1887

Microbiology Society logo

Volume 164, Issue 3

Cytochromes in anaerobic growth of Free

Abstract

The mineral sulfide-oxidising has been extensively studied over many years but some fundamental aspects of its metabolism remain uncertain, particularly with regard to its anaerobic oxidation of sulfur. This label-free, liquid chromatography-electron spray ionisation-mass spectrometry-based proteomic analysis estimated relative protein abundance during aerobic and anaerobic growth of . One of its two complexes, that encoded by the operon, was strongly implicated in anaerobic ferric iron-coupled sulfur oxidation, probably in conjunction with two cytochromes. These two cytochromes are homologs of the Cyc2 and Cyc1 proteins that are involved in ferrous iron oxidation. The previously undetected cytochromes apparently associated with anaerobic growth in appear to be absent in many other ferrous iron-oxidising acidophiles that can also reduce ferric iron, which suggests a diversity in the ferric-iron-coupled sulfur oxidation pathways. For aerobic growth of , this analysis was consistent with the generally accepted mechanism for its oxidation of ferrous iron. Unexpectedly, proteins encoded by the operon were not abundant and generally not detected in the proteomic analyses of cells grown aerobically on sulfur, although there was some expression of genes of the and operons in these cells.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Acidithiobacillus ferrooxidans , anaerobic growth and novel cytochromes
© 2018 The Authors
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000616
2018-03-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/164/3/383.html?itemId=/content/journal/micro/10.1099/mic.0.000616&mimeType=html&fmt=ahah

References

  1. Brock TD, Gustafson J. Ferric iron reduction by sulfur- and iron-oxidizing bacteria. Appl Environ Microbiol 1976; 32:567–571[PubMed]
     [Google Scholar]
  2. Goodman AE, Babij T, Ritchie AIM. Leaching of a sulphide ore by Thiobacillus ferrooxidans under anaerobic conditions. In Rossi G, Torma AE. (editors) Recent Progress in Biohydrometallurgy Iglesias, Italy: Associazione Mineraria Sarda; 1983 pp. 361–376
     [Google Scholar]
  3. Donati E, Pogliani C, Boiardi JL. Anaerobic leaching of covellite by Thiobacillus ferrooxidans . Appl Microbiol Biotechnol 1997; 47:636–639 [View Article]
     [Google Scholar]
  4. Ohmura N, Sasaki K, Matsumoto N, Saiki H. Anaerobic respiration using Fe3+, S0, and H2 in the chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans . J Bacteriol 2002; 184:2081–2087 [View Article][PubMed]
     [Google Scholar]
  5. Ingledew WJ. Thiobacillus ferrooxidans: the bioenergetics of an acidophilic chemolithotroph. Biochim Biophys Acta 1982; 683:89–117 [View Article][PubMed]
     [Google Scholar]
  6. Bonnefoy V, Holmes DS. Genomic insights into microbial iron oxidation and iron uptake strategies in extremely acidic environments. Environ Microbiol 2012; 14:1597–1611 [View Article][PubMed]
     [Google Scholar]
  7. Castelle C, Guiral M, Malarte G, Ledgham F, Leroy G et al. A new iron-oxidizing/O2-reducing supercomplex spanning both inner and outer membranes, isolated from the extreme acidophile Acidithiobacillus ferrooxidans . J Biol Chem 2008; 283:25803–25811 [View Article][PubMed]
     [Google Scholar]
  8. Quatrini R, Appia-Ayme C, Denis Y, Jedlicki E, Holmes DS et al. Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans . BMC Genomics 2009; 10:394 [View Article][PubMed]
     [Google Scholar]
  9. Castelle C, Ilbert M, Infossi P, Leroy G, Giudici-Orticoni MT. An unconventional copper protein required for cytochrome c oxidase respiratory function under extreme acidic conditions. J Biol Chem 2010; 285:21519–21525 [View Article][PubMed]
     [Google Scholar]
  10. Appia-Ayme C, Guiliani N, Ratouchniak J, Bonnefoy V. Characterization of an operon encoding two c-type cytochromes, an aa3- type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020. Appl Environ Microbiol 1999; 65:4781–4787[PubMed]
     [Google Scholar]
  11. Bruscella P, Appia-Ayme C, Levicán G, Ratouchniak J, Jedlicki E et al. Differential expression of two bc 1 complexes in the strict acidophilic chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans suggests a model for their respective roles in iron or sulfur oxidation. Microbiology 2007; 153:102–110 [View Article][PubMed]
     [Google Scholar]
  12. Li TF, Painter RG, Ban B, Blake RC. The multicenter aerobic iron respiratory chain of Acidithiobacillus ferrooxidans Functions as an ensemble with a single macroscopic rate constant. J Biol Chem 2015; 290:18293–18303 [View Article][PubMed]
     [Google Scholar]
  13. Harrison AP. Genomic and physiological diversity amongst strains of Thiobacillus ferrooxidans, and genomic comparison with Thiobacillus thiooxidans . Arch Microbiol 1982; 131:68–76 [View Article]
     [Google Scholar]
  14. Karavaiko GI, Turova TP, Kondrat'eva TF, Lysenko AM, Kolganova TV et al. Phylogenetic heterogeneity of the species Acidithiobacillus ferrooxidans . Int J Syst Evol Microbiol 2003; 53:113–119 [View Article][PubMed]
     [Google Scholar]
  15. Amouric A, Brochier-Armanet C, Johnson DB, Bonnefoy V, Hallberg KB. Phylogenetic and genetic variation among Fe(II)-oxidizing acidithiobacilli supports the view that these comprise multiple species with different ferrous iron oxidation pathways. Microbiology 2011; 157:111–122 [View Article][PubMed]
     [Google Scholar]
  16. Hedrich S, Johnson DB. Acidithiobacillus ferridurans sp. nov., an acidophilic iron-, sulfur- and hydrogen-metabolizing chemolithotrophic gammaproteobacterium. Int J Syst Evol Microbiol 2013; 63:4018–4025 [View Article][PubMed]
     [Google Scholar]
  17. 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; 14:9–19 [View Article][PubMed]
     [Google Scholar]
  18. Falagán C, Johnson DB. Acidithiobacillus ferriphilus sp. nov., a facultatively anaerobic iron- and sulfur-metabolizing extreme acidophile. Int J Syst Evol Microbiol 2016; 66:206–211 [View Article][PubMed]
     [Google Scholar]
  19. Sasaki K, Ida C, Ando A, Matsumoto N, Saiki H et al. Respiratory isozyme, two types of rusticyanin of Acidithiobacillus ferrooxidans . Biosci Biotechnol Biochem 2003; 67:1039–1047 [View Article][PubMed]
     [Google Scholar]
  20. Kusano T, Takeshima T, Sugawara K, Inoue C, Shiratori T et al. Molecular cloning of the gene encoding Thiobacillus ferrooxidans Fe(II) oxidase. High homology of the gene product with HiPIP. J Biol Chem 1992; 267:11242–11247[PubMed]
     [Google Scholar]
  21. Sugio T, Mizunashi W, Inagaki K, Tano T. Purification and some properties of sulfur:ferric ion oxidoreductase from Thiobacillus ferrooxidans . J Bacteriol 1987; 169:4916–4922 [View Article][PubMed]
     [Google Scholar]
  22. Sugio T, Taha TM, Takeuchi F. Ferrous iron production mediated by tetrathionate hydrolase in tetrathionate-, sulfur-, and iron-grown Acidithiobacillus ferrooxidans ATCC 23270 cells. Biosci Biotechnol Biochem 2009; 73:1381–1386 [View Article][PubMed]
     [Google Scholar]
  23. Corbett CM, Ingledew WJ. Is Fe 3+/2+ cycling an intermediate in sulphur oxidation by Fe 2+ -grown Thiobacillus ferrooxidans . FEMS Microbiol Lett 1987; 41:1–6 [View Article]
     [Google Scholar]
  24. Kucera J, Bouchal P, Cerna H, Potesil D, Janiczek O et al. Kinetics of anaerobic elemental sulfur oxidation by ferric iron in Acidithiobacillus ferrooxidans and protein identification by comparative 2-DE-MS/MS. Antonie van Leeuwenhoek 2012; 101:561–573 [View Article][PubMed]
     [Google Scholar]
  25. Kucera J, Pakostova E, Lochman J, Janiczek O, Mandl M. Are there multiple mechanisms of anaerobic sulfur oxidation with ferric iron in Acidithiobacillus ferrooxidans?. Res Microbiol 2016; 167:357–366 [View Article][PubMed]
     [Google Scholar]
  26. Osorio H, Mangold S, Denis Y, Ñancucheo I, Esparza M et al. Anaerobic sulfur metabolism coupled to dissimilatory iron reduction in the extremophile Acidithiobacillus ferrooxidans . Appl Environ Microbiol 2013; 79:2172–2181 [View Article][PubMed]
     [Google Scholar]
  27. Patel VJ, Thalassinos K, Slade SE, Connolly JB, Crombie A et al. A comparison of labeling and label-free mass spectrometry-based proteomics approaches. J Proteome Res 2009; 8:3752–3759 [View Article][PubMed]
     [Google Scholar]
  28. Abergel C, Nitschke W, Malarte G, Bruschi M, Claverie J-M et al. The structure of Acidithiobacillus ferrooxidans c 4-cytochrome: a model for complex-induced electron transfer tuning. Structure 2003; 11:547–555[PubMed] [Crossref]
     [Google Scholar]
  29. Malarte G, Leroy G, Lojou E, Abergel C, Bruschi M et al. Insight into molecular stability and physiological properties of the diheme cytochrome CYC41 from the acidophilic bacterium Acidithiobacillus ferrooxidans . Biochemistry 2005; 44:6471–6481 [View Article][PubMed]
     [Google Scholar]
  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; 70:4491–4498 [View Article][PubMed]
     [Google Scholar]
  31. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011; 8:785–786 [View Article][PubMed]
     [Google Scholar]
  32. Nuñez H, Moya-Beltrán A, Covarrubias PC, Issotta F, Cárdenas JP et al. Molecular systematics of the genus Acidithiobacillus: insights into the phylogenetic structure and diversification of the taxon. Front Microbiol 2017; 8: http://journal.frontiersin.org/article/10.3389/fmicb.2017.00030 [View Article][PubMed]
     [Google Scholar]
  33. Pablo Cárdenas J, Ortiz R, Norris PR, Watkin E, Holmes DS. Reclassification of 'Thiobacillus prosperus' Huber and Stetter 1989 as Acidihalobacter prosperus gen. nov., sp. nov., a member of the family Ectothiorhodospiraceae . Int J Syst Evol Microbiol 2015; 65:3641–3644 [View Article][PubMed]
     [Google Scholar]
  34. Nicolle J Le C, Simmons S, Bathe S, Norris PR. Ferrous iron oxidation and rusticyanin in halotolerant, acidophilic 'Thiobacillus prosperus'. Microbiology 2009; 155:1302–1309 [View Article][PubMed]
     [Google Scholar]
  35. Norris PR, Davis-Belmar CS, Nicolle J Le C, Calvo-Bado LA, Angelatou V. Pyrite oxidation and copper sulfide ore leaching by halotolerant, thermotolerant bacteria. Hydrometallurgy 2010; 104:432–436 [View Article]
     [Google Scholar]
  36. Norris PR, Simmons S. Pyrite oxidation by halotolerant, acidophilic bacteria. In Tsezos M, Hatzikioseyian A, Remoundaki E. (editors) Biohydrometallurgy Athens, Greece: National Technical University of Athens; 2004 pp. 1347–1351
     [Google Scholar]
  37. Pronk JT, de Bruyn JC, Bos P, Kuenen JG. Anaerobic growth of Thiobacillus ferrooxidans . Appl Environ Microbiol 1992; 58:2227–2230[PubMed]
     [Google Scholar]
  38. Brasseur G, Bruscella P, Bonnefoy V, Lemesle-Meunier D. The bc 1 complex of the iron-grown acidophilic chemolithotrophic bacterium Acidithiobacillus ferrooxidans functions in the reverse but not in the forward direction. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2002; 1555:37–43 [View Article]
     [Google Scholar]
  39. Yarzábal A, Appia-Ayme C, Ratouchniak J, Bonnefoy V. Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin. Microbiology 2004; 150:2113–2123 [View Article][PubMed]
     [Google Scholar]
  40. Jeans C, Singer SW, Chan CS, Verberkmoes NC, Shah M et al. Cytochrome 572 is a conspicuous membrane protein with iron oxidation activity purified directly from a natural acidophilic microbial community. ISME J 2008; 2:542–550 [View Article][PubMed]
     [Google Scholar]
  41. Ullrich SR, Poehlein A, Tischler JS, González C, Ossandon FJ et al. Genome analysis of the biotechnologically relevant acidophilic iron oxidising strain JA12 indicates phylogenetic and metabolic diversity within the novel genus "Ferrovum". PLoS One 2016; 11:e0146832 [View Article][PubMed]
     [Google Scholar]
  42. Ullrich SR, Poehlein A, Levicán GJ, Schlömann M, Mühling M. Molecular response of the acidophilic iron oxidizer “Ferrovum” sp. JA12 to the exposure to elevated concentrations of ferrous iron. Solid State Phenomena 2017; 262:482–486 [View Article]
     [Google Scholar]
  43. Hallberg KB, Hedrich S, Johnson DB. Acidiferrobacter thiooxydans, gen. nov. sp. nov.; an acidophilic, thermo-tolerant, facultatively anaerobic iron- and sulfur-oxidizer of the family Ectothiorhodospiraceae . Extremophiles 2011; 15:271–279 [View Article][PubMed]
     [Google Scholar]
  44. Norris PR, Gould OJP, Ogden TJ. Iron solubilization during anaerobic growth of acidophilic microorganisms with a polymetallic sulfide ore. Miner Eng 2015; 75:77–84 [View Article]
     [Google Scholar]
  45. Barr DW, Ingledew WJ, Norris PR. Respiratory chain components of iron-oxidizing acidophilic bacteria. FEMS Microbiol Lett 1990; 70:85–89 [View Article]
     [Google Scholar]
  46. Blake RC, Shute EA, Greenwood MM, Spencer GH, Ingledew WJ. Enzymes of aerobic respiration on iron. FEMS Microbiol Rev 1993; 11:9–18 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000616
Loading
Cytochromes in anaerobic growth of Acidithiobacillus ferrooxidans
Microbiology 164, 383 (2018); https://doi.org/10.1099/mic.0.000616
/content/journal/micro/10.1099/mic.0.000616
/content/journal/micro/10.1099/mic.0.000616
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error