Anaerobic sulfur metabolism coupled to dissimilatory iron reduction in the extremophile Acidithiobacillus ferrooxidans

Applied and Environmental Microbiology

Volumn 79, Issue 7, 2013, Pages 2172-2181

  Osorio, Héctor ^a,b   Mangold, Stefanie ^c   Denis, Yann ^d   Ñancucheo, Ivan ^e,h   Esparza, Mario ^a,b,i   Johnson, D Barrie ^e   Bonnefoy, Violaine ^f   Dopson, Mark ^b,g   Holmesa, David S ^a,b  

^a Fundación Ciencia y Vida   (Chile)

^b UNIVERSIDAD ANDRÉS BELLO   (Chile)

^c UMEÅ UNIVERSITY   (Sweden)

^d CNRS   (France)

^e BANGOR UNIVERSITY   (United Kingdom)

^f AIX MARSEILLE UNIVERSITÉ   (France)

^g LINNAEUS UNIVERSITY   (Sweden)

^h UNIVERSIDAD ARTURO PRAT   (Chile)

ⁱ UNIVERSIDAD DE ANTOFAGASTA   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDITHIOBACILLUS FERROOXIDANS; AEROBIC AND ANAEROBIC CONDITIONS; AEROBIC CONDITION; ANAEROBIC CONDITIONS; DISSIMILATORY IRON REDUCTION; ELECTRON ACCEPTOR; GENE TRANSCRIPTIONS; RESPIRATORY CHAINS;

BIOLEACHING; CARBON DIOXIDE; ELECTRONS; IRON; MOLECULAR BIOLOGY; SULFUR; TRANSCRIPTION;

IRON COMPOUNDS;

HYDROGEN SULFIDE; IRON; PROTEOME; SULFUR; TRANSCRIPTOME;

ANOXIC CONDITIONS; BACTERIOLOGY; BACTERIUM; BIOGEOCHEMICAL CYCLE; CARBON DIOXIDE; ENZYME ACTIVITY; GENE EXPRESSION; GROWTH RATE; INDUSTRIAL PRACTICE; IRON; METABOLISM; OXIC CONDITIONS; PHYSIOLOGY; PROTEIN; PROTEOMICS; REDUCTION; SULFUR;

ACIDITHIOBACILLUS; ANAEROBIC GROWTH; ARTICLE; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION;

ACIDITHIOBACILLUS; ANAEROBIOSIS; GENE EXPRESSION PROFILING; HYDROGEN SULFIDE; IRON; METABOLIC NETWORKS AND PATHWAYS; OXIDATION-REDUCTION; PROTEOME; SULFUR; TRANSCRIPTOME;

ACIDITHIOBACILLUS FERROOXIDANS;

EID: 84875547325     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03057-12     Document Type: Article

References (61)

1. Johnson DB, Hallberg KB. 2009. Carbon, iron and sulfur metabolism in acidophilic micro-organisms. Adv. Microb. Physiol. 54:201-255.
2. Liermann LJ, Hausrath EM, Anbar AD, Brantley SL. 2007. Assimilatory and dissimilatory processes of microorganisms affecting metals in the environment. J. Anal. Atom. Spectrom. 22:867-877.
3. Bird LJ, Bonnefoy V, Newman DK. 2011. Bioenergetic challenges of microbial iron metabolisms. Trends Microbiol. 19:330-340.
4. Shi L, Squier TC, Zachara JM, Fredrickson JK. 2007. Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol. Microbiol. 65:12-20.
5. Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR. 2008. Shewanella secretes flavins that mediate extracellular electron transfer. Proc. Natl. Acad. Sci. U. S. A. 105:3968-3973.
6. Taillefert M, Beckler JS, Carey E, Burns JL, Fennessey CM, DiChristina TJ. 2007. Shewanella putrefaciens produces an Fe(III)-solubilizing organic ligand during anaerobic respiration on insoluble Fe(III) oxides. J. Inorg. Biochem. 101:1760-1767.
7. Johnson DB, Kanao T, Hedrich S. 2012. Redox transformations of iron at extremely low pH: fundamental and applied aspects. Front. Microbiol. 3:96. doi:10.3389/fmicb.2012.00096.
8. Lovley DR, Holmes DE, Nevin KP. 2004. Dissimilatory Fe(III) and Mn(IV) reduction. Adv. Microb. Physiol. 49:219-286.
9. Welham NJ, Malatt KA, Vukcevic S. 2000. The effect of solution speciation on iron-sulphur-arsenic-chloride systems at 298 K. Hydrometallurgy 57:209-223.
10. Straub KL, Benz M, Schink B. 2001. Iron metabolism in anoxic environments at near neutral pH. FEMS Microbiol. Ecol. 34:181-186.
11. Hedrich S, Schlomann M, Johnson DB. 2011. The iron-oxidizing proteobacteria. Microbiology 157:1551-1564.
12. 3+, S0, and H2 in the chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans. J. Bacteriol. 184:2081-2087.
13. Pronk JT, De Bruyn JC, Bos P, Kuenen JG. 1992. Anaerobic growth of Thiobacillus ferrooxidans. Appl. Environ. Microbiol. 58:2227-2230.
14. Pronk JT, Liem K, Bos P, Keunen JG. 1991. Energy transduction by anaerobic ferric iron respiration in Thiobacillus ferrooxidans. Appl. Environ. Microbiol. 57:2063-2068.
15. Valdes J, Pedroso I, Quatrini R, Dodson RJ, Tettelin H, Blake R, Eisen JA, Holmes DS. 2008. Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genomics 9:597. doi: 10.1186/1471-2164-9-597.
16. Fischer J, Quentmeier A, Kostka S, Kraft R, Friedrich CG. 1996. Purification and characterization of the hydrogenase from Thiobacillus ferrooxidans. Arch. Microbiol. 165:289-296.
17. Schroder O, Bleijlevens B, de Jongh TE, Chen Z, Li T, Fischer J, Forster J, Friedrich CG, Bagley KA, Albracht SP, Lubitz W. 2007. Characterization of a cyanobacterial-like uptake [NiFe] hydrogenase: EPR and FTIR spectroscopic studies of the enzyme from Acidithiobacillus ferrooxidans. J. Biol. Inorg. Chem. 12:212-233.
18. Ng KY, Sawada R, Inoue S, Kamimura K, Sugio T. 2000. Purification and some properties of sulfur reductase from the iron-oxidizing bacterium Thiobacillus ferrooxidans NASF-1. J. Biosci. Bioeng. 90:199-203.
19. 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. Proteomics 6:2239-2251.
20. Quatrini R, Appia-Ayme C, Denis Y, Jedlicki E, Holmes D, Bonnefoy V. 2009. Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans. BMC Genomics 10:394. doi:10 .1186/1471-2164-10-394.
21. Holmes DS, Bonnefoy V. 2007. Genetic and bioinformatic insights into iron and sulfur oxidation mechanisms of bioleaching organisms, p 281-307. In Rawlings DE, Johnson DB (ed), Biomining. Springer-Verlag, Berlin, Germany.
22. Rohwerder T, Sand W. 2007. Oxidation of inorganic sulfur compounds in acidophilic prokaryotes. Eng. Life Sci. 7:301-309.
23. Bonnefoy V, Holmes DS. 2012. Genomic insights into microbial oxidation and iron homeostasis in extremely acidic environments. Environ. Microbiol. 14:1597-1611.
24. 2+ grown Thiobacillus ferrooxidans? FEMS Microbiol. Lett. 41:1-6.
25. Sugio T, Domatsu C, Munukata O, Tano T, Imai K. 1985. Role of a ferric iron-reducing system in sulfur oxidation by Thiobacillus ferrooxidans. Appl. Environ. Microbiol. 49:1401-1406.
26. Sugio T, Mizunashi W, Magaki K, Tano T. 1987. Purification and some properties of sulfur-ferric iron oxidoreductase from Thiobacillus ferrooxidans. J. Bacteriol. 169:4916-4922.
27. Sugio T, Hirose T, Ye LZ, Tano T. 1992. Purification and some properties of sulfite-ferric ion oxidoreductase from Thiobacillus ferrooxidans. J. Bacteriol. 174:4189-4192.
28. Sugio T, Taha TM, Takeuchi F. 2009. Ferrous iron production mediated by tetrathionate hydrolase in tetrathionate-, sulfur-, and iron-grown Acidithiobacillus ferrooxidansATCC23270 cells. Biosci. Biotechnol. Biochem. 73:1381-1386.
29. Mo H, Chen Q, Du J, Tang L, Qin F, Miao B, Wu X, Zeng J. 2011. Ferric reductase activity of the ArsH protein from Acidithiobacillus ferrooxidans. J. Microbiol. Biotechnol. 21:464-469.
30. Kucera J, Bouchal P, Cerna H, Potesil D, Janiczek O, Zdrahal Z, Mandl M. 2012. Kinetics of anaerobic elemental sulfur oxidation by ferric iron in Acidithiobacillus ferrooxidans and protein identification by comparative 2-DE-MS/MS. Antonie van Leeuwenhoek 101:561-573.
31. Hallberg KB, Grail BM, du Plessis C, Johnson DB. 2011. Reductive dissolution of ferric iron minerals: a new approach for bioprocessing nickel laterites. Miner. Eng. 24:620-624.
32. Johnson DB, Hallberg KB. 2007. Techniques for detecting and identifying acidophilic mineral-oxidizing microorganisms. In Rawlings DE, Johnson DB (ed), Biomining. Springer-Verlag, Berlin, Germany.
33. Lovley DR, Phillips EJ. 1987. Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl. Environ. Microbiol. 53:1536-1540.
34. Ñancucheo I, Johnson DB. 2012. Selective removal of transition metals from acidic mine waters by novel consortia of acidophilic sulfidogenic bacteria. Microb. Biotechnol. 5:34-44.
35. Mangold S, Valdes J, Holmes DS, Dopson M. 2011. Sulfur metabolism in the extreme acidophile Acidithiobacillus caldus. Front. Microbiol. 2:17. doi:10.3389/fmicb.2011.00017.
36. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. 1999. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551-3567.
37. Quatrini R, Appia-Ayme C, Denis Y, Ratouchniak J, Veloso F, Valdes J, Lefimil C, Silver S, Roberto F, Orellana O, Denizot F, Jedlicki E, Holmes D, Bonnefoy V. 2006. Insights into the iron and sulfur energetic metabolism of Acidithiobacillus ferrooxidans by microarray transcriptome profiling. Hydrometallurgy 83:263-272.
38. Peterson JD, Umayam LA, Dickinson T, Hickey EK, White O. 2001. The comprehensive microbial resource. Nucleic Acids Res. 29:123-125.
39. Nieto PA, Covarrubias PC, Jedlicki E, Holmes DS, Quatrini R. 2009. Selection and evaluation of reference genes for improved interrogation of microbial transcriptomes: case study with the extremophile Acidithiobacillus ferrooxidans. BMC Mol. Biol. 10:63. doi:10.1186/1471-2199-10-63.
40. Nie L, Wu G, Culley DE, Scholten JC, Zhang W. 2007. Integrative analysis of transcriptomic and proteomic data: challenges, solutions and applications. Crit. Rev. Biotechnol. 27:63-75.
41. Scherl A, Francois P, Bento M, Deshusses JM, Charbonnier Y, Converset V, Huyghe A, Walter N, Hoogland C, Appel RD, Sanchez JC, Zimmermann-Ivol CG, Corthals GL, Hochstrasser DF, Schrenzel J. 2005. Correlation of proteomic and transcriptomic profiles of Staphylococcus aureus during the post-exponential phase of growth. J. Microbiol. Methods 60:247-257.
42. Nie L, Wu G, Zhang W. 2006. Correlation between mRNA and protein abundance in Desulfovibrio vulgaris: a multiple regression to identify sources of variations. Biochem. Biophys. Res. Commun. 339:603-610.
43. Greenbaum D, Colangelo C, Williams K, Gerstein M. 2003. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol. 4:117. doi:10.1186/gb-2003-4-9-117.
44. Rohwerder T, Sand W. 2003. The sulfane sulfur of persulfides is the actual substrate of the sulfur-oxidizing enzymes from Acidithiobacillus and Acidiphilium spp. Microbiology 149:1699-1709.
45. Chen L, Ren Y, Lin J, Liu X, Pang X. 2012. Acidithiobacillus caldus sulfur oxidation model based on transcriptome analysis between the wild type and sulfur oxygenase reductase defective mutant. PLoS One 7:e39470. doi: 10.1371/journal.pone.0039470.
46. Dahl C, Schulte A, Stockdreher Y, Hong C, Grimm F, Sander J, Kim R, Kim SH, Shin DH. 2008. Structural and molecular genetic insight into a widespread sulfur oxidation pathway. J. Mol. Biol. 384:1287-1300.
47. Ikeuchi Y, Shigi N, Kato J, Nishimura A, Suzuki T. 2006. Mechanistic insights into sulfur relay by multiple sulfur mediators involved in thiouridine biosynthesis at tRNA wobble positions. Mol. Cell 21:97-108.
48. Stockdreher Y, Venceslau SS, Josten M, Sahl HG, Pereira IA, Dahl C. 2012. Cytoplasmic sulfurtransferases in the purple sulfur bacterium Allochromatium vinosum: evidence for sulfur transfer from DsrEFH to DsrC. PLoS One 7:e40785. doi:10.1371/journal.pone.0040785.
49. Guiral M, Tron P, Aubert C, Gloter A, Iobbi-Nivol C, Giudici-Orticoni MT. 2005. A membrane-bound multienzyme, hydrogen-oxidizing, and sulfur-reducing complex from the hyperthermophilic bacterium Aquifex aeolicus. J. Biol. Chem. 280:42004-42015.
50. Frederiksen TM, Finster K. 2004. The transformation of inorganic sulfur compounds and the assimilation of organic and inorganic carbon by the sulfur disproportionating bacterium Desulfocapsa sulfoexigens. Antonie van Leeuwenhoek 85:141-149.
51. Valdes J, Veloso F, Jedlicki E, Holmes D. 2003. Metabolic reconstruction of sulfur assimilation in the extremophile Acidithiobacillus ferrooxidans based on genome analysis. BMC Genomics 4:51. doi:10.1186/1471-2164-4-51.
52. Kelly DP. 1999. Thermodynamic aspects of energy conservation by chemolithotrophic sulfur bacteria in relation to the sulfur oxidation pathways. Arch. Microbiol. 171:219-229.
53. Ingledew WJ. 1982. Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph. Biochim. Biophys. Acta 683:89-117.
54. Braun TF, Poulson S, Gully JB, Empey JC, Van Way S, Putnam A, Blair DF. 1999. Function of proline residues of MotA in torque generation by the flagellar motor of Escherichia coli. J. Bacteriol. 181:3542-3551.
55. Lee PT, Hsu AY, Ha HT, Clarke CF. 1997. A C-methyltransferase involved in both ubiquinone and menaquinone biosynthesis: isolation and identification of the Escherichia coli ubiE gene. J. Bacteriol. 179:1748-1754.
56. Esparza M, Bowien B, Jedlicki E, Holmes DS. 2009. Gene organization and CO2-responsive expression of four cbb operons in the biomining bacterium Acidithiobacillus ferrooxidans. Adv. Mater. Res. 71-73:207-210.
57. Esparza M, Cardenas JP, Bowien B, Jedlicki E, Holmes DS. 2010. Genes and pathways for CO2 fixation in the obligate, chemolithoautotrophic acidophile, Acidithiobacillus ferrooxidans. BMC Microbiol. 10:229. doi:10 .1186/1471-2180-10-229.
58. Bryan CG, Davis-Belmar CS, van Wyk N, Fraser MK, Dew D, Rautenbach GF, Harrison ST. 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.
59. van den Berg B. 2010. Going forward laterally: transmembrane passage of hydrophobic molecules through protein channel walls. Chembiochem 11: 1339-1343.
60. 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. 70:4491-4498.
61. Lazar SW, Kolter R. 1996. SurA assists the folding of Escherichia coli outer membrane proteins. J. Bacteriol. 178:1770-1773.