Liochev and Fridovich  suggested that Dfx catalyzes the reduction of superoxide rather than its dismutation, and that it uses cellular reductants such as NAD(P)H. Subsequently, the Dfx enzyme was confirmed as an oxidoreductase [23–25, 27]. Finally, the superoxide reductase activity of those proteins were established by two groups [21, 23].
Dfx and Nlr proteins have different numbers of iron sites: both contain a similar C-terminal single iron-containing site (centre II) but also has Dfx a second N-terminal site (centre I) [22, 28]. Centre II is the active site of SOR and consists of a pentacoordinated Fe2+ centre with four equatorial histidines and one axial cysteine in a square pyramidal geometry (Fe(His)4(Cys) [29–31]). The binding site for the substrate O2- is the free sixth axial site of the reduced enzyme centre . The additional N-terminal domain of the 2Fe-SOR contains a rubredoxin-like centre, with Fe3+ ligated by four cysteines in a distorted tetrahedral geometry (centre I, Fe(Cys)4, ). A first classification of these enzymes was proposed according to the number of metal centres: neelaredoxin or 1Fe-SOR and desulfoferrodoxin or 2Fe-SOR [33, 34]. An additional class was proposed after the isolation of a Treponema pallidum SOR that contains an extended non-iron N-terminal domain of unknown function [25, 35]. In all these three classes, only the reduced form of the iron-containing active centre II is able to react with the superoxide anion O2•-.
SOD are found in nearly every living organism except in some strictly anaerobic species [36, 37]. Tally et al suggested that the diversity in the oxygen tolerance of anaerobes is generally related to their level of SOD . SOR were first thought to be restricted to anaerobic prokaryotes but were subsequently discovered in some micro-aerophilic and micro-aerotolerant Bacteria and Archaea [39, 40]. More recently, a SOR encoding gene was also discovered in an eukaryote, Giardia intestinalis, a microaerophilic protozoan (cited by ). Although SOD and SOR both detoxify superoxide, there is a fundamental difference in their properties: SOD generate one-half mole of oxygen and one-half mole of hydrogen peroxide per superoxide molecule whereas SOR produce only one mole of hydrogen peroxide. The physiological conditions, that determine SOR or SOD preference in organisms, have not be completely determined, although the presence of SOR rather than SOD may be associated with the amount of redox proteins produced by organisms .
Most genomes, even those of anaerobic species, contain both SOD and SOR although some species have only one of the two enzymes. The increasing number of sequenced genomes makes allows comparative genomic analyses, to elucidate the evolutionary or functional processes of SOR. Unfortunately, there are several problems with the annotation of superoxide reductase genes, partly a consequence of heterogeneous transfer of annotations from previously characterized neelaredoxin, desulfoferrodoxin, superoxide reductase or rubredoxin oxidase. Moreover, due to the absence of updating or correction of databases, many sor genes remained anonymous because of the transfer of annotations from SOR genes initially annotated as "hypothetical", "function unknown" or "putative activity". Also, SOR are small proteins, ca. 200 amino acids on average, and mis-annotations are frequent for proteins of this length .
For all these reasons, we developed SORGOdb, the first resource specifically dedicated to superoxide reductase genes in entirely sequenced and in-draft genomes. SOR sequences were curated manually, analysed and stored using a new ontology in a publically available resource (http://sorgo.genouest.org/). SOR genes were detected in the three kingdoms of life, and only on chromosomal replicons. Although no N-terminal signal sequences were previously described for bacteria SOR , we predicted seven SOR to be potentially TAT-secreted (Twin-arginine translocation) in some bacteria, including for example in Desulfovibrio salexigens DSM 2638, Desulfuromonas acetoxidans DSM 684 and Geobacter uraniireducens Rf4. Our analysis confirms the observations by Pinto et al in 2010 that (1) the repartition of SOR classes does not correlate with organism phylogeny and that (2) sor genes occur in very diverse genetic environments. Indeed, although some sor are clustered with genes encoding electron donors (such as rubredoxin in D. vulgaris) or inter-related oxidative responsive genes, most are close to functionally unrelated genes. This is consistent with sor genes being acquired, or lost, through lateral gene transfer .
Construction and content
Collection of SOR
SOR proteins with entrie(s) in Pubmed and/or PDB structure
Desulfovibrio desulfuricans ssp. desulfuricans. ATCC 27774
Desulfovibrio Desulfuricans ssp. desulfuricans G20
2JI1, 1VZI, 1VZG, 1VZH
Pyrococcus horikoshii Ot3
Pyrococcus furiosus DSM 3638
1DQI, 1DO6, 1DQK
Treponema pallidum ssp. pallidum str. Nichols
Archaeoglobus fulgidus DSM 4304
Desulfovibrio vulgaris 'Miyazaki F
Desulfovibrio vulgaris sp. vulgaris str. Hildenborough
Clostridium acetobutylicum ATCC 824
Nanoarchaeum equitans Kin4-M
At the end of this integrative research, we had a collection of 325 non-redundant and curated predicted SOR in 274 organisms, covering all the three kingdoms: Bacteria (270 genes), Archaea (52 genes) and Eukaryota (3 genes).
New Classification and ontology
Classes of SOR in SORGOdb (Number of proteins per classes)
SOR in SORGOdb
SORGOdb website construction
SORGOdb Web interface
The navigation menu (on the left) provides access to SORGOdb functions through three modules. (i) Browse: browse SOR proteins according to phylogeny criteria (kingdom, phylum, class and order) or locus tag name. (ii) Search: by organism name query and by sequence similarity through a BlastP form that allows users to enter primary sequences to find similar entries into the SORGOdb database and (iii) Pre-computed Results that include data statistics (organized in three tabs), classes (details about SORGOdb classes and ontology) and useful links (reference, tools and websites). Statistical results about SORGOdb classification were presented in the Classification tab (http://sorgo.genouest.org/classif-Stat.php).
The results panel (on the right) provides intermediary selection options and displays SOR record information in a tabular way including organism name, locus tag name, SORGOdb classification and domains architecture. When available, SORGOdb includes a CGView  representation of the distribution of SOR and all SOD genes (MnSOD, FeSOD CuZnSOD and NiSOD)  in the replicons and a gView  map to illustrate the genetic organisation and encoded functions surrounding each SOR (window of 11 genes max.).
SORGOdb synopsis and download
Utility and Dicussion
As an example, SORGOdb allows the study of the distribution of genes encoding superoxide reductase across a whole phylum. As a case study, we decided to consider the Archaea as these organisms are considered to be originate from a hyperthermophilic anaerobic common ancestor and were probably already prevalent when the Earth had its primative anoxic H2 and CO2 atmosphere.
Nanoarchaeota  and Korarchaeota  are obligately anaerobic sulphur-dependent organisms placed close to the root of the archaeal SSU rRNA tree. Nanoarchaeota is currently known from a single organism Candidatus Nanoarchaeum equitans, a hyperthermophilic symbiont that grows on the surface of Ignicoccus hospitalis [62, 63]. There are currently no representatives of Korarchaeota in pure culture but the genome of K. cryptophilum, a very thin filamentous thermophilic heterotroph, has been determined from a sample of Yellowstone National Park Obsidian Pool. Both C. N. equitans and K. cryptophilum are found together in the 16S tree, in the vicinity of the Crenarchaeota group, and contain genes encoding superoxide reductase with a SOR (centre II) functional domain and do not encode superoxide dismutase genes.
Thermococcus and Pyrococcus are obligate anaerobes that live in environments where there is no oxygen and both produce a SOR-type superoxide reductase that is catalytically active at temperatures below the optimum growth temperature but representing conditions likely corresponding to zones of oxygen exposure .
The protein tree also revealed two interesting phenomena: Msp_0788 that is a non-canonical Dx-SOR (as the Dx active site is incomplete) that is branched as an out-group close to the entire archaeal Dx-SOR group (Figure 5, point 1). This is consistent with the presumed loss-of-function of Dx of Msp_0788 being relatively recent. Also, the Kcr_1172 locus forms a major divergent branch (Figure 5, point 2).). Using the "Browse by locus tag" option, Kcr_1172 is revealed to be a fusion protein with an additional C-terminal module sharing significantly similarities with archaeal proteins annotated as "hypothetical" or "redoxin domain-containing". The best-conserved component is a CXXC motif (i.e. cysteines separated by two amino acids), found in many redox proteins for the formation, the isomerization and the reduction of disulphide bonds and for other redox functions . Kcr_1172 has a new SOR-derived architecture with the presence of two CXXC active sites (in the C-terminal fusion and N-terminal "Dx parts"), separated by the functional SOR centre II. This arrangement is unique and interesting as a combination of two sites CXXC motifs has been shown to be involved in protein disulphide-shuffling in hyperthermophiles . Although the true function of this protein needs to be determined experimentally, we show with this example that SORGOdb can also be used to reveal possible new SOR features.
The distribution of genes encoding SOR and SOD is extremely heterogeneous, both qualitatively and quantitatively, in the group of methanogenic archaea as shown in Figure 3. Thus, for the genus Methanosarcina, Methanosarcina acetivorans (5.8 Mb) possesses one SOR and two SOD whereas Methanosarcina mazei (4.1 Mb) encodes only one SOR. M. barkeri, that shares 80% identity with both M. acetivorans and M. mazei , encodes two SOD  but no SOR. The presence of these various combinations of oxygen-dependent SOD and SOR genes confirm that methanogens, that are sensitive to oxygen and are rapidly killed by even very low concentrations of O2, protect themselves from ROS; however, the factors that influence the presence and evolution of these genes remain unidentified. No clear relationship can be established between oxygen tolerance and the existence of superoxide reductase functions in the genome of microbes. A difficulty is the different connotations of the term 'anoxia' as used by geologists, zoologists and microbiologists. Geologists call an environment 'aerobic' if the oxygen content exceeds 18%. Zoologists talk about 'hypoxic' conditions when referring to oxygen levels that limit respiration (usually less than ca. 50% O2). For microbiologists, the so-called 'Pasteur point' of switch from aerobic respiration to fermentation is generally less than about 1 per cent of the atmospheric levels of oxygen; microbes, though, are affected by very low levels of oxygen, often much less than 0.1 per cent whereas some "anaerobes" living today are able to tolerate oxygen even at higher levels.
The SORGOdb server is the first web server that centralizes and provides an interface for information concerning superoxide reductase proteins. SORGOdb provides integrated features: (1) Multiple options for data browsing and searching (2) Complete descriptions of SOR and a new domain-based classification (3) Synthetic and downloadable synopsis for each locus tag (4) A SOR-homology analysis tool using BlastP similarity searches with the SORGOdb-positive dataset (5) An integrated access to external hyperlinks to various public data sources (notably NCBI GenBank, and Pubmed). SORGOdb is a unique mining tool that can assist researchers with diverse interests to retrieve, visualize and analyse superoxide reductase genes and proteins.
Availability and requirements
Database name: SORGOdb
Project home page: http://sorgo.genouest.org/index.php
Operating system(s): Platform independent, designed for Safari and Firefox browser and not available for Internet Explorer.
List of abbreviations used
Reactive Oxygen Species
CLM is supported by Agence Nationale de la Recherche and DG by the Ministère de la Recherche. We wish to thank the bioinformatics platform of Biogenouest of Rennes for providing the hosting infrastructure.
- Holland HD: The oxygenation of the atmosphere and oceans. Philos Trans R Soc Lond B Biol Sci. 2006, 361 (1470): 903-915. 10.1098/rstb.2006.1838.PubMedPubMed CentralView ArticleGoogle Scholar
- Kasting JF: Earth's early atmosphere. Science. 1993, 259 (5097): 920-926. 10.1126/science.11536547.PubMedView ArticleGoogle Scholar
- Massey V, Strickland S, Mayhew SG, Howell LG, Engel PC, Matthews RG, Schuman M, Sullivan PA: The production of superoxide anion radicals in the reaction of reduced flavins and flavoproteins with molecular oxygen. Biochem Biophys Res Commun. 1969, 36 (6): 891-897. 10.1016/0006-291X(69)90287-3.PubMedView ArticleGoogle Scholar
- Imlay JA: Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem. 2008, 77: 755-776. 10.1146/annurev.biochem.77.061606.161055.PubMedPubMed CentralView ArticleGoogle Scholar
- Imlay JA: Pathways of oxidative damage. Annu Rev Microbiol. 2003, 57: 395-418. 10.1146/annurev.micro.57.030502.090938.PubMedView ArticleGoogle Scholar
- Kuo CF, Mashino T, Fridovich I: alpha, beta-Dihydroxyisovalerate dehydratase. A superoxide-sensitive enzyme. J Biol Chem. 1987, 262 (10): 4724-4727.PubMedGoogle Scholar
- Flint DH, Tuminello JF, Emptage MH: The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J Biol Chem. 1993, 268 (30): 22369-22376.PubMedGoogle Scholar
- Adams MW, Holden JF, Menon AL, Schut GJ, Grunden AM, Hou C, Hutchins AM, Jenney FE, Kim C, Ma K, et al: Key role for sulfur in peptide metabolism and in regulation of three hydrogenases in the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol. 2001, 183 (2): 716-724. 10.1128/JB.183.2.716-724.2001.PubMedPubMed CentralView ArticleGoogle Scholar
- McCord JM, Fridovich I: Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969, 244 (22): 6049-6055.PubMedGoogle Scholar
- Sturtz LA, Diekert K, Jensen LT, Lill R, Culotta VC: A fraction of yeast Cu,Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria. A physiological role for SOD1 in guarding against mitochondrial oxidative damage. J Biol Chem. 2001, 276 (41): 38084-38089.PubMedGoogle Scholar
- Landis GN, Tower J: Superoxide dismutase evolution and life span regulation. Mech Ageing Dev. 2005, 126 (3): 365-379. 10.1016/j.mad.2004.08.012.PubMedView ArticleGoogle Scholar
- Abreu IA, Cabelli DE: Superoxide dismutases-a review of the metal-associated mechanistic variations. Biochim Biophys Acta. 2010, 1804 (2): 263-274.PubMedView ArticleGoogle Scholar
- Pilon M, Ravet K, Tapken W: The biogenesis and physiological function of chloroplast superoxide dismutases. Biochim Biophys Acta. 2010Google Scholar
- Myouga F, Hosoda C, Umezawa T, Iizumi H, Kuromori T, Motohashi R, Shono Y, Nagata N, Ikeuchi M, Shinozaki K: A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell. 2008, 20 (11): 3148-3162. 10.1105/tpc.108.061341.PubMedPubMed CentralView ArticleGoogle Scholar
- Hassan HM: Microbial superoxide dismutases. Adv Genet. 1989, 26: 65-97.PubMedView ArticleGoogle Scholar
- Youn HD, Kim EJ, Roe JH, Hah YC, Kang SO: A novel nickel-containing superoxide dismutase from Streptomyces spp. Biochem J. 1996, 318 (Pt 3): 889-896.PubMedPubMed CentralView ArticleGoogle Scholar
- Youn HD, Youn H, Lee JW, Yim YI, Lee JK, Hah YC, Kang SO: Unique isozymes of superoxide dismutase in Streptomyces griseus. Arch Biochem Biophys. 1996, 334 (2): 341-348. 10.1006/abbi.1996.0463.PubMedView ArticleGoogle Scholar
- Palenik B, Brahamsha B, Larimer FW, Land M, Hauser L, Chain P, Lamerdin J, Regala W, Allen EE, McCarren J, et al: The genome of a motile marine Synechococcus. Nature. 2003, 424 (6952): 1037-1042. 10.1038/nature01943.PubMedView ArticleGoogle Scholar
- McCord JM, Keele BB, Fridovich I: An enzyme-based theory of obligate anaerobiosis: the physiological function of superoxide dismutase. Proc Natl Acad Sci USA. 1971, 68 (5): 1024-1027. 10.1073/pnas.68.5.1024.PubMedPubMed CentralView ArticleGoogle Scholar
- Moura I, Tavares P, Moura JJ, Ravi N, Huynh BH, Liu MY, LeGall J: Purification and characterization of desulfoferrodoxin. A novel protein from Desulfovibrio desulfuricans (ATCC 27774) and from Desulfovibrio vulgaris (strain Hildenborough) that contains a distorted rubredoxin center and a mononuclear ferrous center. J Biol Chem. 1990, 265 (35): 21596-21602.PubMedGoogle Scholar
- Lombard M, Fontecave M, Touati D, Niviere V: Reaction of the desulfoferrodoxin from Desulfoarculus baarsii with superoxide anion. Evidence for a superoxide reductase activity. J Biol Chem. 2000, 275 (1): 115-121. 10.1074/jbc.275.1.115.PubMedView ArticleGoogle Scholar
- Chen L, Sharma P, Le Gall J, Mariano AM, Teixeira M, Xavier AV: A blue non-heme iron protein from Desulfovibrio gigas. Eur J Biochem. 1994, 226 (2): 613-618. 10.1111/j.1432-1033.1994.tb20087.x.PubMedView ArticleGoogle Scholar
- Jenney FE, Verhagen MF, Cui X, Adams MW: Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science. 1999, 286 (5438): 306-309. 10.1126/science.286.5438.306.PubMedView ArticleGoogle Scholar
- Pianzzola MJ, Soubes M, Touati D: Overproduction of the rbo gene product from Desulfovibrio species suppresses all deleterious effects of lack of superoxide dismutase in Escherichia coli. J Bacteriol. 1996, 178 (23): 6736-6742.PubMedPubMed CentralGoogle Scholar
- Lombard M, Touati D, Fontecave M, Niviere V: Superoxide reductase as a unique defense system against superoxide stress in the microaerophile Treponema pallidum. J Biol Chem. 2000, 275 (35): 27021-27026.PubMedGoogle Scholar
- Silva G, LeGall J, Xavier AV, Teixeira M, Rodrigues-Pousada C: Molecular characterization of Desulfovibrio gigas neelaredoxin, a protein involved in oxygen detoxification in anaerobes. J Bacteriol. 2001, 183 (15): 4413-4420. 10.1128/JB.183.4.4413-4420.2001.PubMedPubMed CentralView ArticleGoogle Scholar
- Liochev SI, Fridovich I: A mechanism for complementation of the sodA sodB defect in Escherichia coli by overproduction of the rbo gene product (desulfoferrodoxin) from Desulfoarculus baarsii. J Biol Chem. 1997, 272 (41): 25573-25575. 10.1074/jbc.272.41.25573.PubMedView ArticleGoogle Scholar
- Tulipan DJ, Eaton RG, Eberhart RE: The Darrach procedure defended: technique redefined and long-term follow-up. J Hand Surg Am. 1991, 16 (3): 438-444. 10.1016/0363-5023(91)90010-9.PubMedView ArticleGoogle Scholar
- Clay MD, Jenney FE, Hagedoorn PL, George GN, Adams MW, Johnson MK: Spectroscopic studies of Pyrococcus furiosus superoxide reductase: implications for active-site structures and the catalytic mechanism. J Am Chem Soc. 2002, 124 (5): 788-805. 10.1021/ja016889g.PubMedView ArticleGoogle Scholar
- Yeh AP, Hu Y, Jenney FE, Adams MW, Rees DC: Structures of the superoxide reductase from Pyrococcus furiosus in the oxidized and reduced states. Biochemistry. 2000, 39 (10): 2499-2508. 10.1021/bi992428k.PubMedView ArticleGoogle Scholar
- Coelho AV, Matias PM, Fulop V, Thompson A, Gonzalez A, Carrondo MA: Desulfoferrodoxin structure determined by MAD phasing and refinement to 1.9-Å resolution reveals a unique combination of a tetrahedral FeS4 centre with a square pyramidal FeSN4 centre. J Biol Inorg Chem. 1997, 2 (6): 680-689. 10.1007/s007750050184.View ArticleGoogle Scholar
- Archer M, Huber R, Tavares P, Moura I, Moura JJ, Carrondo MA, Sieker LC, LeGall J, Romao MJ: Crystal structure of desulforedoxin from Desulfovibrio gigas determined at 1.8 A resolution: a novel non-heme iron protein structure. J Mol Biol. 1995, 251 (5): 690-702. 10.1006/jmbi.1995.0465.PubMedView ArticleGoogle Scholar
- Kurtz DM, Coulter ED: The mechanism(s) of superoxide reduction by superoxide reductases in vitro and in vivo. J Biol Inorg Chem. 2002, 7 (6): 653-658. 10.1007/s00775-002-0360-4.PubMedView ArticleGoogle Scholar
- Pereira SA, Tavares P, Folgosa F, Almeida RM, Moura I, Moura JJG: European Journal of Inorganic Chemistry. European Journal of Inorganic Chemistry. 2007, 2007 (18): 2569-2581. 10.1002/ejic.200700008.View ArticleGoogle Scholar
- Jovanovic T, Ascenso C, Hazlett KR, Sikkink R, Krebs C, Litwiller R, Benson LM, Moura I, Moura JJ, Radolf JD, et al: Neelaredoxin, an iron-binding protein from the syphilis spirochete, Treponema pallidum, is a superoxide reductase. J Biol Chem. 2000, 275 (37): 28439-28448.PubMedView ArticleGoogle Scholar
- Thybert D, Avner S, Lucchetti-Miganeh C, Cheron A, Barloy-Hubler F: OxyGene: an innovative platform for investigating oxidative-response genes in whole prokaryotic genomes. BMC Genomics. 2008, 9: 637-10.1186/1471-2164-9-637.PubMedPubMed CentralView ArticleGoogle Scholar
- Brioukhanov AL, Netrusov AI: Catalase and superoxide dismutase: distribution, properties, and physiological role in cells of strict anaerobes. Biochemistry (Mosc). 2004, 69 (9): 949-962.View ArticleGoogle Scholar
- Tally FP, Goldin BR, Jacobus NV, Gorbach SL: Superoxide dismutase in anaerobic bacteria of clinical significance. Infect Immun. 1977, 16 (1): 20-25.PubMedPubMed CentralGoogle Scholar
- Rusnak F, Ascenso C, Moura I, Moura JJ: Superoxide reductase activities of neelaredoxin and desulfoferrodoxin metalloproteins. Methods Enzymol. 2002, 349: 243-258.PubMedView ArticleGoogle Scholar
- Niviere V, Fontecave M: Discovery of superoxide reductase: an historical perspective. J Biol Inorg Chem. 2004, 9 (2): 119-123. 10.1007/s00775-003-0519-7.PubMedView ArticleGoogle Scholar
- Pinto AF, Rodrigues JV, Teixeira M: Reductive elimination of superoxide: Structure and mechanism of superoxide reductases. Biochim Biophys Acta. 2010, 1804 (2): 285-297.PubMedView ArticleGoogle Scholar
- Skovgaard M, Jensen LJ, Brunak S, Ussery D, Krogh A: On the total number of genes and their length distribution in complete microbial genomes. Trends Genet. 2001, 17 (8): 425-428. 10.1016/S0168-9525(01)02372-1.PubMedView ArticleGoogle Scholar
- Dolla A, Fournier M, Dermoun Z: Oxygen defense in sulfate-reducing bacteria. J Biotechnol. 2006, 126 (1): 87-100. 10.1016/j.jbiotec.2006.03.041.PubMedView ArticleGoogle Scholar
- Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol. 1990, 215 (3): 403-410.PubMedView ArticleGoogle Scholar
- Gertz EM, Yu YK, Agarwala R, Schaffer AA, Altschul SF: Composition-based statistics and translated nucleotide searches: improving the TBLASTN module of BLAST. BMC Biol. 2006, 4: 41-10.1186/1741-7007-4-41.PubMedPubMed CentralView ArticleGoogle Scholar
- Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22 (22): 4673-4680. 10.1093/nar/22.22.4673.PubMedPubMed CentralView ArticleGoogle Scholar
- Higgins DG, Thompson JD, Gibson TJ: Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 1996, 266: 383-402.PubMedView ArticleGoogle Scholar
- Edgar RC: MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 2004, 5: 113-10.1186/1471-2105-5-113.PubMedPubMed CentralView ArticleGoogle Scholar
- Koonin EV, Wolf YI, Karev GP: The structure of the protein universe and genome evolution. Nature. 2002, 420 (6912): 218-223. 10.1038/nature01256.PubMedView ArticleGoogle Scholar
- Ponting CP, Russell RR: The natural history of protein domains. Annu Rev Biophys Biomol Struct. 2002, 31: 45-71. 10.1146/annurev.biophys.31.082901.134314.PubMedView ArticleGoogle Scholar
- Abreu IA, Saraiva LM, Carita J, Huber H, Stetter KO, Cabelli D, Teixeira M: Oxygen detoxification in the strict anaerobic archaeon Archaeoglobus fulgidus: superoxide scavenging by neelaredoxin. Mol Microbiol. 2000, 38 (2): 322-334. 10.1046/j.1365-2958.2000.02121.x.PubMedView ArticleGoogle Scholar
- Mathe C, Niviere V, Houee-Levin C, Mattioli TA: Fe(3+)-eta(2)-peroxo species in superoxide reductase from Treponema pallidum. Comparison with Desulfoarculus baarsii. Biophys Chem. 2006, 119 (1): 38-48. 10.1016/j.bpc.2005.06.013.PubMedView ArticleGoogle Scholar
- Kratzer C, Welte C, Dorner K, Friedrich T, Deppenmeier U: Methanoferrodoxin represents a new class of superoxide reductase containing an iron-sulfur cluster. FEBS J. 2011, 278 (3): 442-451. 10.1111/j.1742-4658.2010.07964.x.PubMedView ArticleGoogle Scholar
- Coulter ED, Kurtz DM: A role for rubredoxin in oxidative stress protection in Desulfovibrio vulgaris: catalytic electron transfer to rubrerythrin and two-iron superoxide reductase. Arch Biochem Biophys. 2001, 394 (1): 76-86. 10.1006/abbi.2001.2531.PubMedView ArticleGoogle Scholar
- Rodrigues JV, Saraiva LM, Abreu IA, Teixeira M, Cabelli DE: Superoxide reduction by Archaeoglobus fulgidus desulfoferrodoxin: comparison with neelaredoxin. J Biol Inorg Chem. 2007, 12 (2): 248-256. 10.1007/s00775-006-0182-x.PubMedView ArticleGoogle Scholar
- Coelho AV, Matias PM, Carrondo MA, Tavares P, Moura JJ, Moura I, Fulop V, Hajdu J, Le Gall J: Preliminary crystallographic analysis of the oxidized form of a two mono-nuclear iron centres protein from Desulfovibrio desulfuricans ATCC 27774. Protein Sci. 1996, 5 (6): 1189-1191.PubMedPubMed CentralView ArticleGoogle Scholar
- Stothard P, Wishart DS: Circular genome visualization and exploration using CGView. Bioinformatics. 2005, 21 (4): 537-539. 10.1093/bioinformatics/bti054.PubMedView ArticleGoogle Scholar
- Petkau A, Stuart-Edwards M, Stothard P, Van Domselaar G: Interactive Microbial Genome Visualization with GView. Bioinformatics. 2010Google Scholar
- Goudenege D, Avner S, Lucchetti-Miganeh C, Barloy-Hubler F: CoBaltDB: Complete bacterial and archaeal orfeomes subcellular localization database and associated resources. BMC Microbiol. 2010, 10: 88-10.1186/1471-2180-10-88.PubMedPubMed CentralView ArticleGoogle Scholar
- Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO: SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007, 35 (21): 7188-7196. 10.1093/nar/gkm864.PubMedPubMed CentralView ArticleGoogle Scholar
- Barns SM, Delwiche CF, Palmer JD, Dawson SC, Hershberger KL, Pace NR: Phylogenetic perspective on microbial life in hydrothermal ecosystems, past and present. Ciba Found Symp. 1996, 202: 24-32. discussion 32-29.PubMedGoogle Scholar
- Huber H, Hohn MJ, Rachel R, Fuchs T, Wimmer VC, Stetter KO: A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature. 2002, 417 (6884): 63-67. 10.1038/417063a.PubMedView ArticleGoogle Scholar
- Paper W, Jahn U, Hohn MJ, Kronner M, Nather DJ, Burghardt T, Rachel R, Stetter KO, Huber H: Ignicoccus hospitalis sp. nov., the host of 'Nanoarchaeum equitans'. Int J Syst Evol Microbiol. 2007, 57 (Pt 4): 803-808.PubMedView ArticleGoogle Scholar
- Burggraf S, Huber H, Stetter KO: Reclassification of the crenarchael orders and families in accordance with 16S rRNA sequence data. Int J Syst Bacteriol. 1997, 47 (3): 657-660. 10.1099/00207713-47-3-657.PubMedView ArticleGoogle Scholar
- Kawarabayasi Y, Hino Y, Horikawa H, Yamazaki S, Haikawa Y, Jin-no K, Takahashi M, Sekine M, Baba S, Ankai A, et al: Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1. DNA Res. 1999, 6 (2): 83-101. 10.1093/dnares/6.2.83. 145-152PubMedView ArticleGoogle Scholar
- Lee HJ, Kwon HW, Koh JU, Lee DK, Moon JY, Kong KH: An efficient method for the expression and reconstitution of thermostable Mn/Fe superoxide dismutase from Aeropyrum pernix K1. J Microbiol Biotechnol. 2010, 20 (4): 727-731.PubMedGoogle Scholar
- Niederberger TD, Gotz DK, McDonald IR, Ronimus RS, Morgan HW: Ignisphaera aggregans gen. nov., sp. nov., a novel hyperthermophilic crenarchaeote isolated from hot springs in Rotorua and Tokaanu, New Zealand. Int J Syst Evol Microbiol. 2006, 56 (Pt 5): 965-971.PubMedView ArticleGoogle Scholar
- Rose RW, Bruser T, Kissinger JC, Pohlschroder M: Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol Microbiol. 2002, 45 (4): 943-950. 10.1046/j.1365-2958.2002.03090.x.PubMedView ArticleGoogle Scholar
- Bendtsen JD, Nielsen H, Widdick D, Palmer T, Brunak S: Prediction of twin-arginine signal peptides. BMC Bioinformatics. 2005, 6: 167-10.1186/1471-2105-6-167.PubMedPubMed CentralView ArticleGoogle Scholar
- Hafenbradl D, Keller M, Dirmeier R, Rachel R, Rossnagel P, Burggraf S, Huber H, Stetter KO: Ferroglobus placidus gen. nov., sp. nov., A novel hyperthermophilic archaeum that oxidizes Fe2+ at neutral pH under anoxic conditions. Arch Microbiol. 1996, 166 (5): 308-314. 10.1007/s002030050388.PubMedView ArticleGoogle Scholar
- Klenk HP, Clayton RA, Tomb JF, White O, Nelson KE, Ketchum KA, Dodson RJ, Gwinn M, Hickey EK, Peterson JD, et al: The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature. 1997, 390 (6658): 364-370. 10.1038/37052.PubMedView ArticleGoogle Scholar
- Burggraf S, Jannasch HW, Nicolaus B, Stetter KO: Archaeoglobus profundus sp. nov., represents a new species within the sulfate-reducing archaebacteria. Syst Appl Microbiol. 1990, 13: 24-28.View ArticleGoogle Scholar
- Fomenko DE, Gladyshev VN: Identity and functions of CxxC-derived motifs. Biochemistry. 2003, 42 (38): 11214-11225. 10.1021/bi034459s.PubMedView ArticleGoogle Scholar
- Ladenstein R, Ren B: Reconsideration of an early dogma, saying "there is no evidence for disulfide bonds in proteins from archaea". Extremophiles. 2008, 12 (1): 29-38. 10.1007/s00792-007-0076-z.PubMedView ArticleGoogle Scholar
- Maeder DL, Anderson I, Brettin TS, Bruce DC, Gilna P, Han CS, Lapidus A, Metcalf WW, Saunders E, Tapia R, et al: The Methanosarcina barkeri genome: comparative analysis with Methanosarcina acetivorans and Methanosarcina mazei reveals extensive rearrangement within methanosarcinal genomes. J Bacteriol. 2006, 188 (22): 7922-7931. 10.1128/JB.00810-06.PubMedPubMed CentralView ArticleGoogle Scholar
- Devreese B, Tavares P, Lampreia J, Van Damme N, Le Gall J, Moura JJ, Van Beeumen J, Moura I: Primary structure of desulfoferrodoxin from Desulfovibrio desulfuricans ATCC 27774, a new class of non-heme iron proteins. FEBS Lett. 1996, 385 (3): 138-142. 10.1016/0014-5793(96)00364-X.PubMedView ArticleGoogle Scholar
- Tavares P, Ravi N, Moura JJ, LeGall J, Huang YH, Crouse BR, Johnson MK, Huynh BH, Moura I: Spectroscopic properties of desulfoferrodoxin from Desulfovibrio desulfuricans (ATCC 27774). J Biol Chem. 1994, 269 (14): 10504-10510.PubMedGoogle Scholar
- Romao CV, Liu MY, Le Gall J, Gomes CM, Braga V, Pacheco I, Xavier AV, Teixeira M: The superoxide dismutase activity of desulfoferrodoxin from Desulfovibrio desulfuricans ATCC 27774. Eur J Biochem. 1999, 261 (2): 438-443. 10.1046/j.1432-1327.1999.00278.x.PubMedView ArticleGoogle Scholar
- Adam V, Royant A, Niviere V, Molina-Heredia FP, Bourgeois D: Structure of superoxide reductase bound to ferrocyanide and active site expansion upon X-ray-induced photo-reduction. Structure. 2004, 12 (9): 1729-1740. 10.1016/j.str.2004.07.013.PubMedView ArticleGoogle Scholar
- Katona G, Carpentier P, Niviere V, Amara P, Adam V, Ohana J, Tsanov N, Bourgeois D: Raman-assisted crystallography reveals end-on peroxide intermediates in a nonheme iron enzyme. Science. 2007, 316 (5823): 449-453. 10.1126/science.1138885.PubMedView ArticleGoogle Scholar
- Niviere V, Asso M, Weill CO, Lombard M, Guigliarelli B, Favaudon V, Houee-Levin C: Superoxide reductase from Desulfoarculus baarsii: identification of protonation steps in the enzymatic mechanism. Biochemistry. 2004, 43 (3): 808-818. 10.1021/bi035698i.PubMedView ArticleGoogle Scholar
- Mathe C, Mattioli TA, Horner O, Lombard M, Latour JM, Fontecave M, Niviere V: Identification of iron(III) peroxo species in the active site of the superoxide reductase SOR from Desulfoarculus baarsii. J Am Chem Soc. 2002, 124 (18): 4966-4967. 10.1021/ja025707v.PubMedView ArticleGoogle Scholar
- Mathe C, Weill CO, Mattioli TA, Berthomieu C, Houee-Levin C, Tremey E, Niviere V: Assessing the role of the active-site cysteine ligand in the superoxide reductase from Desulfoarculus baarsii. J Biol Chem. 2007, 282 (30): 22207-22216. 10.1074/jbc.M700279200.PubMedView ArticleGoogle Scholar
- Mathe C, Niviere V, Mattioli TA: Fe3+-hydroxide ligation in the superoxide reductase from Desulfoarculus baarsii is associated with pH dependent spectral changes. J Am Chem Soc. 2005, 127 (47): 16436-16441. 10.1021/ja053808y.PubMedView ArticleGoogle Scholar
- Horner O, Mouesca JM, Oddou JL, Jeandey C, Niviere V, Mattioli TA, Mathe C, Fontecave M, Maldivi P, Bonville P, et al: Mossbauer characterization of an unusual high-spin side-on peroxo-Fe3+ species in the active site of superoxide reductase from Desulfoarculus Baarsii. Density functional calculations on related models. Biochemistry. 2004, 43 (27): 8815-8825. 10.1021/bi0498151.PubMedView ArticleGoogle Scholar
- Berthomieu C, Dupeyrat F, Fontecave M, Vermeglio A, Niviere V: Redox-dependent structural changes in the superoxide reductase from Desulfoarculus baarsii and Treponema pallidum: a FTIR study. Biochemistry. 2002, 41 (32): 10360-10368. 10.1021/bi020344x.PubMedView ArticleGoogle Scholar
- Bonnot F, Houee-Levin C, Favaudon V, Niviere V: Photochemical processes observed during the reaction of superoxide reductase from Desulfoarculus baarsii with superoxide: re-evaluation of the reaction mechanism. Biochim Biophys Acta. 2010, 1804 (4): 762-767.PubMedView ArticleGoogle Scholar
- Clay MD, Jenney FE, Noh HJ, Hagedoorn PL, Adams MW, Johnson MK: Resonance Raman characterization of the mononuclear iron active-site vibrations and putative electron transport pathways in Pyrococcus furiosus superoxide reductase. Biochemistry. 2002, 41 (31): 9833-9841. 10.1021/bi025833b.PubMedView ArticleGoogle Scholar
- Grunden AM, Jenney FE, Ma K, Ji M, Weinberg MV, Adams MW: In vitro reconstitution of an NADPH-dependent superoxide reduction pathway from Pyrococcus furiosus. Appl Environ Microbiol. 2005, 71 (3): 1522-1530. 10.1128/AEM.71.3.1522-1530.2005.PubMedPubMed CentralView ArticleGoogle Scholar
- Clay MD, Cosper CA, Jenney FE, Adams MW, Johnson MK: Nitric oxide binding at the mononuclear active site of reduced Pyrococcus furiosus superoxide reductase. Proc Natl Acad Sci USA. 2003, 100 (7): 3796-3801. 10.1073/pnas.0636858100.PubMedPubMed CentralView ArticleGoogle Scholar
- Im YJ, Ji M, Lee A, Killens R, Grunden AM, Boss WF: Expression of Pyrococcus furiosus superoxide reductase in Arabidopsis enhances heat tolerance. Plant Physiol. 2009, 151 (2): 893-904. 10.1104/pp.109.145409.PubMedPubMed CentralView ArticleGoogle Scholar
- Santos-Silva T, Trincao J, Carvalho AL, Bonifacio C, Auchere F, Raleiras P, Moura I, Moura JJ, Romao MJ: The first crystal structure of class III superoxide reductase from Treponema pallidum. J Biol Inorg Chem. 2006, 11 (5): 548-558. 10.1007/s00775-006-0104-y.PubMedView ArticleGoogle Scholar
- Santos-Silva T, Trincao J, Carvalho AL, Bonifacio C, Auchere F, Moura I, Moura JJ, Romao MJ: Superoxide reductase from the syphilis spirochete Treponema pallidum: crystallization and structure determination using soft X-rays. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2005, 61 (Pt 11): 967-970.PubMedPubMed CentralView ArticleGoogle Scholar
- Niviere V, Lombard M, Fontecave M, Houee-Levin C: Pulse radiolysis studies on superoxide reductase from Treponema pallidum. FEBS Lett. 2001, 497 (2-3): 171-173. 10.1016/S0014-5793(01)02468-1.PubMedView ArticleGoogle Scholar
- Auchere F, Sikkink R, Cordas C, Raleiras P, Tavares P, Moura I, Moura JJ: Overexpression and purification of Treponema pallidum rubredoxin; kinetic evidence for a superoxide-mediated electron transfer with the superoxide reductase neelaredoxin. J Biol Inorg Chem. 2004, 9 (7): 839-849. 10.1007/s00775-004-0584-6.PubMedView ArticleGoogle Scholar
- Hazlett KR, Cox DL, Sikkink RA, Auch'ere F, Rusnak F, Radolf JD: Contribution of neelaredoxin to oxygen tolerance by Treponema pallidum. Methods Enzymol. 2002, 353: 140-156.PubMedView ArticleGoogle Scholar
- Auchere F, Raleiras P, Benson L, Venyaminov SY, Tavares P, Moura JJ, Moura I, Rusnak F: Formation of a stable cyano-bridged dinuclear iron cluster following oxidation of the superoxide reductases from Treponema pallidum and Desulfovibrio vulgaris with K(3)Fe(CN)(6). Inorg Chem. 2003, 42 (4): 938-940. 10.1021/ic0262886.PubMedView ArticleGoogle Scholar
- Lombard M, Houee-Levin C, Touati D, Fontecave M, Niviere V: Superoxide reductase from Desulfoarculus baarsii: reaction mechanism and role of glutamate 47 and lysine 48 in catalysis. Biochemistry. 2001, 40 (16): 5032-5040. 10.1021/bi0023908.PubMedView ArticleGoogle Scholar
- Niviere V, Lombard M: Superoxide reductase from Desulfoarculus baarsii. Methods Enzymol. 2002, 349: 123-129.PubMedView ArticleGoogle Scholar
- Bandeiras TM, Romao CV, Rodrigues JV, Teixeira M, Matias PM: Purification, crystallization and X-ray crystallographic analysis of Archaeoglobus fulgidus neelaredoxin. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2010, 66 (Pt 3): 316-319.PubMedPubMed CentralView ArticleGoogle Scholar
- Rodrigues JV, Abreu IA, Cabelli D, Teixeira M: Superoxide reduction mechanism of Archaeoglobus fulgidus one-iron superoxide reductase. Biochemistry. 2006, 45 (30): 9266-9278. 10.1021/bi052489k.PubMedView ArticleGoogle Scholar
- Todorovic S, Rodrigues JV, Pinto AF, Thomsen C, Hildebrandt P, Teixeira M, Murgida DH: Resonance Raman study of the superoxide reductase from Archaeoglobus fulgidus, E12 mutants and a 'natural variant'. Phys Chem Chem Phys. 2009, 11 (11): 1809-1815.PubMedView ArticleGoogle Scholar
- Abreu IA, Saraiva LM, Soares CM, Teixeira M, Cabelli DE: The mechanism of superoxide scavenging by Archaeoglobus fulgidus neelaredoxin. J Biol Chem. 2001, 276 (42): 38995-39001. 10.1074/jbc.M103232200.PubMedView ArticleGoogle Scholar
- Kitamura M, Koshino Y, Kamikawa Y, Kohno K, Kojima S, Miura K, Sagara T, Akutsu H, Kumagai I, Nakaya T: Cloning and expression of the rubredoxin gene from Desulfovibrio vulgaris (Miyazaki F)--comparison of the primary structure of desulfoferrodoxin. Biochim Biophys Acta. 1997, 1351 (1-2): 239-247.PubMedView ArticleGoogle Scholar
- Huang VW, Emerson JP, Kurtz DM: Reaction of Desulfovibrio vulgaris two-iron superoxide reductase with superoxide: insights from stopped-flow spectrophotometry. Biochemistry. 2007, 46 (40): 11342-11351. 10.1021/bi700450u.PubMedView ArticleGoogle Scholar
- Wildschut JD, Lang RM, Voordouw JK, Voordouw G: Rubredoxin:oxygen oxidoreductase enhances survival of Desulfovibrio vulgaris hildenborough under microaerophilic conditions. J Bacteriol. 2006, 188 (17): 6253-6260. 10.1128/JB.00425-06.PubMedPubMed CentralView ArticleGoogle Scholar
- Clay MD, Emerson JP, Coulter ED, Kurtz DM, Johnson MK: Spectroscopic characterization of the [Fe(His)(4)(Cys)] site in 2Fe-superoxide reductase from Desulfovibrio vulgaris. J Biol Inorg Chem. 2003, 8 (6): 671-682. 10.1007/s00775-003-0465-4.PubMedView ArticleGoogle Scholar
- Emerson JP, Coulter ED, Cabelli DE, Phillips RS, Kurtz DM: Kinetics and mechanism of superoxide reduction by two-iron superoxide reductase from Desulfovibrio vulgaris. Biochemistry. 2002, 41 (13): 4348-4357. 10.1021/bi0119159.PubMedView ArticleGoogle Scholar
- Silva G, Oliveira S, Gomes CM, Pacheco I, Liu MY, Xavier AV, Teixeira M, Legall J, Rodrigues-pousada C: Desulfovibrio gigas neelaredoxin. A novel superoxide dismutase integrated in a putative oxygen sensory operon of an anaerobe. Eur J Biochem. 1999, 259 (1-2): 235-243. 10.1046/j.1432-1327.1999.00025.x.PubMedView ArticleGoogle Scholar
- Riebe O, Fischer RJ, Bahl H: Desulfoferrodoxin of Clostridium acetobutylicum functions as a superoxide reductase. FEBS Lett. 2007, 581 (29): 5605-5610. 10.1016/j.febslet.2007.11.008.PubMedView ArticleGoogle Scholar
- Kawasaki S, Sakai Y, Takahashi T, Suzuki I, Niimura Y: O2 and reactive oxygen species detoxification complex, composed of O2-responsive NADH:rubredoxin oxidoreductase-flavoprotein A2-desulfoferrodoxin operon enzymes, rubperoxin, and rubredoxin, in Clostridium acetobutylicum. Appl Environ Microbiol. 2009, 75 (4): 1021-1029. 10.1128/AEM.01425-08.PubMedPubMed CentralView ArticleGoogle Scholar
- Rodrigues JV, Victor BL, Huber H, Saraiva LM, Soares CM, Cabelli DE, Teixeira M: Superoxide reduction by Nanoarchaeum equitans neelaredoxin, an enzyme lacking the highly conserved glutamate iron ligand. J Biol Inorg Chem. 2008, 13 (2): 219-228. 10.1007/s00775-007-0313-z.PubMedView ArticleGoogle Scholar
- Clamp M, Cuff J, Searle SM, Barton GJ: The Jalview Java alignment editor. Bioinformatics. 2004, 20 (3): 426-427. 10.1093/bioinformatics/btg430.PubMedView ArticleGoogle Scholar
- Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ: Jalview Version 2--a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009, 25 (9): 1189-1191. 10.1093/bioinformatics/btp033.PubMedPubMed CentralView ArticleGoogle Scholar
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