Computational identification of a new SelD-like family that may participate in sulfur metabolism in hyperthermophilic sulfur-reducing archaea

BMC Genomics

Yan Zhang²  Qiong Liu³  Jia-Zuan Ni³  Liang Jiang³  Gao-Peng Li¹ 

[1] Key Laboratory of Systems Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Shanghai 200031, P. R. China;Key Laboratory of Nutrition and Metabolism, Institute for Nutritional Sciences, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Shanghai 200031, P. R. China;College of Life Sciences, Shenzhen University, Shenzhen 518060, Guangdong Province, P. R. China

关键词: Archaea;    Comparative genomics;    Bioinformatics;    Selenophosphate synthetase;    Sulfur;    Selenium;   

Others  :  1128448
DOI  :  10.1186/1471-2164-15-908

 received in 2013-09-05, accepted in 2014-10-07,  发布年份 2014

【 摘 要 】

Background

Selenium (Se) and sulfur (S) are closely related elements that exhibit similar chemical properties. Some genes related to S metabolism are also involved in Se utilization in many organisms. However, the evolutionary relationship between the two utilization traits is unclear.

Results

In this study, we conducted a comparative analysis of the selenophosphate synthetase (SelD) family, a key protein for all known Se utilization traits, in all sequenced archaea. Our search showed a very limited distribution of SelD and Se utilization in this kingdom. Interestingly, a SelD-like protein was detected in two orders of Crenarchaeota: Sulfolobales and Thermoproteales. Sequence and phylogenetic analyses revealed that SelD-like protein contains the same domain and conserved functional residues as those of SelD, and might be involved in S metabolism in these S-reducing organisms. Further genome-wide analysis of patterns of gene occurrence in different thermoproteales suggested that several genes, including SirA-like, Prx-like and adenylylsulfate reductase, were strongly related to SelD-like gene. Based on these findings, we proposed a simple model wherein SelD-like may play an important role in the biosynthesis of certain thiophosphate compound.

Conclusions

Our data suggest novel genes involved in S metabolism in hyperthermophilic S-reducing archaea, and may provide a new window for understanding the complex relationship between Se and S metabolism in archaea.

【 授权许可】

   
2014 Li et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Rayman MP: Selenium and human health. Lancet 2012, 379:1256-1268.
• [2]Stadtman TC: Selenocysteine. Annu Rev Biochem 1996, 65:83-100.
• [3]Hatfield DL, Gladyshev VN: How selenium has altered our understanding of the genetic code. Mol Cell Biol 2002, 22:3565-3576.
• [4]Low SC, Berry MJ: Knowing when not to stop: selenocysteine incorporation in eukaryotes. Trends Biochem Sci 1996, 21:203-208.
• [5]Driscoll DM, Copeland PR: Mechanism and regulation of selenoprotein synthesis. Annu Rev Nutr 2003, 23:17-40.
• [6]Böck A: Biosynthesis of selenoproteins: an overview. Biofactors 2000, 11:77-78.
• [7]Allmang C, Wurth L, Krol A: The selenium to selenoprotein pathway in eukaryotes: more molecular partners than anticipated. Biochim Biophys Acta 2009, 1790:1415-1423.
• [8]Thanbichler M, Böck A: Selenoprotein biosynthesis: purification and assay of components involved in selenocysteine biosynthesis and insertion in Escherichia coli. Methods Enzymol 2002, 347:3-16.
• [9]Turner RJ, Weiner JH, Taylor DE: Selenium metabolism in Escherichia coli. Biometals 1998, 11:223-227.
• [10]Donovan J, Copeland PR: Threading the needle: getting selenocysteine into proteins. Antioxid Redox Signal 2010, 12:881-892.
• [11]Xu XM, Carlson BA, Zhang Y, Mix H, Kryukov GV, Glass RS, Berry MJ, Gladyshev VN, Hatfield DL: New developments in selenium biochemistry: selenocysteine biosynthesis in eukaryotes and archaea. Biol Trace Elem Res 2007, 119:234-241.
• [12]Squires JE, Berry MJ: Eukaryotic selenoprotein synthesis: mechanistic insight incorporating new factors and new functions for old factors. IUBMB Life 2008, 60:232-235.
• [13]Ching WM, Alzner-DeWeerd B, Stadtman TC: A selenium-containing nucleoside at the first position of the anticodon in seleno-tRNAGlu from Clostridium sticklandii. Proc Natl Acad Sci U S A 1985, 82:347-350.
• [14]Haft DH, Self WT: Orphan SelD proteins and selenium-dependent molybdenum hydroxylases. Biol Direct 2008, 3:4. BioMed Central Full Text
• [15]Srivastava M, Mallard C, Barke T, Hancock LE, Self WT: A selenium-dependent xanthine dehydrogenase triggers biofilm proliferation in Enterococcus faecalis through oxidant production. J Bacteriol 2011, 193:1643-1652.
• [16]Zhang Y, Turanov AA, Hatfield DL, Gladyshev VN: In silico identification of genes involved in selenium metabolism: evidence for a third selenium utilization trait. BMC Genomics 2008, 9:251. BioMed Central Full Text
• [17]Romero H, Zhang Y, Gladyshev VN, Salinas G: Evolution of selenium utilization traits. Genome Biol 2005, 6:R66. BioMed Central Full Text
• [18]McCulloch KM, Kinsland C, Begley TP, Ealick SE: Structural studies of thiamin monophosphate kinase in complex with substrates and products. Biochemistry 2008, 47:3810-3821.
• [19]Veres Z, Kim IY, Scholz TD, Stadtman TC: Selenophosphate synthetase: enzyme properties and catalytic reaction. J Biol Chem 1994, 269:10597-10603.
• [20]Couture RM, Sekowska A, Fang G, Danchin A: Linking selenium biogeochemistry to the sulfur-dependent biological detoxification of arsenic. Environ Microbiol 2012, 14:1612-1623.
• [21]Preabrazhenskaya YV, Kim IY, Stadtman TC: Binding of ATP and its derivatives to selenophosphate synthetase from Escherichia coli. Biochemistry (Mosc) 2009, 74:910-916.
• [22]Sculaccio SA, Rodrigues EM, Cordeiro AT, Magalhães A, Braga AL, Alberto EE, Thiemann OH: Selenocysteine incorporation in Kinetoplastid: selenophosphate synthetase (SELD) from Leishmania major and Trypanosoma brucei. Mol Biochem Parasitol 2008, 162:165-171.
• [23]Xu XM, Carlson BA, Irons R, Mix H, Zhong N, Gladyshev VN, Hatfield DL: Selenophosphate synthetase 2 is essential for selenoprotein biosynthesis. Biochem J 2007, 404:115-120.
• [24]Collins R, Johansson AL, Karlberg T, Markova N, van den Berg S, Olesen K, Hammarström M, Flores A, Schüler H, Schiavone LH, Brzezinski P, Arnér ES, Högbom M: Biochemical discrimination between selenium and sulfur 1: a single residue provides selenium specificity to human selenocysteine lyase. PLoS One 2012, 7:e30581.
• [25]Aguilar-Barajas E, Díaz-Pérez C, Ramírez-Díaz MI, Riveros-Rosas H, Cervantes C: Bacterial transport of sulfate, molybdate, and related oxyanions. Biometals 2011, 24:687-707.
• [26]Lobanov AV, Fomenko DE, Zhang Y, Sengupta A, Hatfield DL, Gladyshev VN: Evolutionary dynamics of eukaryotic selenoproteomes: large selenoproteomes may associate with aquatic life and small with terrestrial life. Genome Biol 2007, 8:R198. BioMed Central Full Text
• [27]Zhang Y, Romero H, Salinas G, Gladyshev VN: Dynamic evolution of selenocysteine utilization in bacteria: a balance between selenoprotein loss and evolution of selenocysteine from redox active cysteine residues. Genome Biol 2006, 7:R94. BioMed Central Full Text
• [28]Zhang Y, Gladyshev VN: General trends in trace element utilization revealed by comparative genomic analyses of Co, Cu, Mo, Ni, and Se. J Biol Chem 2010, 285:3393-3405.
• [29]Itoh Y, Sekine S, Matsumoto E, Akasaka R, Takemoto C, Shirouzu M, Yokoyama S: Structure of selenophosphate synthetase essential for selenium incorporation into proteins and RNAs. J Mol Biol 2009, 385(5):1456-1469.
• [30]Noinaj N, Wattanasak R, Lee DY, Wally JL, Piszczek G, Chock PB, Stadtman TC, Buchanan SK: Structural insights into the catalytic mechanism of Escherichia coli selenophosphate synthetase. J Bacteriol 2012, 194:499-508.
• [31]Osbourn AE, Field B: Operons. Cell Mol Life Sci 2009, 66:3755-3775.
• [32]Mizuno Y, Kanesaka Y, Fujita H, Minowa O, Shiokawa H: The primary structure of two molecular species of porcine organ-common type acylphosphatase. J Biochem 1991, 110:790-794.
• [33]Stefani M, Taddei N, Ramponi G: Insights into acylphosphatase structure and catalytic mechanism. Cell Mol Life Sci 1997, 53:141-151.
• [34]Bemporad F, Vannocci T, Varela L, Azuaga AI, Chiti F: A model for the aggregation of the acylphosphatase from Sulfolobus solfataricus in its native-like state. Biochim Biophys Acta 2008, 1784:1986-1996.
• [35]Bemporad F, Chiti F: “Native-like aggregation” of the acylphosphatase from Sulfolobus solfataricus and its biological implications. FEBS Lett 2009, 583:2630-2638.
• [36]Flohé L, Budde H, Hofmann B: Peroxiredoxins in antioxidant defense and redox regulation. Biofactors 2003, 19:3-10.
• [37]Meyer B, Kuever J: Molecular analysis of the diversity of sulfate-reducing and sulfur-oxidizing prokaryotes in the environment, using aprA as functional marker gene. Appl Environ Microbiol 2007, 73:7664-7679.
• [38]Dahl C, Trüper HG: Sulfite reductase and APS reductase from Archaeoglobus fulgidus. Methods Enzymol 2001, 331:427-441.
• [39]Pereira IA, Ramos AR, Grein F, Marques MC, da Silva SM, Venceslau SS: A comparative genomic analysis of energy metabolism in sulfate reducing bacteria and archaea. Front Microbiol 2011, 2:69.
• [40]Zhang CM, Liu C, Slater S, Hou YM: Aminoacylation of tRNA with phosphoserine for synthesis of cysteinyl-tRNA(Cys). Nat Struct Mol Biol 2008, 15:507-514.
• [41]The NCBI Genome Table [http://www.ncbi.nlm.nih.gov/genome/browse/ webcite]
• [42]Wolf YI, Koonin EV: A tight link between orthologs and bidirectional best hits in bacterial and archaeal genomes. Genome Biol Evol 2012, 4:1286-1294.
• [43]Sievers F, Wilm A, Dineen DG, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG: Fast, scalable generation of high-quality protein multiple sequence alignments using clustal omega. Mol Syst Biol 2011, 7:539.
• [44]Felsenstein J: PHYLIP – Phylogeny Inference Package (Version 3.2). Cladistics 1989, 5:164-166.
• [45]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
• [46]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
• [47]Xu XM, Carlson BA, Mix H, Zhang Y, Saira K, Glass RS, Berry MJ, Gladyshev VN, Hatfield DL: Biosynthesis of selenocysteine on its tRNA in eukaryotes. PLoS Biol 2007, 5:e4.