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Biophysical and structural characterization of the putative nickel chaperone CooT from Carboxydothermus hydrogenoformans

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Abstract

Carboxydothermus hydrogenoformans is a model microorganism for the study of [NiFe]–CODH, a key enzyme of carbon cycle in anaerobic microorganisms. The enzyme possesses a unique active site (C-cluster), constituted of a distorted [NiFe3S4] cubane linked to a mononuclear Fe(II) center. Both the biogenesis of the C-cluster and the activation of CODH by nickel insertion remain unclear. Among the three accessory proteins thought to play a role in this latter step (CooC, CooJ, and CooT), CooT is identified as a nickel chaperone involved in CODH maturation in Rhodospirillum rubrum. Here, we structurally and biophysically characterized a putative CooT protein present in C. hydrogenoformans (pChCooT). Despite the low sequence homologies between CooT from R. rubrum (RrCooT) and pChCooT (19% sequence identity), the two proteins share several similarities, such as their overall structure and a solvent-exposed Ni(II)-binding site at the dimer interface. Moreover, the X-ray structure of pChCooT reveals the proximity between the histidine 55, a potential nickel-coordinating residue, and the cysteine 2, a highly conserved key residue in Ni(II)-binding.

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References

  1. Fontecilla-Camps JC, Amara P, Cavazza C, Nicolet Y, Volbeda A (2009) Nature 460:814–822

    Article  PubMed  CAS  Google Scholar 

  2. Drennan CL, Peters JW (2003) Curr Opin Struct Biol 13:220–226

    Article  PubMed  CAS  Google Scholar 

  3. Peters JW, Schut GJ, Boyd ES, Mulder DW, Shepard EM, Broderick JB, King PW, Adams MWW (2015) Bba-Mol Cell Res 1853:1350–1369

    CAS  Google Scholar 

  4. Kung Y, Drennan CL (2011) Curr Opin Chem Biol 15:276–283

    Article  PubMed  CAS  Google Scholar 

  5. Wu M, Ren QH, Durkin AS, Daugherty SC, Brinkac LM, Dodson RJ, Madupu R, Sullivan SA, Kolonay JF, Nelson WC, Tallon LJ, Jones KM, Ulrich LE, Gonzalez JM, Zhulin IB, Robb FT, Eisen JA (2005) PLoS Genet 1:563–574

    Article  CAS  Google Scholar 

  6. Domnik L, Merrouch M, Goetzl S, Jeoung JH, Leger C, Dementin S, Fourmond V, Dobbek H (2017) Angew Chem Int Ed 56:15466–15469

    Article  CAS  Google Scholar 

  7. Drennan CL, Heo JY, Sintchak MD, Schreiter E, Ludden PW (2001) Proc Natl Acad Sci USA 98:11973–11981

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Dobbek H, Svetlitchnyi V, Gremer L, Huber R, Meyer O (2001) Science 293:1281–1285

    Article  PubMed  CAS  Google Scholar 

  9. Fesseler J, Jeoung JH, Dobbek H (2015) Angew Chem Int Ed 54:8560–8564

    Article  CAS  Google Scholar 

  10. Ribbe MW (2015) Angew Chem Int Ed 54:8337–8339

    Article  CAS  Google Scholar 

  11. Ciaccafava A, Tombolelli D, Domnik L, Jeoung JH, Dobbek H, Mroginski MA, Zebger I, Hildebrandt P (2017) Angew Chem Int Ed 56:7398–7401

    Article  CAS  Google Scholar 

  12. Spangler NJ, Lindahl PA, Bandarian V, Ludden PW (1996) J Biol Chem 271:7973–7977

    Article  PubMed  CAS  Google Scholar 

  13. Jeon WB, Singer SW, Ludden PW, Rubio LM (2005) J Biol Inorg Chem 10:903–912

    Article  PubMed  CAS  Google Scholar 

  14. Sydor AM, Lebrette H, Ariyakumaran R, Cavazza C, Zamble DB (2014) J Biol Chem 289:3828–3841

    Article  PubMed  CAS  Google Scholar 

  15. Maier T, Lottspeich F, Bock A (1995) Eur J Biochem 230:133–138

    Article  PubMed  CAS  Google Scholar 

  16. Yuen MH, Fong YH, Nim YS, Lau PH, Wong KB (2017) Proc Natl Acad Sci USA 114:10890–10898

    Article  CAS  Google Scholar 

  17. Zeer-Wanklyn CJ, Zamble DB (2017) Curr Opin Chem Biol 37:80–88

    Article  PubMed  CAS  Google Scholar 

  18. Jeoung JH, Giese T, Grunwald M, Dobbek H (2009) Biochemistry 48:11505–11513

    Article  PubMed  CAS  Google Scholar 

  19. Gregg CM, Goetzl S, Jeoung JH, Dobbek H (2016) J Biol Chem 291:18129–18138

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Inoue T, Takao K, Fukuyama Y, Yoshida T, Sako Y (2014) Biosci Biotech Bioch 78:582–587

    Article  CAS  Google Scholar 

  21. Kerby RL, Hong SS, Ensign SA, Coppoc LJ, Ludden PW, Roberts GP (1992) J Bacteriol 174:5284–5294

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Jeon WB, Cheng JJ, Ludden PW (2001) J Biol Chem 276:38602–38609

    Article  PubMed  CAS  Google Scholar 

  23. Kerby RL, Ludden PW, Roberts GP (1997) J Bacteriol 179:2259–2266

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Watt RK, Ludden PW (1998) J Biol Chem 273:10019–10025

    Article  PubMed  CAS  Google Scholar 

  25. Timm J, Brochier-Armanet C, Perard J, Zambelli B, Ollagnier-de-Choudens S, Ciurli S, Cavazza C (2017) Metallomics 9:575–583

    Article  PubMed  CAS  Google Scholar 

  26. Kabsch W (2010) Acta Crystallogr Sect D-Biol Crystallogr 66:125–132

    Article  CAS  Google Scholar 

  27. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) Acta Crystallogr Sect D-Biol Crystallogr 66:213–221

    Article  CAS  Google Scholar 

  28. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Acta Crystallogr Sect D-Biol Crystallogr 66:486–501

    Article  CAS  Google Scholar 

  29. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC (2010) Acta Crystallogr Sect D-Biol Crystallogr 66:12–21

    Article  CAS  Google Scholar 

  30. Joosten RP, Long F, Murshudov GN, Perrakis A (2014) IUCrJ 1:213–220

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Schut GJ, Lipscomb GL, Nguyen DMN, Kelly RM, Adams MWW (2016) Front Microbiol 7

  32. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) Nucleic Acids Res 44:D279–D285

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by “the ITERLIS PhD program, CEA Life sciences” for MA’s PhD funding, the “FUNBIOCO” project (IDEX-UGA, Initiatives de Recherche stratégiques) and the “COSYNBIO” project (Projets exploratoires, Cellule energie-CNRS). This work has been partially supported by the Labex ARCANE (ANR-11-LABX-0003-01). The research leading to these results has also received funding from the European Community (iNEXT support, Project ID no. 2310). We thank the High Throughput Crystallization Laboratory (HTX Lab) at the EMBL Grenoble for pChCooT crystallization. We thank the staffs from the BM-30A beamline of the European Synchrotron Facility in Grenoble. We thank Dr. Luca Signor (IBS, Grenoble) for mass spectrometry experiments in denaturing conditions (Integrated Structural Biology Grenoble platform).

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Authors and Affiliations

  1. University of Grenoble Alpes, CEA, CNRS, BIG, CBM, 38000, Grenoble, France

    M. Alfano, J. Pérard, R. Miras, P. Catty & C. Cavazza

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  1. M. Alfano
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  2. J. Pérard
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  3. R. Miras
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  4. P. Catty
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  5. C. Cavazza
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Correspondence to C. Cavazza.

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Alfano, M., Pérard, J., Miras, R. et al. Biophysical and structural characterization of the putative nickel chaperone CooT from Carboxydothermus hydrogenoformans. J Biol Inorg Chem 23, 809–817 (2018). https://doi.org/10.1007/s00775-018-1576-2

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  • DOI: https://doi.org/10.1007/s00775-018-1576-2

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