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Iron and sulfur oxidation pathways of Acidithiobacillus ferrooxidans

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Abstract

Acidithiobacillus ferrooxidans is a gram-negative, autotrophic and rod-shaped bacterium. It can gain energy through the oxidation of Fe(II) and reduced inorganic sulfur compounds for bacterial growth when oxygen is sufficient. It can be used for bio-leaching and bio-oxidation and contributes to the geobiochemical circulation of metal elements and nutrients in acid mine drainage environments. The iron and sulfur oxidation pathways of A. ferrooxidans play key roles in bacterial growth and survival under extreme circumstances. Here, the electrons transported through the thermodynamically favourable pathway for the reduction to H2O (downhill pathway) and against the redox potential gradient reduce to NAD(P)(H) (uphill pathway) during the oxidation of Fe(II) were reviewed, mainly including the electron transport carrier, relevant operon and regulation of its expression. Similar to the electron transfer pathway, the sulfur oxidation pathway of A. ferrooxidans, related genes and operons, sulfur oxidation mechanism and sulfur oxidase system are systematically discussed.

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References

  • Abergel C, Nitschke W, Malarte G, Bruschi M, Claverie JM, Giudiciorticoni MT (2003) The structure of Acidithiobacillus ferrooxidans c(4)-cytochrome: a model for complex-induced electron transfer tuning. Structure 11:547–555. https://doi.org/10.1016/s0969-2126(03)00072-8

    Article  CAS  PubMed  Google Scholar 

  • Agnès A, Céline BA, Barrie D, Violaine J, Hallberg KB (2011) Phylogenetic and genetic variation among Fe(II)-oxidizing acidithiobacilli supports the view that these comprise multiple species with different ferrous iron oxidation pathways. Microbiology 157:111–122

    Google Scholar 

  • Ai C, Liang Y, Miao B, Chen M, Zeng W, Qiu G (2018) Identification and analysis of a novel gene cluster involves in Fe2+ oxidation in Acidithiobacillus ferrooxidans ATCC 23270, a typical biomining acidophile. Curr Microbiol 75:818. https://doi.org/10.1007/s00284-018-1453-9

    Article  CAS  PubMed  Google Scholar 

  • Alcaraz LA, Donaire A (2010) Unfolding process of rusticyanin: evidence of protein aggregation. Eur J Biochem 271:4284–4292. https://doi.org/10.1111/j.1432-1033.2004.04368

    Article  Google Scholar 

  • Almárcegui RJ, Navarro CA, Paradela A, Albar JP, Von BD, Jerez CA (2014) Response to copper of Acidithiobacillus ferrooxidans ATCC 23270 grown in elemental sulfur. Res Microbiol 165:761–772. https://doi.org/10.1016/j.resmic.2014.07.005

    Article  CAS  PubMed  Google Scholar 

  • Amouric A, Appia-Ayme C, Yarzabal A, Bonnefoy V (2009) Regulation of the iron and sulfur oxidation pathways in the acidophilic Acidithiobacillus Ferrooxidans. Adv Mater Res 71–73:163–166

    Google Scholar 

  • Amouric A, Brochierarmanet C, Johnson DB, Bonnefoy V, Hallberg KB (2011) Phylogenetic and genetic variation among Fe(II)-oxidizing acidithiobacilli supports the view that these comprise multiple species with different ferrous iron oxidation pathways. Microbiology 157:111–122. https://doi.org/10.1099/mic.0.044537-0

    Article  CAS  PubMed  Google Scholar 

  • Appiaayme C, Guiliani N, Ratouchniak J, Bonnefoy V (1999) Characterization of an operon encoding two c-type cytochromes, an aa3-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020. Appl Environ Microbiol 65:4781–4787

    CAS  Google Scholar 

  • Appiaayme C, Bengrine A, Cavazza C, Giudiciorticoni MT, Bruschi M, Chippaux M, Bonnefoy V (2010) Characterization and expression of the co-transcribed cyc1 and cyc2 genes encoding the cytochrome c4 (c552) and a high-molecular-mass cytochrome c from Thiobacillus ferrooxidans ATCC 33020. Fems Microbiol Lett 167:171–177. https://doi.org/10.1016/S0378-1097(98)00385-1

    Article  Google Scholar 

  • Barrett ML et al (2006) Atomic resolution crystal structures, EXAFS, and quantum chemical studies of rusticyanin and its two mutants provide insight into its unusual properties. Biochemistry 45:2927–2939. https://doi.org/10.1021/bi052372w

    Article  CAS  PubMed  Google Scholar 

  • Bonnefoy V, Grail BM, Johnson DB (2018) Salt stress-induced loss of iron oxido-reduction activities and re-acquisition of this phenotype depend on the rus operon transcription in Acidithiobacillus ferridurans. Appl Environ Microbiol 84:e02795–02817. https://doi.org/10.1128/AEM.02795-17

    Article  PubMed  PubMed Central  Google Scholar 

  • Bouchal P, Zdrahal Z, Helanova S, Janiczek O, Hallberg KB, Mandl M (2010) Proteomic and bioinformatic analysis of iron- and sulfur-oxidizing Acidithiobacillus ferrooxidans using immobilized pH gradients mass spectrometry. Proteomics 6:4278–4285. https://doi.org/10.1002/pmic.200500719

    Article  CAS  Google Scholar 

  • Brasseur G, Bruscella P, Bonnefoy V, Lemesle-Meunier D (2002) The bc1 complex of the iron-grown acidophilic chemolithotrophic bacterium Acidithiobacillus ferrooxidans functions in the reverse but not in the forward direction: is there a second bc1 complex? Biochim Biophys Acta Bioenerg 1555:37–43. https://doi.org/10.1016/S0005-2728(02)00251-7

    Article  CAS  Google Scholar 

  • Breed AW, Dempers CJ, Searby GE, Gardner MN, Rawlings DE, Hansford GS (2015) The effect of temperature on the continuous ferrous-iron oxidation kinetics of a predominantly Leptospirillum ferrooxidans culture. Biotechnol Bioeng 65:44–53. https://doi.org/10.1002/(SICI)1097-0290(19991005)65:1%3C44::AID-BIT6%3E3.0.CO;2-V

    Article  Google Scholar 

  • Brito JA et al (2009) Structural and functional insights into sulfide: quinone oxidoreductase. Biochemistry 48:5613. https://doi.org/10.1021/bi9003827

    Article  CAS  PubMed  Google Scholar 

  • Bruscella P, Appia-Ayme C, Levicã nG, Ratouchniak J, Jedlicki E, Holmes DS, Bonnefoy V (2007) Differential expression of two bc1 complexes in the strict acidophilic chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans suggests a model for their respective roles in iron or sulfur oxidation. Microbiology 153:102–110. https://doi.org/10.1099/mic.0.2006/000067-0

    Article  CAS  PubMed  Google Scholar 

  • Bryan CG, Davis-Belmar CS, Van WN, Fraser MK, Dew D, Rautenbach GF, Harrison STL (2012) The effect of CO2 availability on the growth, iron oxidation and CO2-fixation rates of pure cultures of Leptospirillum ferriphilum and Acidithiobacillus ferrooxidans. Biotechnol Bioeng 109:1693–1703. https://doi.org/10.1002/bit.24453

    Article  CAS  PubMed  Google Scholar 

  • Casimiro DR, Toy-Palmer A, Dyson HJ (1995) Gene synthesis, high-level expression, and mutagenesis of Thiobacillus ferrooxidans rusticyanin: His 85 is a ligand to the blue copper center. Biochemistry 34:6640. https://doi.org/10.1021/bi00020a009

    Article  CAS  PubMed  Google Scholar 

  • Castelle C, Guiral M, Malarte G, Ledgham F, Leroy G, Brugna M, Giudiciorticoni MT (2008) New iron-oxidizing/O2-reducing supercomplex spanning both inner and outer membranes, isolated from the extreme acidophile Acidithiobacillus ferrooxidans. J Biol Chem 283:25803–25811. https://doi.org/10.1074/jbc.M802496200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavazza C, Giudici-Orticoni MT, Nitschke W, Appia C, Bonnefoy V, Bruschi M (2010) Characterisation of a soluble cytochrome c4 isolated from Thiobacillus ferrooxidans. Eur J Biochem 242:308–314. https://doi.org/10.1111/j.1432-1033.1996.0308r.x

    Article  Google Scholar 

  • Ccorahuasanto R, Eca A, Abanto M, Guerra G, Ramírez P (2017) Physiological and comparative genomic analysis of Acidithiobacillus ferrivorans PQ33 provides psychrotolerant fitness evidence for oxidation at low temperature. Res Microbiol 168:482–492. https://doi.org/10.1016/j.resmic.2017.01.007

    Article  CAS  Google Scholar 

  • Chen P, Yan L, Wang Q, Li H (2013) Arsenic precipitation in the bioleaching of realgar using Acidithiobacillus ferrooxidans. J Appl Chem 2013:1–5

    Google Scholar 

  • Cheng J (2008) Sulfur-oxidation related doxDA operons in Acidithiobacillus ferrooxidans. Microbiology 35:1155–1170

    Google Scholar 

  • Cherney MM, Zhang Y, Solomonson M, Weiner JH, James MNG (2010) Crystal structure of sulfide: quinone oxidoreductase from Acidithiobacillus ferrooxidans: insights into sulfidotrophic respiration and detoxification. J Mol Biol 398:292–305

    CAS  PubMed  Google Scholar 

  • Chi A, Valenzuela L, Beard S, Mackey AJ, Shabanowitz J, Hunt DF, Jerez CA (2007) Periplasmic proteins of the extremophile Acidithiobacillus ferrooxidans: a high throughput proteomics analysis. Mol Cell Proteom 6:2239–2251

    CAS  Google Scholar 

  • Colmer AR, Hinkle ME (1947) The role of microorganisms in acid mine drainage: a preliminary report. Science 106(2751):253–256

    CAS  PubMed  Google Scholar 

  • Ferguson SJ, Ingledew WJ (2008) Energetic problems faced by micro-organisms growing or surviving on parsimonious energy sources and at acidic pH: I. Acidithiobacillus ferrooxidans as a paradigm. Biochim Biophys Acta Bioenerg 1777:1471–1479

    CAS  Google Scholar 

  • Findlay AJ, Kamyshny A (2017) Turnover rates of intermediate sulfur species (Sx 2–, S0, S2O3 2–, S4O6 2–, SO3 2–) in anoxic freshwater and sediments. Front Microbiol 8:2551–2566

    PubMed  PubMed Central  Google Scholar 

  • Giudici-Orticoni MT, Leroy G, Nitschke W, Bruschi M (2000) Characterization of a new dihemic c(4)-type cytochrome isolated from Thiobacillus ferrooxidans. Biochemistry 39:7205–7211

    CAS  PubMed  Google Scholar 

  • González-Arribas E, Falk M, Aleksejeva O, Bushnev S, Sebastián P, Feliu JM, Shleev S (2018) A conventional symmetric biosupercapacitor based on rusticyanin modified gold electrodes. J Electroanal Chem 816:253–258

    Google Scholar 

  • Harahuc L, Suzuki I (2001) Sulfite oxidation by iron-grown cells of Thiobacillus ferrooxidans at pH 3 possibly involves free radicals, iron, and cytochrome oxidase. Can J Microbiol 47:424–430

    CAS  PubMed  Google Scholar 

  • He H, Xia J, Huang G, Jiang HC, Tao XX, Zhao YD, He W (2011) Analysis of the elemental sulfur bio-oxidation by Acidithiobacillus ferrooxidans with sulfur K-edge XANES. World J Microbiol Biotechnol 27:1927–1931

    CAS  Google Scholar 

  • He S, Barco RA, Emerson D, Roden EE (2017) Comparative genomic analysis of neutrophilic iron(II) oxidizer genomes for candidate genes in extracellular electron transfer. Front Microbiol 8:1584–1601

    PubMed  PubMed Central  Google Scholar 

  • Hedrich S, Schlömann M, Johnson DB (2011) The iron-oxidizing proteobacteria. Microbiology 157:1551–1564

    CAS  PubMed  Google Scholar 

  • Hirose T, Suzuki H, Inagaki K, Tanaka H, Tano T, Sugio T (2014) Inhibition of sulfur use by sulfite ion in Thiobacillus ferrooxidans. J Agric Chem Soc Japan 55:2479–2484

    Google Scholar 

  • Holmes DS, Bonnefoy V (2007) Genetic and bioinformatic insights into iron and sulfur oxidation mechanisms of bioleaching organisms. Springer, Heidelberg

    Google Scholar 

  • Ilbert M, Bonnefoy V (2013) Insight into the evolution of the iron oxidation pathways. Biochim Biophys Acta Bioenerg 1827:161–175

    CAS  Google Scholar 

  • Jiang CY, Liu LJ, Guo X, You XY, Liu SJ, Poetsch A (2014) Resolution of carbon metabolism and sulfur-oxidation pathways of Metallosphaera cuprina Ar-4 via comparative proteomics. J Proteom 109:276–289

    CAS  Google Scholar 

  • Jonas P, Fabian M, Karin L, Bastian N, Reinhard M, Friedrich L, Arnulf K (2011) An extracellular tetrathionate hydrolase from the thermoacidophilic archaeon Acidianus Ambivalens with an activity optimum at pH 1. Front Microbiol 2:68–80

    Google Scholar 

  • Jong GAHD, Hazeu W, Bos P, Kuenen JG (2010) Isolation of the tetrathionate hydrolase from Thiobacillus Acidophilus. Fed Eur Biochem Soc 243:678–683

    Google Scholar 

  • Kanao T et al (2013) Crystallization and preliminary X-ray diffraction analysis of tetrathionate hydrolase from Acidithiobacillus ferrooxidans. Acta Crystallogr A 69:692–694

    CAS  Google Scholar 

  • Kanbi LD, Antonyuk S, Hough MA, Hall JF, Dodd FE, Hasnain SS (2002) Crystal structures of the Met148Leu and Ser86Asp mutants of rusticyanin from Thiobacillus ferrooxidans: insights into the structural relationship with the cupredoxins and the multi copper proteins. J Mol Biol 320:263–275

    CAS  PubMed  Google Scholar 

  • Kato S (2015) Biotechnological aspects of microbial extracellular electron transfer. Microb Environ 30:133–139

    Google Scholar 

  • Klatt JM, Polerecky L (2015) Assessment of the stoichiometry and efficiency of CO2 fixation coupled to reduced sulfur oxidation. Front Microbiol 6:484–503

    PubMed  PubMed Central  Google Scholar 

  • Kucera J, Pakostova E, Janiczek O, Mandl M (2015) Changes in Acidithiobacillus ferrooxidans ability to reduce ferric iron by elemental sulfur. Adv Mater Res 1130:97–100

    Google Scholar 

  • Kucera J, Pakostova E, Lochman J, Janiczek O, Mandl M (2016a) Are there multiple mechanisms of anaerobic sulfur oxidation with ferric iron in Acidithiobacillus ferrooxidans? Res Microbiol 167:357–366

    CAS  PubMed  Google Scholar 

  • Kucera J, Sedo O, Potesil D, Janiczek O, Zdrahal Z, Mandl M (2016b) Comparative proteomic analysis of sulfur-oxidizing Acidithiobacillus ferrooxidans CCM 4253 cultures having lost the ability to couple anaerobic elemental sulfur oxidation with ferric iron reduction. Res Microbiol 167:587–594

    CAS  PubMed  Google Scholar 

  • Kucera J, Janiczek O, Smoldas J, Mandl M (2017) Proteins binding to immobilized rusticyanin detected by affinity chromatography. Solid State Phenom 262:344–349

    Google Scholar 

  • Levican G, Bonnefoy V, Holmes D, Jedlicki E, Lemesle-Meunier D (2004) Apparent redundancy of electron transfer pathways via bc(1) complexes and terminal oxidases in the extremophilic chemolithoautotrophic Acidithiobacillus ferrooxidans. Biochimica Biophysica Acta Bioenerg 1656:114–126

    Google Scholar 

  • Levicán G, Bruscella P, Guacunano M, Inostroza C, Bonnefoy V, Holmes DS, Jedlicki E (2002) Characterization of the petI and res operons of Acidithiobacillus ferrooxidans. J Bacteriol 184:1498–1501

    PubMed  PubMed Central  Google Scholar 

  • Li Y, Li H (2014) Type IV pili of Acidithiobacillus ferrooxidans can transfer electrons from extracellular electron donors. J Basic Microbiol 54:226–231

    CAS  PubMed  Google Scholar 

  • Liu W, Lin J, Pang X, Cui S, Mi S, Lin J (2010) Overexpression of rusticyanin in Acidithiobacillus ferrooxidans ATCC19859 increased Fe(II) oxidation activity. Curr Microbiol 62:320–324

    PubMed  Google Scholar 

  • Liu H et al (2011) The co-culture of Acidithiobacillus ferrooxidans and Acidiphilium acidophilum enhances the growth, iron oxidation, and CO2 fixation. Arch Microbiol 193:857–866

    CAS  PubMed  Google Scholar 

  • Liu J, Qian L, Zheng C (2013a) Biogenesis and transfer of iron-sulfur clusters from Acidithiobacillus ferrooxidans. In: International biohydrometallurgy symposium pp 198–201

  • Liu Y, Guo S, Yu R, Ji J, Qiu G (2013b) HdrC2 from Acidithiobacillus ferrooxidans owns two iron-sulfur binding motifs but binds only one variable cluster between [4Fe-4S] and [3Fe-4S]. Curr Microbiol 66:88–95

    PubMed  Google Scholar 

  • Liu W, Lin J, Pang X, Mi S, Cui S, Lin J (2014a) Increases of ferrous iron oxidation activity and arsenic stressed cell growth by overexpression of Cyc2 in Acidithiobacillus ferrooxidans ATCC19859. Biotechnol Appl Biochem 60:623–628

    Google Scholar 

  • Liu Y, Guo S, Yu R, Zou K, Qiu G (2014b) A new cytoplasmic monoheme cytochrome c from Acidithiobacillus ferrooxidans involved in sulfur oxidation. Curr Microbiol 68:285–292

    CAS  PubMed  Google Scholar 

  • Luo H, Shen L, Yin H, Li Q, Chen Q, Luo Y, Liao L, Qiu G, Liu X (2009) Comparative genomic analysis of Acidithiobacillus ferrooxidans strains using the A. ferrooxidans ATCC 23270 whole-genome oligonucleotide microarray Canadian. J Microbiol 55:587–598

    CAS  Google Scholar 

  • Maluckov BS, Mitrić MN (2018) Electrochemical behavior of pyrite in sulfuric acid in presence of amino acids belonging to the amino acid sequence of rusticyanin. Bioelectrochemistry 123:112–118

    CAS  PubMed  Google Scholar 

  • Mangold S, Valdés J, Holmes DS, Dopson M (2011) Sulfur metabolism in the extreme acidophile Acidithiobacillus Caldus. Front Microbiol 2:17–35

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mei K, Nogami S, Kanao T, Takada J, Kamimura K (2013) Tetrathionate-forming thiosulfate dehydrogenase from the acidophilic, chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans. Appl Environ Microbiol 79:113–120

    Google Scholar 

  • Mo H et al (2011) Ferric reductase activity of the ArsH protein from Acidithiobacillus ferrooxidans. J Microbiol Biotechnol 21:464–469

    CAS  PubMed  Google Scholar 

  • Moinier D, Byrne D, Amouric AS, Bonnefoy V (2013) How the RegBA Redox responding system controls iron and sulfur oxidation in Acidithiobacillus ferrooxidans. Adv Mater Res 825:186–189

    Google Scholar 

  • Moinier D, Byrne D, Amouric A, Bonnefoy V (2017) The Global redox responding RegB/RegA signal transduction system regulates the genes involved in ferrous iron and inorganic sulfur compound oxidation of the acidophilic Acidithiobacillus ferrooxidans. Front Microbiol 8:1277–1293

    PubMed  PubMed Central  Google Scholar 

  • Morton NM et al (2016) Genetic identification of thiosulfate sulfurtransferase as an adipocyte-expressed antidiabetic target in mice selected for leanness. Nat Med 22:771–779

    CAS  PubMed  PubMed Central  Google Scholar 

  • Navarro CA, Von BD, MartãNez-Bussenius C, Castillo RA, Jerez CA (2016) Cytoplasmic CopZ-Like protein and periplasmic rusticyanin and AcoP proteins as possible copper resistance determinants in Acidithiobacillus ferrooxidans ATCC 23270. Appl Environ Microbiol 82:1015–1022

    CAS  PubMed  PubMed Central  Google Scholar 

  • Neale C, Bennett WF, Tieleman DP, Pomès R (2011) Statistical convergence of equilibrium properties in simulations of molecular solutes embedded in lipid bilayers. J Chem Theory Comput 7:4175–4189

    CAS  PubMed  Google Scholar 

  • Norris PR, Laigle L, Slade S (2018) Cytochromes in anaerobic growth of. Acidithiobacillus ferrooxidans. Microbiology 164:383–394

    CAS  PubMed  Google Scholar 

  • Oetiker N et al (2018) Possible role ofenvelope components in the extreme copper resistance of the biomining Acidithiobacillus ferrooxidans. Genes 9:347–362

    PubMed Central  Google Scholar 

  • Ouyang J, Chen X (2009) Reserch progresses in ferrous oxidation system of Acidithiobacillus ferrooxidans. Biotechnol Bull 19:46–49

    Google Scholar 

  • Ouyang J, Guo W, Li B, Li G, Zhang H, Chen X (2013) Proteomic analysis of differential protein expression in Acidithiobacillus ferrooxidans cultivated in high potassium concentration. Microbiol Res 168:455–460

    CAS  PubMed  Google Scholar 

  • Pakostova E, Mandl M, Pokorna BO, Diviskova E, Lojek A (2013) Cellular ATP changes in Acidithiobacillus ferrooxidans cultures oxidizing ferrous iron and elemental sulfur. Geomicrobiol J 30:1–7

    CAS  Google Scholar 

  • Panyushkina AE, Tsaplina IA, Kondrat’Eva TF, Belyi AV, Bulaev AG (2018) Physiological and morphological characteristics of acidophilic bacteria Leptospirillum ferriphilum and Acidithiobacillus thiooxidans, members of a chemolithotrophic. Microb Consort Microbiol 87:326–338

    CAS  Google Scholar 

  • Paulino LC, de Mello MP, Ottoboni LM (2015) Differential gene expression in response to copper in Acidithiobacillus ferrooxidans analyzed by RNA arbitrarily primed polymerase chain reaction. Electrophoresis 23:520–527

    Google Scholar 

  • Pyne P, Alam M, Rameez MJ, Mandal S, Sar A, Mondal N, Debnath U, Mathew B, Misra AK (2018) Homologs from sulfur oxidation (Sox) and methanol dehydrogenation (Xox) enzyme systems collaborate to give rise to a novel pathway of chemolithotrophic tetrathionate oxidation. Mol Microbiol 109:1–23

    Google Scholar 

  • Qian L, Zheng C, Liu J (2013) Characterization of iron-sulfur cluster assembly protein IscA from Acidithiobacillus ferrooxidans. Biochemistry 78:244–251

    CAS  PubMed  Google Scholar 

  • Quatrini R et al (2006) Insights into the iron and sulfur energetic metabolism of Acidithiobacillus ferrooxidans by microarray transcriptome profiling. Hydrometallurgy 83:263–272

    CAS  Google Scholar 

  • Quatrini R, Appia-Ayme C, Denis Y, Jedlicki E, Holmes DS, Bonnefoy V (2009) Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans. BMC Genom 10:394–413. https://doi.org/10.1186/1471-2164-10-394

    Article  CAS  Google Scholar 

  • Ramírez P, Guiliani N, Valenzuela L, Beard S, Jerez CA (2004) Differential protein expression during growth of Acidithiobacillus ferrooxidans on ferrous iron, sulfur compounds or metal sulfides. Appl Environ Microbiol 70:4491–4498

    PubMed  PubMed Central  Google Scholar 

  • Robin S, Arese M, Forte E, Sarti P, Kolaj-Robin O, Giuffrè A, Soulimane T (2014) Functional dissection of the multi-domain di-heme ctochrome c550 from Thermus thermophilus. PLoS ONE 8:e55129–e55140

    Google Scholar 

  • Santana MM, Gonzalez JM, Clara MI (2016) Inferring pathways leading to organic-sulfur mineralization in the Bacillales. Crit Rev Microbiol 42:1–15

    Google Scholar 

  • Song JL, Jiang CY, Liu SJ (2015) Insight into the sulfur metabolism by thermoacidophilic archaeon Metallosphaera cuprina with genomic, proteomic and biochemical tools. Adv Mater Res 1130:145–148

    Google Scholar 

  • Sugio T, Tano T, Imai K (2006) Isolation and some properties of two kinds of cytochrome c oxidase from iron-grown Thiobacillus ferrooxidans. J Agric Chem Soc Jpn 45:1791–1799

    Google Scholar 

  • Sugio T, Taha TM, Kanao T, Takeuchi F (2007) Increase in Fe2+-Producing activity during growth of Acidithiobacillus ferrooxidans ATCC23270 on Sulfur. J Agric Chem Soc Jpn 71:2663–2669

    CAS  Google Scholar 

  • Sugio T, Ako A, Takeuchi F (2010) Sulfite oxidation catalyzed by aa(3)-type cytochrome c oxidase in Acidithiobacillus ferrooxidans. J Agric Chem Soc Jpn 74:2242–2247

    CAS  Google Scholar 

  • Sugio T, Fujii M, Ninomiya Y, Kanao T, Negishi A, Takeuchi F (2014a) Reduction of Hgwith reduced mammalian cytochrome by cytochrome oxidase purified from a mercury-resistant strain, MON-1. Biosci Biotechnol Biochem 72:1756–1763

    Google Scholar 

  • Sugio T, Taha TM, Kanao T, Takeuchi F (2014b) Increase in Fe-producing activity during growth of ATCC23270 on sulfur. Biosci Biotechnol Biochem. https://doi.org/10.1271/bbb.70253

    Article  Google Scholar 

  • Sun J, Yu RL, Miao L, Zhong DL, Liu J, Gu GH (2011) Electrochemical mechanism of rusticyanin (Rus.) isolated from A. ferrooxidans measured by Rus.-ZnS-QDs/L-Cys/Au electrode. J Cent South Univ 18(5):1389–1394

    CAS  Google Scholar 

  • Taha MTM (2009) Involvement of iron oxidation- and iron-reduction-enzyme systems in sulfur oxidation of iron-oxidizing bacterium Acidithiobacillus ferrooxidans. China Occup Med 27:3892–3895

    Google Scholar 

  • Taha TM, Kanao T, Takeuchi F, Sugio T (2007) Involvement of ironoxidation enzyme system in sulfur oxidation of Acidithiobacillus ferrooxidans ATCC 23270. Adv Mater Res 20–21:443–446

    Google Scholar 

  • Tu Z, Guo C, Zhang T, Lu G, Wan J, Liao C, Dang Z (2017) Investigation of intermediate sulfur species during pyrite oxidation in the presence and absence of Acidithiobacillus ferrooxidans. Hydrometallurgy 167:58–65

    CAS  Google Scholar 

  • Valdés J et al (2008) Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genom 9:597–597

    Google Scholar 

  • Violaine B, Holmes DS (2012) Genomic insights into microbial iron oxidation and iron uptake strategies in extremely acidic environments. Environ Microbiol 14:1597–1611

    Google Scholar 

  • Walter RL, Ealick SE, Friedman AM, Proctor P, Shoham M (1996) Multiple wavelength anomalous diffraction (MAD) crystal structure of rusticyanin: a highly oxidizing cupredoxin with extreme acid stability. J Mol Biol 263:730–751

    CAS  PubMed  Google Scholar 

  • Wang H, Liu S, Liu X, Li X, Wen Q, Lin J (2014) Identification and characterization of an ETHE1-like sulfur dioxygenase in extremely acidophilic Acidithiobacillus spp. Appl Microbiol Biotechnol 98:7511–7522

    CAS  PubMed  Google Scholar 

  • White GF, Edwards MJ, Gomez-Perez L, Richardson DJ, Butt JN, Clarke TA (2016) Chapter three-mechanisms of bacterial extracellular electron exchange. Adv Microb Physiol 68:87–138

    CAS  PubMed  Google Scholar 

  • Wu X, Liu L, Zhang Z, Deng F, Liu X (2014) Phylogenetic and genetic characterization of Acidithiobacillus strains isolated from different environments. World J Microbiol Biotechnol 30:3197–3209

    PubMed  Google Scholar 

  • Yarzã bA, Appia-Ayme C, Ratouchniak J, Bonnefoy V (2004) Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c a cytochrome oxidase rusticyanin. Microbiology 150:2113–2123

    Google Scholar 

  • Yarzábal A, Brasseur G, Bonnefoy V (2002a) Cytochromes c of Acidithiobacillus ferrooxidans. Fems Microbiol Lett 209:189–195

    PubMed  Google Scholar 

  • Yarzábal A, Brasseur G, Ratouchniak J, Lund K, Lemeslemeunier D, Demoss JA, Bonnefoy V (2002b) The high-molecular-weight cytochrome c Cyc2 of Acidithiobacillus ferrooxidans is an outer membrane protein. J Bacteriol 184:313

    PubMed  PubMed Central  Google Scholar 

  • Yu Y (2010) Isolation and characterization of the petII promoter of Acidithiobacillus ferrooxidans. J Bacteriol 196:2255–2264

    Google Scholar 

  • Zeng J, Geng M, Liu Y, Zhao W, Xia L, Liu J, Qiu G (2007) Expression, purification and molecular modelling of the Iro protein from Acidithiobacillus ferrooxidans Fe-1 Protein. Exp Purifi 52:146–152

    CAS  Google Scholar 

  • Zhan Q, Ding Z, Cui L, Fan J, Wang W, Liu H (2016) Identification, characterization and expression of NK-lysin in Megalobrama amblycephala. J Fish China 40:1145–1155

    Google Scholar 

  • Zhang Y, Yang Y, Liu J, Qiu G (2013) Isolation and characterization of Acidithiobacillus ferrooxidans strain QXS-1 capable of unusual ferrous iron and. sulfur utilization. Hydrometallurgy 136:51–57

    Google Scholar 

  • Zhang Y, Cherney MM, Weiner JH (2014) P97 characterization, structure and mechanism of sulfide: quinone oxidoreductase (SQR) from Acidithiobacillus ferrooxidans. Nitric Oxide 39:45–57

    Google Scholar 

  • Zhang Y, Qadri A, Weiner JH (2015) The quinone-binding site of Acidithiobacillus ferrooxidans sulfide: quinone oxidoreductase controls both sulfide oxidation and quinone reduction. Biochem Cell Biol 94:1–12

    Google Scholar 

  • Zhang R, Wei D, Shen Y, Liu W, Lu T, Han C (2016) Catalytic effect of polyethylene glycol on sulfur oxidation in chalcopyrite bioleaching by Acidithiobacillus ferrooxidans. Miner Eng 95:74–78

    CAS  Google Scholar 

  • Zhang R, Hedrich S, Ostertag-Henning C, Schippers A (2018a) Effect of elevated pressure on ferric iron reduction coupled to sulfur oxidation by biomining microorganisms. Hydrometallurgy 178:215–223

    CAS  Google Scholar 

  • Zhang S, Yan L, Xing W, Chen P, Zhang Y, Wang W (2018b) Acidithiobacillus ferrooxidans and its potential application. Extremophiles 22:563–579

    CAS  PubMed  Google Scholar 

  • Zheng C et al (2009) Characterization and reconstitute of a [Fe4S4] adenosine 5′-phosphosulfate reductase from Acidithiobacillus ferrooxidans. Curr Microbiol 58:586–592

    CAS  PubMed  Google Scholar 

  • Zheng C et al (2018) Effects of cadmium exposure on expression of glutathione synthetase system genes in Acidithiobacillus ferrooxidans. Extremophiles 1–8:1431–0651

    Google Scholar 

  • Zhi-Guo HE, Yang YP, Zhou S, Yue-Hua HU, Zhong H (2014) Effect of pyrite, elemental sulfur and ferrous ions on EPS production by metal sulfide bioleaching microbes. Trans Nonferrous Met Soc China 24:1171–1178

    Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 41471201), Natural Science Foundation of Heilongjiang Province of China (Grant No. QC2014023), Longjiang Scholar Program of Heilongjiang Province (Grant No. Q201815). University Nursing Program for Young Scholars with Creative Talents in Heilongjiang Province (Grant No. UNPYSCT-2015086), Open Foundation of the Heilongjiang Provincial Key Laboratory of Environmental Microbiology and Recycling of Argo-Waste in Cold Region (Grant No. 201704), Research Innovation Program for Graduate Students of Heilongjiang Bayi Agricultural University (Grant No. YJSCX2017-Y63), Support Program of Scientific Research Team and Platform of HBAU (Grant No. TDJH201809) and Technology Program of Land Reclamation General Bureau of Heilongjiang (Grant No. HNK135-04-08).

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  1. Heilongjiang Provincial Key Laboratory of Environmental Microbiology and Recycling of Argo-Waste in Cold Region, College of Life Science and Biotechnology, Heilongjiang Bayi Agricultural University, 5 Xinfeng Road, Daqing, 163319, Heilongjiang Province, People’s Republic of China

    Yue Zhan, Mengran Yang, Shuang Zhang, Dan Zhao, Weidong Wang & Lei Yan

  2. School of Pharmacy, Lanzhou University, Donggang West Road No. 199, Lanzhou, 730020, Gansu Province, People’s Republic of China

    Jiangong Duan

  3. College of Food Science, Heilongjiang Bayi Agricultural University, 5 Xinfeng Road, Daqing, 163319, Heilongjiang Province, People’s Republic of China

    Lei Yan

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  1. Yue Zhan
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Correspondence to Lei Yan.

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Zhan, Y., Yang, M., Zhang, S. et al. Iron and sulfur oxidation pathways of Acidithiobacillus ferrooxidans. World J Microbiol Biotechnol 35, 60 (2019). https://doi.org/10.1007/s11274-019-2632-y

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