Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Insights into Systems for Iron-Sulfur Cluster Biosynthesis in Acidophilic Microorganisms

  • Myriam, Perez (Universidad de Santiago de Chile (USACH), Facultad de Quimica y Biologia, Departamento de Biologia.) ;
  • Braulio, Paillavil (Universidad de Santiago de Chile (USACH), Facultad de Quimica y Biologia, Departamento de Biologia.) ;
  • Javiera, Rivera-Araya (Universidad de Santiago de Chile (USACH), Facultad de Quimica y Biologia, Departamento de Biologia.) ;
  • Claudia, Munoz-Villagran (Universidad de Santiago de Chile (USACH), Facultad de Quimica y Biologia, Departamento de Biologia.) ;
  • Omar, Orellana (Universidad de Chile, Facultad de Medicina, Instituto de Ciencias Biomedicas) ;
  • Renato, Chavez (Universidad de Santiago de Chile (USACH), Facultad de Quimica y Biologia, Departamento de Biologia.) ;
  • Gloria, Levican (Universidad de Santiago de Chile (USACH), Facultad de Quimica y Biologia, Departamento de Biologia.)
  • Received : 2022.06.23
  • Accepted : 2022.08.17
  • Published : 2022.09.28
Download PDF
⟨ Previous Next ⟩

Abstract

Fe-S clusters are versatile and essential cofactors that participate in multiple and fundamental biological processes. In Escherichia coli, the biogenesis of these cofactors requires either the housekeeping Isc pathway, or the stress-induced Suf pathway which plays a general role under conditions of oxidative stress or iron limitation. In the present work, the Fe-S cluster assembly Isc and Suf systems of acidophilic Bacteria and Archaea, which thrive in highly oxidative environments, were studied. This analysis revealed that acidophilic microorganisms have a complete set of genes encoding for a single system (either Suf or Isc). In acidophilic Proteobacteria and Nitrospirae, a complete set of isc genes (iscRSUAX-hscBA-fdx), but not genes coding for the Suf system, was detected. The activity of the Isc system was studied in Leptospirillum sp. CF-1 (Nitrospirae). RT-PCR experiments showed that eight candidate genes were co-transcribed and conform the isc operon in this strain. Additionally, RT-qPCR assays showed that the expression of the iscS gene was significantly up-regulated in cells exposed to oxidative stress imposed by 260 mM Fe2(SO4)3 for 1 h or iron starvation for 3 h. The activity of cysteine desulfurase (IscS) in CF-1 cell extracts was also upregulated under such conditions. Thus, the Isc system from Leptospirillum sp. CF-1 seems to play an active role in stressful environments. These results contribute to a better understanding of the distribution and role of Fe-S cluster protein biogenesis systems in organisms that thrive in extreme environmental conditions.

Keywords

Acknowledgement

This study was funded by grants from Fondo Nacional de Desarrollo Cientifico y Tecnologico from the government of Chile (Fondecyt 170799/1211386) and the research fund from Dicyt-USACH (021943LJ_POSTDOC).

References

  1. Roche B, Aussel L, Ezraty B, Mandin P, Py B, Barras F. 2013. Iron/sulfur proteins biogenesis in prokaryotes: formation, regulation and diversity. Biochim. Biophys. Acta 1827: 455-469. https://doi.org/10.1016/j.bbabio.2012.12.010
  2. Fontecave M, Ollagnier-de-Choudens S. 2008. Iron-sulfur cluster biosynthesis in bacteria: mechanisms of cluster assembly and transfer. Arch. Biochem. Biophys. 474: 226-237. https://doi.org/10.1016/j.abb.2007.12.014
  3. Blanc B, Gerez C, Ollagnier de Choudens S. 2015. Assembly of Fe/S proteins in bacterial systems: biochemistry of the bacterial ISC system. Biochim. Biophys. Acta 1853: 1436-1447. https://doi.org/10.1016/j.bbamcr.2014.12.009
  4. Beinert, H. 2000. Iron-sulfur proteins: ancient structures, still full of surprises. J. Biol. Inorg. Chem. 5: 2-15. https://doi.org/10.1007/s007750050002
  5. Brzoska K, Meczynska S, Kruszewski M. 2006. Iron-sulfur cluster proteins: electron transfer and beyond. Acta Biochim. Pol. 53: 685-691. https://doi.org/10.18388/abp.2006_3296
  6. Khodour Y, Kaguni LS, Stiban J. 2019. Iron-sulfur clusters in nucleic acid metabolism: varying roles of ancient cofactors. Enzymes 45: 225-256. https://doi.org/10.1016/bs.enz.2019.08.003
  7. Imlay JA. 2021. Where in the world do bacteria experience oxidative stress? Environ. Microbiol. 21: 521-530. https://doi.org/10.1111/1462-2920.14445
  8. Perard J, Ollagnier de Choudens S. 2018. Iron-sulfur clusters biogenesis by the SUF machinery: close to the molecular mechanism understanding. J. Biol. Inorg. Chem. 23: 581-596. https://doi.org/10.1007/s00775-017-1527-3
  9. Baussier C, Fakroun S, Aubert C, Dubrac S, Mandin P, Py B, et al. 2020. Making iron-sulfur cluster: structure, regulation and evolution of the bacterial ISC system. Adv. Microb. Physiol. 76: 1-39. https://doi.org/10.1016/bs.ampbs.2020.01.001
  10. Outten FW, Djaman O, Storz G. 2004. A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli. Mol. Microbiol. 52: 861-872. https://doi.org/10.1111/j.1365-2958.2004.04025.x
  11. Yeo WS, Lee JH, Lee KC, Roe JH. 2006. IscR acts as an activator in response to oxidative stress for the suf operon encoding Fe-S assembly proteins. Mol. Microbiol. 61: 206-218. https://doi.org/10.1111/j.1365-2958.2006.05220.x
  12. Jang S, Imlay JA. 2010. Hydrogen peroxide inactivates the Escherichia coli Isc iron-sulphur assembly system, and OxyR induces the Suf system to compensate. Mol. Microbiol. 78: 1448-1467. https://doi.org/10.1111/j.1365-2958.2010.07418.x
  13. Lee KC, Yeo WS, Roe JH. 2008. Oxidant-responsive induction of the suf operon, encoding a Fe-S assembly system, through Fur and IscR in Escherichia coli. J. Bacteriol. 190: 8244-8247. https://doi.org/10.1128/JB.01161-08
  14. Roche B, Agrebi R, Huguenot A, Ollagnier de Choudens S, Barras F, Py B. 2015. Turning Escherichia coli into a frataxin-dependent organism. PLoS Genet. 11: e1005134. https://doi.org/10.1371/journal.pgen.1005134
  15. Lill R. 2009. Function and biogenesis of iron-sulphur proteins. Nature 460: 831-838. https://doi.org/10.1038/nature08301
  16. Ayala-Castro C, Saini A, Outten FW. 2008. Fe-S Cluster assembly pathways in bacteria. Microbiol. Mol. Biol. Rev. 72: 110-125. https://doi.org/10.1128/MMBR.00034-07
  17. Rosario-Cruz Z, Boyd JM. 2016. Physiological roles of bacillithiol in intracellular metal processing. Curr. Genet. 62: 59-65. https://doi.org/10.1007/s00294-015-0511-0
  18. Lim S, Jung JH, Blanchard L, de Groot A. 2019. Conservation and diversity of radiation and oxidative stress resistance mechanisms in Deinococcus species. FEMS Microbiol. Rev. 43: 19-52. https://doi.org/10.1093/femsre/fuy037
  19. Jones G, Corin KC, Van Hille R, Harrison STL. 2011. The generation of toxic reactive oxygen species (ROS) from mechanically activated sulphide concentrates and its effect on thermophilic bioleaching. Miner. Eng. 24: 1908-1208.
  20. Ferrer A, Orellana O, Levicaan G. 2016. Chapter 4 - Oxidative stress and metal tolerance in extreme acidophiles. pp. 63-76. In Acidophiles: life in extremely acidic environments. Quatrini, R. and Johnson, D. (eds.): Caister Academic Press.
  21. Ferrer M, Golyshina OV, Beloqui A, Golyshin PN, Timmis KN. 2007. The cellular machinery of Ferroplasma acidiphilum is iron-protein-dominated. Nature 445: 91-94. https://doi.org/10.1038/nature05362
  22. Bruscella P, Appia-Ayme C, Levican G, Ratouchniak J, Jedlicki E, Holmes DS, et al. 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(Pt 1): 102-110. https://doi.org/10.1099/mic.0.2006/000067-0
  23. ten Brink F, Schoepp-Cothenet B, van Lis R, Nitschke W, Baymann F. 2013. Multiple Rieske/cyt b complexes in a single organism. Biochim. Biophys. Acta 1827: 1392-1406. https://doi.org/10.1016/j.bbabio.2013.03.003
  24. Belnap CP, Pan C, VerBerkmoes NC, Power ME, Samatova NF, Carver RL, et al. 2010. Cultivation and quantitative proteomic analyses of acidophilic microbial communities. ISME J. 4: 520-530. https://doi.org/10.1038/ismej.2009.139
  25. Norambuena J, Flores R, Cardenas JP, Quatrini R, Chavez R, Levican G. 2012. Thiol/Disulfide system plays a crucial role in redox protection in the acidophilic iron-oxidizing bacterium Leptospirillum ferriphilum. PLoS One 7: e44576. https://doi.org/10.1371/journal.pone.0044576
  26. Rivera-Araya J, Pollender A, Huynh D, Schlomann M, Chavez R, Levican G. 2019. Osmotic imbalance, cytoplasm acidification and oxidative stress induction support the high toxicity of chloride in acidophilic bacteria. Front. Microbiol. 10: 2455. https://doi.org/10.3389/fmicb.2019.02455
  27. Ferrer A, Bunk B, Sproer C, Biedendieck R, Valdes N, Jahn M, et al. 2016. Complete genome sequence of the bioleaching bacterium Leptospirillum sp. group II strain CF-1. J. Biotechnol. 222: 21-22. https://doi.org/10.1016/j.jbiotec.2016.02.008
  28. Zheng L, White RH, Cash VL, Jack RF, Dean DR. 1993. Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc. Natl. Acad. Sci. USA 90: 2754-2758. https://doi.org/10.1073/pnas.90.7.2754
  29. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35: 1547-1549. https://doi.org/10.1093/molbev/msy096
  30. Ghosal D, Omelchenko MV, Gaidamakova EK, Matrosova VY, Vasilenko A, Venkateswaran A, et al. 2005. How radiation kills cells: survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress. FEMS Microbiol. Rev. 29: 361-375. https://doi.org/10.1016/j.fmrre.2004.12.007
  31. Cardenas JP, Moya F, Covarrubias P, Shmaryahu A, Levican G, Holmes DS, et al. 2012. Comparative genomics of the oxidative stress response in bioleaching microorganisms. Hydrometallurgy 12: 162-167.
  32. Fujishiro T, Ryosuke Nakamura R, Kouhei Kunichika K, Takahashi Y. 2022. Structural diversity of cysteine desulfurases involved in iron-sulfur cluster biosynthesis. Biophys. Physicobiol. 19: 1-18.
  33. Tian T, He H, Liu XQ. 2014. The SufBCD protein complex is the scaffold for iron-sulfur cluster assembly in Thermus thermophiles HB8. Biochem. Biophys. Res. Commun. 443: 376-381. https://doi.org/10.1016/j.bbrc.2013.11.131
  34. Gonzalez D, Alamos P, Rivero M, Orellana O, Norambuena J, Chavez R, et al. 2020. Deciphering the role of multiple thioredoxin fold proteins of Leptospirillum sp. in oxidative stress tolerance. Int. J. Mol. Sci. 21: 1880. https://doi.org/10.3390/ijms21051880
  35. Farias R, Norambuena J, Ferrer A, Camejo P, Zapata C, Chavez R, et al. 2021. Redox stress response and UV tolerance in the acidophilic iron-oxidizing bacteria Leptospirillum ferriphilum and Acidithiobacillus ferrooxidans. Res. Microbiol. 172: 103833. https://doi.org/10.1016/j.resmic.2021.103833
  36. Mihara H, Esaki N. 2002. Bacterial cysteine desulfurases: their function and mechanisms. Appl. Microbiol. Biotechnol. 60: 12-23. https://doi.org/10.1007/s00253-002-1107-4
  37. Slade D, Radman M. 2011. Oxidative stress resistance in Deinococcus radiodurans. Microbiol. Mol. Biol. Rev. 75: 133-191. https://doi.org/10.1128/MMBR.00015-10
  38. Andreini C, Antonio Rosato A, Banci L. 2017. The relationship between environmental dioxygen and Iron-Sulfur proteins explored at the genome level. PLoS One 12: e0171279. https://doi.org/10.1371/journal.pone.0171279
  39. Potrykus J, Rao W, Dopson M. 2010. Iron homeostasis and responses to iron limitation in extreme acidophiles from the Ferroplasma genus. Proteomics 11: 52-63. https://doi.org/10.1002/pmic.201000193
  40. Iwasaki T. 2010. Iron-sulfur world in aerobic and hyperthermoacidophilic archaea Sulfolobus. Archaea 2010: 842639. https://doi.org/10.1155/2010/842639
  41. Johnson C, England A, Munro-Ehrlich M, Colman DR, DuBois JL, Boyd ES. 2021. Pathways of iron and sulfur acquisition, cofactor assembly, destination, and storage in diverse archaeal methanogens and alkanotrophs. J. Bacteriol. 203: e0011721.
  42. Liu Y, Sieprawska-Lupa M, Whitman WB, White RH. 2010. Cysteine is not the methanogenic archaeon Methanococcus maripaludis. J. Biol. Chem. 285: 31923-31929. https://doi.org/10.1074/jbc.M110.152447
  43. Tokumoto U, Kitamura S, Fukuyama K, Takahashi Y. 2004. Interchangeability and distinct properties of bacterial Fe-S cluster assembly systems: functional replacement of the isc and suf operons in Escherichia coli with the nifSU-like operon from Helicobacter pylori. J. Biochem. 136: 199-209. https://doi.org/10.1093/jb/mvh104
  44. Pascal LE, True LD, Campbell DS, Deutsch EW, Risk M, Coleman IM, et al. 2008. Correlation of mRNA and protein levels: cell typespecific gene expression of cluster designation antigens in the prostate. BMC Genomics 9: 246. https://doi.org/10.1186/1471-2164-9-246
  45. Schwartz CJ, Giel JL, Patschkowski T, Luther C, Ruzicka FJ, Beinert H, et al. 2001. IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. Proc. Natl. Acad. Sci. USA 98: 14895-14900. https://doi.org/10.1073/pnas.251550898
  46. Giel JL, Nesbit AD, Mettert EL, Fleischhacker AS, Wanta BT, Kiley PJ. 2013. Regulation of iron-sulphur cluster homeostasis through transcriptional control of the Isc pathway by [2Fe-2S]-IscR in Escherichia coli. Mol. Microbiol. 87: 478-492. https://doi.org/10.1111/mmi.12052
  47. Osorio H, Martinez V, Nieto PA, Holmes DH, Quatrini R. 2008. Microbial iron management mechanisms in extremely acidic environments: comparative genomics evidence for diversity and versatility. BMC Microbiol. 8: 203. https://doi.org/10.1186/1471-2180-8-203