Advertisement

Iron and sulfur oxidation pathways of Acidithiobacillus ferrooxidans

  • Yue Zhan
  • Mengran Yang
  • Shuang Zhang
  • Dan Zhao
  • Jiangong Duan
  • Weidong Wang
  • Lei YanEmail author
Review
  • 159 Downloads

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.

Keywords

Acidithiobacillus ferrooxidans Iron and sulfur oxidation Electron transfer pathway Carrier and operon Regulation 

Notes

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).

References

  1. 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 CrossRefPubMedGoogle Scholar
  2. 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 157:111–122Google Scholar
  3. 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 CrossRefPubMedGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefPubMedGoogle Scholar
  6. 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 71–73:163–166Google Scholar
  7. 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 CrossRefPubMedGoogle Scholar
  8. 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 65:4781–4787Google Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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 CrossRefPubMedGoogle Scholar
  11. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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 CrossRefGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. Brito JA et al (2009) Structural and functional insights into sulfide: quinone oxidoreductase. Biochemistry 48:5613.  https://doi.org/10.1021/bi9003827 CrossRefPubMedGoogle Scholar
  16. 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 CrossRefPubMedGoogle Scholar
  17. 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 CrossRefPubMedGoogle Scholar
  18. 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 CrossRefPubMedGoogle Scholar
  19. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. Chen P, Yan L, Wang Q, Li H (2013) Arsenic precipitation in the bioleaching of realgar using Acidithiobacillus ferrooxidans. J Appl Chem 2013:1–5Google Scholar
  23. Cheng J (2008) Sulfur-oxidation related doxDA operons in Acidithiobacillus ferrooxidans. Microbiology 35:1155–1170Google Scholar
  24. 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 398:292–305PubMedGoogle Scholar
  25. 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 6:2239–2251Google Scholar
  26. Colmer AR, Hinkle ME (1947) The role of microorganisms in acid mine drainage: a preliminary report. Science 106(2751):253–256PubMedGoogle Scholar
  27. 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 1777:1471–1479Google Scholar
  28. 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 8:2551–2566PubMedPubMedCentralGoogle Scholar
  29. Giudici-Orticoni MT, Leroy G, Nitschke W, Bruschi M (2000) Characterization of a new dihemic c(4)-type cytochrome isolated from Thiobacillus ferrooxidans. Biochemistry 39:7205–7211PubMedGoogle Scholar
  30. 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 816:253–258Google Scholar
  31. 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 47:424–430PubMedGoogle Scholar
  32. 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 27:1927–1931Google Scholar
  33. 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 8:1584–1601PubMedPubMedCentralGoogle Scholar
  34. Hedrich S, Schlömann M, Johnson DB (2011) The iron-oxidizing proteobacteria. Microbiology 157:1551–1564PubMedGoogle Scholar
  35. 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 55:2479–2484Google Scholar
  36. Holmes DS, Bonnefoy V (2007) Genetic and bioinformatic insights into iron and sulfur oxidation mechanisms of bioleaching organisms. Springer, HeidelbergGoogle Scholar
  37. Ilbert M, Bonnefoy V (2013) Insight into the evolution of the iron oxidation pathways. Biochim Biophys Acta Bioenerg 1827:161–175Google Scholar
  38. 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 109:276–289Google Scholar
  39. 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 2:68–80Google Scholar
  40. Jong GAHD, Hazeu W, Bos P, Kuenen JG (2010) Isolation of the tetrathionate hydrolase from Thiobacillus Acidophilus. Fed Eur Biochem Soc 243:678–683Google Scholar
  41. Kanao T et al (2013) Crystallization and preliminary X-ray diffraction analysis of tetrathionate hydrolase from Acidithiobacillus ferrooxidans. Acta Crystallogr A 69:692–694Google Scholar
  42. 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 320:263–275PubMedGoogle Scholar
  43. Kato S (2015) Biotechnological aspects of microbial extracellular electron transfer. Microb Environ 30:133–139Google Scholar
  44. Klatt JM, Polerecky L (2015) Assessment of the stoichiometry and efficiency of CO2 fixation coupled to reduced sulfur oxidation. Front Microbiol 6:484–503PubMedPubMedCentralGoogle Scholar
  45. Kucera J, Pakostova E, Janiczek O, Mandl M (2015) Changes in Acidithiobacillus ferrooxidans ability to reduce ferric iron by elemental sulfur. Adv Mater Res 1130:97–100Google Scholar
  46. 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 167:357–366PubMedGoogle Scholar
  47. 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 167:587–594PubMedGoogle Scholar
  48. Kucera J, Janiczek O, Smoldas J, Mandl M (2017) Proteins binding to immobilized rusticyanin detected by affinity chromatography. Solid State Phenom 262:344–349Google Scholar
  49. 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 1656:114–126Google Scholar
  50. 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 184:1498–1501PubMedPubMedCentralGoogle Scholar
  51. Li Y, Li H (2014) Type IV pili of Acidithiobacillus ferrooxidans can transfer electrons from extracellular electron donors. J Basic Microbiol 54:226–231PubMedGoogle Scholar
  52. 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 62:320–324PubMedGoogle Scholar
  53. Liu H et al (2011) The co-culture of Acidithiobacillus ferrooxidans and Acidiphilium acidophilum enhances the growth, iron oxidation, and CO2 fixation. Arch Microbiol 193:857–866PubMedGoogle Scholar
  54. Liu J, Qian L, Zheng C (2013a) Biogenesis and transfer of iron-sulfur clusters from Acidithiobacillus ferrooxidans. In: International biohydrometallurgy symposium pp 198–201Google Scholar
  55. 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 66:88–95PubMedGoogle Scholar
  56. 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 60:623–628Google Scholar
  57. 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 68:285–292PubMedGoogle Scholar
  58. 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 55:587–598Google Scholar
  59. 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 123:112–118PubMedGoogle Scholar
  60. Mangold S, Valdés J, Holmes DS, Dopson M (2011) Sulfur metabolism in the extreme acidophile Acidithiobacillus Caldus. Front Microbiol 2:17–35PubMedPubMedCentralGoogle Scholar
  61. 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 79:113–120Google Scholar
  62. Mo H et al (2011) Ferric reductase activity of the ArsH protein from Acidithiobacillus ferrooxidans. J Microbiol Biotechnol 21:464–469PubMedGoogle Scholar
  63. 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 825:186–189Google Scholar
  64. 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 8:1277–1293PubMedPubMedCentralGoogle Scholar
  65. Morton NM et al (2016) Genetic identification of thiosulfate sulfurtransferase as an adipocyte-expressed antidiabetic target in mice selected for leanness. Nat Med 22:771–779PubMedPubMedCentralGoogle Scholar
  66. 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 82:1015–1022PubMedPubMedCentralGoogle Scholar
  67. 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 7:4175–4189PubMedGoogle Scholar
  68. Norris PR, Laigle L, Slade S (2018) Cytochromes in anaerobic growth of. Acidithiobacillus ferrooxidans. Microbiology 164:383–394PubMedGoogle Scholar
  69. Oetiker N et al (2018) Possible role ofenvelope components in the extreme copper resistance of the biomining Acidithiobacillus ferrooxidans. Genes 9:347–362PubMedCentralGoogle Scholar
  70. Ouyang J, Chen X (2009) Reserch progresses in ferrous oxidation system of Acidithiobacillus ferrooxidans. Biotechnol Bull 19:46–49Google Scholar
  71. 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 168:455–460PubMedGoogle Scholar
  72. 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 30:1–7Google Scholar
  73. 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 87:326–338Google Scholar
  74. 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 23:520–527Google Scholar
  75. 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 109:1–23Google Scholar
  76. Qian L, Zheng C, Liu J (2013) Characterization of iron-sulfur cluster assembly protein IscA from Acidithiobacillus ferrooxidans. Biochemistry 78:244–251PubMedGoogle Scholar
  77. Quatrini R et al (2006) Insights into the iron and sulfur energetic metabolism of Acidithiobacillus ferrooxidans by microarray transcriptome profiling. Hydrometallurgy 83:263–272Google Scholar
  78. 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 CrossRefGoogle Scholar
  79. 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 70:4491–4498PubMedPubMedCentralGoogle Scholar
  80. 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–e55140Google Scholar
  81. Santana MM, Gonzalez JM, Clara MI (2016) Inferring pathways leading to organic-sulfur mineralization in the Bacillales. Crit Rev Microbiol 42:1–15Google Scholar
  82. 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 1130:145–148Google Scholar
  83. 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 45:1791–1799Google Scholar
  84. 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 71:2663–2669Google Scholar
  85. 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 74:2242–2247Google Scholar
  86. 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 72:1756–1763Google Scholar
  87. 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 CrossRefGoogle Scholar
  88. 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):1389–1394Google Scholar
  89. Taha MTM (2009) Involvement of iron oxidation- and iron-reduction-enzyme systems in sulfur oxidation of iron-oxidizing bacterium Acidithiobacillus ferrooxidans. China Occup Med 27:3892–3895Google Scholar
  90. 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 20–21:443–446Google Scholar
  91. 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 167:58–65Google Scholar
  92. Valdés J et al (2008) Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genom 9:597–597Google Scholar
  93. Violaine B, Holmes DS (2012) Genomic insights into microbial iron oxidation and iron uptake strategies in extremely acidic environments. Environ Microbiol 14:1597–1611Google Scholar
  94. 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 263:730–751PubMedGoogle Scholar
  95. 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 98:7511–7522PubMedGoogle Scholar
  96. 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 68:87–138PubMedGoogle Scholar
  97. 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 30:3197–3209PubMedGoogle Scholar
  98. 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 150:2113–2123Google Scholar
  99. Yarzábal A, Brasseur G, Bonnefoy V (2002a) Cytochromes c of Acidithiobacillus ferrooxidans. Fems Microbiol Lett 209:189–195PubMedGoogle Scholar
  100. 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 184:313PubMedPubMedCentralGoogle Scholar
  101. Yu Y (2010) Isolation and characterization of the petII promoter of Acidithiobacillus ferrooxidans. J Bacteriol 196:2255–2264Google Scholar
  102. 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 52:146–152Google Scholar
  103. 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 40:1145–1155Google Scholar
  104. 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 136:51–57Google Scholar
  105. Zhang Y, Cherney MM, Weiner JH (2014) P97 characterization, structure and mechanism of sulfide: quinone oxidoreductase (SQR) from Acidithiobacillus ferrooxidans. Nitric Oxide 39:45–57Google Scholar
  106. 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 94:1–12Google Scholar
  107. 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 95:74–78Google Scholar
  108. 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 178:215–223Google Scholar
  109. Zhang S, Yan L, Xing W, Chen P, Zhang Y, Wang W (2018b) Acidithiobacillus ferrooxidans and its potential application. Extremophiles 22:563–579PubMedGoogle Scholar
  110. Zheng C et al (2009) Characterization and reconstitute of a [Fe4S4] adenosine 5′-phosphosulfate reductase from Acidithiobacillus ferrooxidans. Curr Microbiol 58:586–592PubMedGoogle Scholar
  111. Zheng C et al (2018) Effects of cadmium exposure on expression of glutathione synthetase system genes in Acidithiobacillus ferrooxidans. Extremophiles 1–8:1431–0651Google Scholar
  112. 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 24:1171–1178Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Yue Zhan
    • 1
  • Mengran Yang
    • 1
  • Shuang Zhang
    • 1
  • Dan Zhao
    • 1
  • Jiangong Duan
    • 2
  • Weidong Wang
    • 1
  • Lei Yan
    • 1
    • 3
    Email author
  1. 1.Heilongjiang Provincial Key Laboratory of Environmental Microbiology and Recycling of Argo-Waste in Cold Region, College of Life Science and BiotechnologyHeilongjiang Bayi Agricultural UniversityDaqingPeople’s Republic of China
  2. 2.School of PharmacyLanzhou UniversityLanzhouPeople’s Republic of China
  3. 3.College of Food ScienceHeilongjiang Bayi Agricultural UniversityDaqingPeople’s Republic of China

Personalised recommendations