期刊论文详细信息
BMC Microbiology
Whole-genome sequencing reveals novel insights into sulfur oxidation in the extremophile Acidithiobacillus thiooxidans
Xueduan Liu2  Jiaojiao Niu2  Liyuan Ma2  Jing Cong2  Yunhua Xiao2  Qi Hu2  Xue Guo2  Yili Liang2  Zhili He1  Xiaoqi Li2  Xian Zhang2  Huaqun Yin2 
[1]Institute for Environmental Genomics, University of Oklahoma, Norman, OK, USA
[2]Key Laboratory of Biometallurgy of Ministry of Education, Central South University, Changsha, China
关键词: Sulfur oxidation model;    Real-time quantitative PCR;    Bioinformatics analysis;    Whole genome sequence;    Acidithiobacillus thiooxidans;   
Others  :  1140850
DOI  :  10.1186/1471-2180-14-179
 received in 2014-02-14, accepted in 2014-06-19,  发布年份 2014
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【 摘 要 】

Background

Acidithiobacillus thiooxidans (A. thiooxidans), a chemolithoautotrophic extremophile, is widely used in the industrial recovery of copper (bioleaching or biomining). The organism grows and survives by autotrophically utilizing energy derived from the oxidation of elemental sulfur and reduced inorganic sulfur compounds (RISCs). However, the lack of genetic manipulation systems has restricted our exploration of its physiology. With the development of high-throughput sequencing technology, the whole genome sequence analysis of A. thiooxidans has allowed preliminary models to be built for genes/enzymes involved in key energy pathways like sulfur oxidation.

Results

The genome of A. thiooxidans A01 was sequenced and annotated. It contains key sulfur oxidation enzymes involved in the oxidation of elemental sulfur and RISCs, such as sulfur dioxygenase (SDO), sulfide quinone reductase (SQR), thiosulfate:quinone oxidoreductase (TQO), tetrathionate hydrolase (TetH), sulfur oxidizing protein (Sox) system and their associated electron transport components. Also, the sulfur oxygenase reductase (SOR) gene was detected in the draft genome sequence of A. thiooxidans A01, and multiple sequence alignment was performed to explore the function of groups of related protein sequences. In addition, another putative pathway was found in the cytoplasm of A. thiooxidans, which catalyzes sulfite to sulfate as the final product by phosphoadenosine phosphosulfate (PAPS) reductase and adenylylsulfate (APS) kinase. This differs from its closest relative Acidithiobacillus caldus, which is performed by sulfate adenylyltransferase (SAT). Furthermore, real-time quantitative PCR analysis showed that most of sulfur oxidation genes were more strongly expressed in the S0 medium than that in the Na2S2O3 medium at the mid-log phase.

Conclusion

Sulfur oxidation model of A. thiooxidans A01 has been constructed based on previous studies from other sulfur oxidizing strains and its genome sequence analyses, providing insights into our understanding of its physiology and further analysis of potential functions of key sulfur oxidation genes.

【 授权许可】

   
2014 Yin et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Hallberg KB, González-Toril E, Johnson DB: Acidithiobacillus ferrivorans, sp. nov.; facultatively anaerobic, psychrotolerant iron-, and sulfur-oxidizing acidophiles isolated from metal mine-impacted environments. Extremophiles 2010, 14(1):9-19.
  • [2]Quatrini R, Appia-Ayme C, Denis Y, Jedlicki E, Holmes DS, Bonnefoy V: Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans. BMC Genomics 2009, 10:394.
  • [3]Rohwerder T, Gehrke T, Kinzler K, Sand W: Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl Microbiol Biotechnol 2003, 63:239-248.
  • [4]Holmes DS, Bonnefoy V: Genetic And Bioinformatic Insights Into Iron And Sulfur Oxidation Mechanisms Of Bioleaching Organisms. In Biomining. Edited by Rawlings DE, Johnson DB. Berlin: Springer; 2007:281-307.
  • [5]Pronk JT, Meulenberg R, Hazeu W, Bos P, Kuenen JG: Oxidation of reduced inorganic sulphur compounds by acidophilic thiobacilli. FEMS Microbiol Lett 1990, 75(2–3):293-306.
  • [6]Valdes J, Pedroso I, Quatrini R, Dodson RJ, Tettelin H, Blake R, Eisen JA, Holmes DS: Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genomics 2008, 9:597.
  • [7]Steudel R: The Chemical Sulfur Cycle. In Environmental Technologies to Treat Sulfur Pollution. Edited by Lens PNL, Pol LH. IWA Publishing: London; 2000:1-31.
  • [8]Rohwerder T, Sand W: The sulfane sulfur of persulfides is the actual substrate of the sulfur-oxidizing enzymes from Acidithiobacillus and Acidiphilium spp. Microbiology 2003, 149(7):1699-1710.
  • [9]Chen L, Ren Y, Lin J, Liu X, Pang X, Lin J: Acidithiobacillus caldus sulfur oxidation model based on transcriptome analysis between the wild type and sulfur oxygenase reductase defective mutant. PLoS One 2012, 7(9):e39470.
  • [10]Bobadilla Fazzini RA, Cortés MP, Padilla L, Maturana D, Budinich M, Maass A, Parada P: Stoichiometric modeling of oxidation of reduced inorganic sulfur compounds (Riscs) in Acidithiobacillus thiooxidans. Biotechnol Bioeng 2013, 110(8):2242-2251.
  • [11]Mangold S, Valdes J, Holmes DS, Dopson M: Sulfur metabolism in the extreme acidophile Acidithiobacillus caldus. Front Microbiol 2011, 2:17.
  • [12]Schütz M, Maldener I, Griesbeck C, Hauska G: Sulfide-quinone reductase from Rhodobacter capsulatus: requirement for growth, periplasmic localization, and extension of gene sequence analysis. J Bacteriol 1999, 181:6516-6523.
  • [13]Friedrich CG: Physiology And Genetics Of Bacterial Sulfur Oxidation. In Advances in Microbial Physiology. Edited by Poole RK. Amsterdam: Elsevier; 1997:235-289.
  • [14]Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J: Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 2001, 67(7):2873-2882.
  • [15]Friedrich CG, Quentmeier A, Bardischewsky F, Rother D, Kraft R, Kostka S, Prinz H: Novel genes coding for lithotrophic sulfur oxidation of Paracoccus pantotrophus GB17. J Bacteriol 2000, 182(17):4677-4687.
  • [16]Rother D, Henrich H, Quentmeier A, Bardischewsky F, Friedrich CG: Novel genes of the sox gene cluster, mutagenesis of the flavoprotein SoxF, and evidence for a general sulfur-oxidizing system in Paracoccus pantotrophus GB17. J Bacteriol 2001, 183(15):4499-4508.
  • [17]Ghosh W, Dam B: Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiol Rev 2009, 33(6):999-1043.
  • [18]de Jong GAH, Hazeu W, Bos P, Kuenen JG: Polythionate degradation by tetrathionate hydrolase of Thiobacillus ferrooxidans. Microbiology 1997, 143(part 2):499-504.
  • [19]Rzhepishevska OI, Valdes J, Marcinkeviciene L, Gallardo CA, Meskys R, Bonnefoy V, Holmes DS, Dopson M: Regulation of a novel Acidithiobacillus caldus gene cluster involved in metabolism of reduced inorganic sulfur compounds. Appl Environ Microbiol 2007, 73(22):7367-7372.
  • [20]Gardner MN, Rawlings DE: Production of rhodanese by bacteria present in bio-oxidation plants used to recover gold from arsenopyrite concentrates. J Appl Microbiol 2000, 89(1):185-190.
  • [21]Yoch DC, Lindstrom ES: Survey of the photosynthetic bacteria for rhodanese (thiosulfate: cyanide sulfur transferase) activity. J Bacteriol 1971, 106(2):700-701.
  • [22]Valdés J, Pedroso I, Quatrini R, Holmes DS: Comparative genome analysis of Acidithiobacillus ferrooxidans.A. thiooxidans and A. caldus: Insights into their metabolism and ecophysiology. Hydrometallurgy 2008, 94(1–4):180-184.
  • [23]Quatrini R, Valdès J, Jedlicki E, Holmes DS: The Use Of Bioinformatics And Genome Biology To Advance Our Understanding Of Bioleaching Microorganisms. In Microbial Processing of Metal Sulfides. Edited by Quatrini R, Valdès J, Jedlicki E, Holmes DS. Berlin: Springer; 2007:221-239.
  • [24]Huang X, Zhao M, Liu W, Guan Y, Shi Y, Wang Q, Wu S, He M: Gigabase-scale transcriptome analysis on four species of pearl oysters. Mar Biotechnol 2013, 15(3):253-264.
  • [25]Delcher AL, Harmon D, Kasif S, White O, Salzberg SL: Improved microbial gene identification with GLIMMER. Nucleic Acids Res 1999, 27(23):4636-4641.
  • [26]Bedell JA, Korf I, Gish W: MaskerAid: a performance enhancement to RepeatMasker. Bioinformatics 2000, 16(11):1040-1041.
  • [27]Lagesen K, Hallin P, Rødland EA, Stærfeldt H, Rognes T, Ussery DW: RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007, 35(9):3100-3108.
  • [28]Lowe TM, Eddy SR: tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 2003, 25(5):955-964.
  • [29]Silverman MP, Lundgren DG: Studies on the chemoautotrophic iron bacterium Ferrobacillus ferrooxidans: An improved medium and a harvesting procedure for securing high cell yields. J Bacteriol 1959, 77(5):642-647.
  • [30]Ramírez P, Guiliani N, Valenzuela L, Beard S, Jerez CA: Differential protein expression during growth of Acidithiobacillus ferrooxidans on ferrous iron, sulfur compounds, or metal sulfides. Appl Environ Microbiol 2004, 70(8):4491-4498.
  • [31]Simms D, Cizdziel P, Chomczynski P: TRIzolTM: A new reagent for optimal single-step isolation of RNA. Focus 1993, 15(4):99-102.
  • [32]Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 2001, 25(4):402-408.
  • [33]Suzuki I: Oxidation of inorganic sulfur compounds: chemical and enzymatic reactions. Can J Microbiol 1999, 45(2):97-105.
  • [34]Zhang L, Liu X, Liu J, Zhang Z: Characteristics and function of sulfur dioxygenase in echiuran worm Urechis unicinctus. PLoS One 2013, 8(12):e81885.
  • [35]Bugaytsova Z, Lindström EB: Localization, purification and properties of a tetrathionate hydrolase from Acidithiobacillus caldus. Eur J Biochem 2004, 271(2):272-280.
  • [36]Wodara C, Kostka S, Egert M, Kelly DP, Friedrich CG: Identification and sequence analysis of the soxB gene essential for sulfur oxidation of Paracoccus denitrificans GB17. J Bacteriol 1994, 176(20):6188-6191.
  • [37]Beller HR, Chain PSG, Letain TE, Chakicherla A, Larimer FW, Richardson PM, Coleman MA, Wood AP, Kelly DP: The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J Bacteriol 2006, 188(4):1473-1488.
  • [38]Kletzin A: Molecular characterization of the sor gene, which encodes the sulfur oxygenase/reductase of the thermoacidophilic Archaeum Desulfurolobus ambivalens. J Bacteriol 1992, 174(18):5854-5859.
  • [39]He Z, Li Y, Zhou P, Liu S: Cloning and heterologous expression of a sulfur oxygenase/reductase gene from the thermoacidophilic archaeon Acidianus sp. S5 in Escherichia coli. FEMS Microbiol Lett 2000, 193(2):217-221.
  • [40]Pelletier N, Leroy G, Guiral M, Giudici-Orticoni M, Aubert C: First characterisation of the active oligomer form of sulfur oxygenase reductase from the bacterium Aquifex aeolicus. Extremophiles 2008, 12(2):205-215.
  • [41]Chen ZW, Liu YY, Wu JF, She Q, Jiang CY, Liu SJ: Novel bacterial sulfur oxygenase reductases from bioreactors treating gold-bearing concentrates. Appl Microbiol Biotechnol 2007, 74(3):688-698.
  • [42]Kletzin A: Coupled enzymatic production of sulfite, thiosulfate, and hydrogen sulfide from sulfur: purification and properties of a sulfur oxygenase reductase from the facultatively anaerobic archaebacterium Desulfurolobus ambivalens. J Bacteriol 1989, 171(3):1638-1643.
  • [43]Kletzin A, Urich T, Müller F, Bandeiras TM, Gomes CM: Dissimilatory oxidation and reduction of elemental sulfur in thermophilic archaea. J Bioenerg Biomembr 2004, 36(1):77-91.
  • [44]Emmel T, Sand W, König WA, Bock E: Evidence for the existence of a sulphur oxygenase in Sulfolobus brierleyi. Microbiology 1986, 132(12):3415-3420.
  • [45]Li M, Chen Z, Zhang P, Pan X, Jiang C, An X, Liu S, Chang W: Crystal structure studies on sulfur oxygenase reductase from Acidianus tengchongensis. Biochem Biophys Res Commun 2008, 369(3):919-923.
  • [46]Urich T, Bandeiras TM, LEAL SS, Rachel R, Albrecht T, Zimmermann P, Scholz C, Teixeira M, Gomes CM, Kletzin A: The sulphur oxygenase reductase from Acidianus ambivalens is a multimeric protein containing a low-potential mononuclear non-haem iron centre. Biochem J 2004, 381:137-146.
  • [47]Urich T, Kroke A, Bauer C, Seyfarth K, Reuff M, Kletzin A: Identification of core active site residues of the sulfur oxygenase reductase from Acidianus ambivalens by site-directed mutagenesis. FEMS Microbiol Lett 2005, 248(2):171-176.
  • [48]Valdes J, Quatrini R, Hallberg K, Dopson M, Valenzuela PDT, Holmes DS: Draft genome sequence of the extremely acidophilic bacterium Acidithiobacillus caldus ATCC 51756 reveals metabolic versatility in the genus Acidithiobacillus. J Bacteriol 2009, 191(18):5877-5878.
  • [49]Valdes J, Ossandon F, Quatrini R, Dopson M, Holmes DS: Draft genome sequence of the extremely acidophilic biomining bacterium Acidithiobacillus thiooxidans ATCC 19377 provides insights into the evolution of the Acidithiobacillus genus. J Bacteriol 2011, 193(24):7003-7004.
  • [50]Chen Z, Jiang C, She Q, Liu S, Zhou P: Key role of cysteine residues in catalysis and subcellular localization of sulfur oxygenase-reductase of Acidianus tengchongensis. Appl Environ Microbiol 2005, 71(2):621-628.
  • [51]Urich T, Gomes CM, Kletzin A, Frazão C: X-ray structure of a self-compartmentalizing sulfur cycle metalloenzyme. Science 2006, 311(5763):992-996.
  • [52]Urich T, Coelho R, Kletzina A, Frazao C: The sulfur oxygenase reductase from Acidianus ambivalens is an icosatetramer as shown by crystallization and Patterson analysis. BBA-Proteins Proteomics 2005, 1747(2):267-270.
  • [53]Schilling CH, Palsson BO: Assessment of the metabolic capabilities of Haemophilus influenzae Rd through a genome-scale pathway analysis. J Theor Biol 2000, 203(3):249-283.
  • [54]Müller FH, Bandeiras TM, Urich T, Teixeira M, Gomes CM, Kletzin A: Coupling of the pathway of sulphur oxidation to dioxygen reduction: characterization of a novel membrane-bound thiosulphate:quinone oxidoreductase. Mol Microbiol 2004, 53(4):1147-1160.
  • [55]Tano T, Kitaguchi H, Harada M, Nagasawa T, Sugio T: Purification and some properties of a tetrathionate decomposing enzyme from Thiobacillus thiooxidans. Biosci Biotechnol Biochem 1996, 60:224-227.
  • [56]Meyer B, Imhoff JF, Kuever J: Molecular analysis of the distribution and phylogeny of the soxB gene among sulfur-oxidizing bacteria – evolution of the Sox sulfur oxidation enzyme system. Environ Microbiol 2007, 9(12):2957-2977.
  • [57]Ghosh W, Mallick S, DasGupta SK: Origin of the Sox multienzyme complex system in ancient thermophilic bacteria and coevolution of its constituent proteins. Res Microbiol 2009, 160(6):409-420.
  • [58]Brasseur G, Levican G, Bonnefoy V, Holmes D, Jedlicki E, Lemesle-Meunier D: Apparent redundancy of electron transfer pathways via bc1 complexes and terminal oxidases in the extremophilic chemolithoautotrophic Acidithiobacillus ferrooxidans. Biochim Biophys Acta-Bioenerg 2004, 1656(2–3):114-126.
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