Advertisement

Antonie van Leeuwenhoek

, Volume 101, Issue 3, pp 561–573 | Cite as

Kinetics of anaerobic elemental sulfur oxidation by ferric iron in Acidithiobacillus ferrooxidans and protein identification by comparative 2-DE-MS/MS

  • Jiri Kucera
  • Pavel Bouchal
  • Hana Cerna
  • David Potesil
  • Oldrich Janiczek
  • Zbynek Zdrahal
  • Martin MandlEmail author
Original Paper

Abstract

Elemental sulfur oxidation by ferric iron in Acidithiobacillus ferrooxidans was investigated. The apparent Michaelis constant for ferric iron was 18.6 mM. An absence of anaerobic ferric iron reduction ability was observed in bacteria maintained on elemental sulfur for an extended period of time. Upon transition from ferrous iron to elemental sulfur medium, the cells exhibited similar kinetic characteristics of ferric iron reduction under anaerobic conditions to those of cells that were originally maintained on ferrous iron. Nevertheless, a total loss of anaerobic ferric iron reduction ability after the sixth passage in elemental sulfur medium was demonstrated. The first proteomic screening of total cell lysates of anaerobically incubated bacteria resulted in the detection of 1599 protein spots in the master two-dimensional electrophoresis gel. A set of 59 more abundant and 49 less abundant protein spots that changed their protein abundances in an anaerobiosis-dependent manner was identified and compared to iron- and sulfur-grown cells, respectively. Proteomic analysis detected a significant increase in abundance under anoxic conditions of electron transporters, such as rusticyanin and cytochrome c552, involved in the ferrous iron oxidation pathway. Therefore we suggest the incorporation of rus-operon encoded proteins in the anaerobic respiration pathway. Two sulfur metabolism proteins were identified, pyridine nucleotide-disulfide oxidoreductase and sulfide-quinone reductase. The important transcription regulator, ferric uptake regulation protein, was anaerobically more abundant. The anaerobic expression of several proteins involved in cell envelope formation indicated a gradual adaptation to elemental sulfur oxidation.

Keywords

Acidithiobacillus Anaerobic sulfur oxidation Ferric iron reduction Proteomics MS analysis 

Notes

Acknowledgments

This work was supported by grants 525/08/0697 from the Czech Science Foundation and MSM0021622413 and MSM 0021622415 from the Czech Ministry of Education.

Supplementary material

10482_2011_9670_MOESM1_ESM.pdf (1.8 mb)
Supplementary material 1 (PDF 1802 kb)

References

  1. Amaro AM, Chamorro D, Seeger M, Arredondo R, Peirano I, Jerez CA (1991) Effect of external pH perturbations on in vivo protein synthesis by the acidophilic bacterium Thiobacillus ferrooxidans. J Bacteriol 173:910–915PubMedGoogle Scholar
  2. Appia-Ayme C, Bengrine A, Cavazza C, Giudici-Orticoni MT, Bruschi M, Chippaux M, Bonnefoy V (1998) 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 167:171–177PubMedGoogle Scholar
  3. Appia-Ayme C, Guiliani N, Ratouchniak J, Bonnefoy V (1999) Characterization of an operon encoding two c-type cytochromes, an aa(3)-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020. Appl Environ Microbiol 65:4781–4787PubMedGoogle Scholar
  4. Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152PubMedCrossRefGoogle Scholar
  5. Bengrine A, Guiliani N, Appia-Ayme C, Jedlicki E, Holmes DS, Chippaux M, Bonnefoy V (1998) Sequence and expression of the rusticyanin structural gene from Thiobacillus ferrooxidans ATCC33020 strain. Biochim Biophys Acta 1443:99–112PubMedGoogle Scholar
  6. Bouchal P, Zdrahal Z, Helanova S, Janiczek O, Hallberg KB, Mandl M (2006) Proteomic and bioinformatic analysis of iron- and sulfur-oxidizing Acidithiobacillus ferrooxidans using immobilized pH gradients and mass spectrometry. Proteomics 6:4278–4285PubMedCrossRefGoogle Scholar
  7. Bouchal P, Struharova I, Budinska E, Sedo O, Vyhlidalova T, Zdrahal Z, Van Spanning R, Kucera I (2010) Unraveling an FNR based regulatory circuit in Paracoccus denitrificans using a proteomics-based approach. Biochim Biophys Acta 1804:1350–1358PubMedGoogle Scholar
  8. Bouveret E, Benedetti H, Rigal A, Loret E, Lazdunski C (1999) In vitro characterization of peptidoglycan-associated lipoprotein (PAL)-peptidoglycan and PAL-TolB interactions. J Bacteriol 181:6306–6311PubMedGoogle Scholar
  9. 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 1555:37–43PubMedCrossRefGoogle Scholar
  10. Brasseur G, Levican G, Bonnefoy V, Holmes DS, Jedlicki E, Lemesle-Meunier D (2004) Apparent redundancy of electron transfer pathways via bc1 complexes and terminal oxidases in the extremophilic chemolithoautotrophic Acidithiobacillus ferrooxidans. Biochim Biophys Acta 1656:114–126PubMedCrossRefGoogle Scholar
  11. Brock TD, Gustafson J (1976) Ferric iron reduction by sulfur- and iron- oxidizing bacteria. Appl Environ Microbiol 32:567–571PubMedGoogle Scholar
  12. Bruscella P, Appia-Ayme C, Levican G, 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. Microbiol 153:102–110CrossRefGoogle Scholar
  13. Carrondo MA (2003) Ferritins iron uptake and storage from the bacterioferritin viewpoint. EMBO J 22:1959–1968PubMedCrossRefGoogle Scholar
  14. Ceskova P, Mandl M, Hubackova J (2000) Kinetic quantitation of sulfur-oxidizing bacteria adsorbed on sulfur. Biotechnol Lett 22:699–701CrossRefGoogle Scholar
  15. Chi A, Valenzuela L, Beard S, Mackey AJ, Shabanowitz J, Hunt DF, Jerez CA (2007) Periplasmic proteins of the extremophile Acidithiobacillus ferrooxidans. Mol Cell Proteomics 6:2239–2251PubMedCrossRefGoogle Scholar
  16. Corbett CM, Ingledew WJ (1987) Is Fe3+/2+ cycling an intermediate in sulphur oxidation by Fe2+-grown Thiobacillus ferrooxidans?. FEMS Microbiol Lett 41:1–6CrossRefGoogle Scholar
  17. Das A, Mishra AK, Roy P (1992) Anaerobic growth on elemental sulfur using dissimilar iron reduction by autotrophic Thiobacillus ferrooxidans. FEMS Microbiol Lett 97:167–172CrossRefGoogle Scholar
  18. Elbehti A, Brasseur G, Lemesle-Meunier D (2000) First evidence for existence of an uphill electron transfer through the bc1 and NADH-Q oxidoreductase complexes of the acidophilic obligate chemolithotrophic ferrous ion-oxidizing bacterium Thiobacillus ferrooxidans. J Bacteriol 182:3602–3606PubMedCrossRefGoogle Scholar
  19. Gehrke T, Telegdi J, Thierry D, Sand W (1998) Importance of extracellular polymeric substances from Thiobacillus ferrooxidans for bioleaching. Appl Environ Microbiol 64:2743–2747PubMedGoogle Scholar
  20. Gentle IE, Burri L, Lithgow T (2005) Molecular architecture and function of the Omp85 family of proteins. Mol Microbiol 58:1216–1225PubMedCrossRefGoogle Scholar
  21. Hallberg KB, Gonzalez-Toril E, Johnson DB (2010) Acidithiobacillus ferrivorans, sp. nov.; facultatively anaerobic, psychrotolerant iron-, and sulfur-oxidizing acidophiles isolated from metal mine-impacted environments. Extremophiles 14:9–19PubMedCrossRefGoogle Scholar
  22. He ZG, Hu YH, Zhong H, Hu WX, Xu J (2005) Preliminary proteomic analysis of Thiobacillus ferrooxidans growing on elemental sulphur and Fe2+ separately. J Biochem Mol Biol 38:307–313PubMedCrossRefGoogle Scholar
  23. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, Mann M (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4:1265–1272PubMedCrossRefGoogle Scholar
  24. Janiczek O, Mandl M, Ceskova P (1998) Metabolic activity of Thiobacillus ferrooxidans on reduced sulfur compounds detected by capillary isotachophoresis. J Biotechnol 61:225–229CrossRefGoogle Scholar
  25. Jerez CA, Seeger M, Amaro AM (1992) Phosphate starvation affects the synthesis of outer membrane proteins in Thiobacillus ferrooxidans. FEMS Microbiol Lett 98:29–34CrossRefGoogle Scholar
  26. Johnson DB (2010) The biogeochemistry of biomining. In: Barton L, Mandl M, Loy A (eds) Geomicrobiology: molecular and environmental perspective. Springer, Dordrecht, pp 401–426CrossRefGoogle Scholar
  27. Jones LJ, Carballido-Lopez R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913–922PubMedCrossRefGoogle Scholar
  28. Layer G, Verfurth K, Mahlitz E, Jahn D (2002) Oxygen-independent coproporphyrinogen-III oxidase HemN from Escherichia coli. J Biol Chem 277:34136–34142PubMedCrossRefGoogle Scholar
  29. Lefimil C, Osorio H, Quatrini R, Holmes DS, Jedlicki E (2009) Regulation of expression of the petI operon involved in iron oxidation in the biomining bacterium Acidithiobacillus ferrooxidans. Adv Mater Res 71–73:199–202CrossRefGoogle Scholar
  30. Levican 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 184:1498–1501PubMedCrossRefGoogle Scholar
  31. Mandl M, Novakova O (1993) An ultraviolet method for the determination of oxidation of iron sulphide minerals by bacteria. Biotechnol Tech 7:573–574CrossRefGoogle Scholar
  32. Matthysse AG, Yarnall H, Boles SB, McMahan S (2000) A region of the Agrobacterium tumefaciens chromosome containing genes required for virulence and attachment to host cells. Biochim Biophys Acta 1490:208–212PubMedGoogle Scholar
  33. Mykytczuk NC, Trevors JT, Foote SJ, Leduc LG, Ferroni GD, Twine SM (2011) Proteomic insights into cold adaptation of psychrotrophic and mesophilic Acidithiobacillus ferrooxidans strains. Antonie van Leeuwenhoek 10:259–277CrossRefGoogle Scholar
  34. Novo MTM, da Silva AC, Moreto R, Cabral PCP, Costacurta A, Garcia O Jr, Ottoboni LMM (2000) Thiobacillus ferrooxidans response to copper and other heavy metals: growth, protein synthesis and protein phosphorylation. Antonie van Leeuwenhoek 77:187–195PubMedCrossRefGoogle Scholar
  35. Ohmura N, Sasaki K, Matsumoto N, Saiki H (2002) Anaerobic respiration using Fe3+, S0, and H2 in the chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans. J Bacteriol 184:2081–2087PubMedCrossRefGoogle Scholar
  36. Osorio H, Martinez V, Nieto PA, Holmes DS, Quatrini R (2008) Microbial iron management mechanisms in extremely acidic environments: comparative genomics evidence for diversity and versatility. BMC Microbiol 8:203PubMedCrossRefGoogle Scholar
  37. Osorio H, Cardenas JP, Valdes J, Holmes DS (2009) Prediction of FNR regulated genes and metabolic pathways potentially involved in anaerobic growth of Acidithiobacillus ferrooxidans. Adv Mater Res 71–73:195–198CrossRefGoogle Scholar
  38. Paradis-Bleau C, Markovski M, Uehara T, Lupoli TJ, Walker S, Kahne DE, Bernhardt TG (2010) Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 143:1110–1120PubMedCrossRefGoogle Scholar
  39. Pokorna B, Mandl M, Borilova S, Ceskova P, Markova R, Janiczek O (2007) Kinetic constant variability in bacterial oxidation of elemental sulfur. Appl Environ Microbiol 37:3752–3754CrossRefGoogle Scholar
  40. Pronk JT, Liem K, Bos P, Kuenen JG (1991) Energy transduction by anaerobic ferric iron respiration in Thiobacillus ferrooxidans. Appl Environ Microbiol 57:2063–2068PubMedGoogle Scholar
  41. Pronk JT, De BJC, Bos P, Kuenen JG (1992) Anaerobic growth of Thiobacillus ferrooxidans. Appl Environ Microbiol 58:2227–2230PubMedGoogle Scholar
  42. Quatrini R, Lefimil C, Veloso FA, Pedroso I, Holmes DS, Jedlicki E (2007) Bioinformatic prediction and experimental verification of Fur-regulated genes in the extreme acidophile Acidithiobacillus ferrooxidans. Nucleic Acids Res 35:2153–2166PubMedCrossRefGoogle Scholar
  43. 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 Genomics 10:394PubMedCrossRefGoogle Scholar
  44. Ramirez 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 70:4491–4498PubMedCrossRefGoogle Scholar
  45. Rawlings DE (2004) Microbially assisted dissolution of minerals and its use in the mining industry. Pure Appl Chem 76:847–859CrossRefGoogle Scholar
  46. Ribeiro DA, Maretto DA, Nogueira FCS, Silva MJ, Campos FAP, Domont GB, Poppi RJ, Ottoboni LMM (2011) Heat and phosphate starvation effects on the proteome, morphology and chemical composition of the biomining bacteria Acidithiobacillus ferrooxidans. World J Microbiol Biotechnol 27:1469–1479CrossRefGoogle Scholar
  47. Silverman MP, Lungred DG (1959) Studies on the chemoautotrophic iron bacterium Ferrobacillus ferrooxidans. J Bacteriol 77:642–647PubMedGoogle Scholar
  48. Sugio T, Domatsu C, Munakato O, Tano T, Imai K (1985) Role of a ferric ion-reducing system in sulfur oxidation of Thiobacillus-ferrooxidans. Appl Environ Microbiol 49:1401–1406PubMedGoogle Scholar
  49. Sugio T, Mizunashi W, Inagaki K, Tano T (1987) Purification and some properties of sulfur:ferric ion oxidoreductase from Thiobacillus ferrooxidans. J Bacteriol 169:4916–4922PubMedGoogle Scholar
  50. Sugio T, Wada K, Mori M, Inagaki K, Tano T (1988) Synthesis of an iron-oxidizing system during growth of Thiobacillus ferrooxidans on sulfur-basal salts medium. Appl Environ Microbiol 54:150–152PubMedGoogle Scholar
  51. Sugio T, Hirose T, Zhen YL, Tano T (1992) Purification and some properties of sulfite:ferric ion oxidoreductase from Thiobacillus ferrooxidans. J Bacteriol 174:4189–4192PubMedGoogle Scholar
  52. Suzuki I, Takeuchi TL, Yuthasastrakosol TD, Oh JK (1990) Ferrous iron and sulfur oxidation and ferric iron reduction activities of Thiobacillus ferrooxidans are affected by growth on ferrous iron, sulfur, or a sulfide ore. Appl Environ Microbiol 56:1620–1626PubMedGoogle Scholar
  53. Tamura H, Goto K (1974) Spectrophotometric determination of iron (II) with 1, 10-phenanthroline in the presence of large amounts of iron(III). Talanta 21:314–318PubMedCrossRefGoogle Scholar
  54. Typas A, Banzhaf M, van Saparoea B, Verheul J, Biboy J, Nichols RJ, Zietek M, Beilharz K, Kannenberg K, von Rechenberg M, Breukink E, den Blaauwen T, Gross CA, Vollmer W (2010) Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143:1097–1109PubMedCrossRefGoogle Scholar
  55. Vijayalakshmi J, Akerley BJ, Saper MA (2008) Structure of YraM, a protein essential for growth of Haemophilus influenzae. Proteins 73:204–217PubMedCrossRefGoogle Scholar
  56. Wakai S, Tsujita M, Kikumoto M, Manchur MA, Kanao T, Kamimura K (2007) Purification and characterization of sulfide:quinone oxidoreductase from an acidophilic iron-oxidizing bacterium Acidithiobacillus ferrooxidans. Biosci Biotechnol Biochem 71:2735–2742PubMedCrossRefGoogle Scholar
  57. Yarzabal A, Brasseur G, Ratouchniak J, Lund K, Lemesle-Meunier D, DeMoss JA, Bonnefoy V (2002) The high-molecular-weight cytochrome c Cyc2 of Acidithiobacillus ferrooxidans is an outer membrane protein. J Bacteriol 184:313–317PubMedCrossRefGoogle Scholar
  58. Yarzabal A, Dusquesne K, Bonnefoy V (2003) Rusticyanin gene expression of Acidithiobacillus ferrooxidans ATCC 33020 in sulfur- and in ferrous iron media. Hydrometallurgy 71:107–114CrossRefGoogle Scholar
  59. Yarzabal A, 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 and rusticyanin. Microbiology 150:2113–2123PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Jiri Kucera
    • 1
  • Pavel Bouchal
    • 1
  • Hana Cerna
    • 1
  • David Potesil
    • 2
  • Oldrich Janiczek
    • 1
  • Zbynek Zdrahal
    • 2
  • Martin Mandl
    • 1
    Email author
  1. 1.Department of Biochemistry, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  2. 2.Core Facility-Proteomics, Central European Institute of TechnologyMasaryk UniversityBrnoCzech Republic

Personalised recommendations