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Alves MN, Neto SE, Alves AS, et al. Characterization of the periplasmic redox network that sustains the versatile anaerobic metabolism of Shewanella oneidensis MR-1. Front Microbiol. 2015;6:665doi: 10.3389/fmicb.2015.00665.
Alves, M. N., Neto, S. E., Alves, A. S., Fonseca, B. M., Carrêlo, A., Pacheco, I., Paquete, C. M., Soares, C. M., & Louro, R. O. (2015). Characterization of the periplasmic redox network that sustains the versatile anaerobic metabolism of Shewanella oneidensis MR-1. Frontiers in microbiology, 6665. https://doi.org/10.3389/fmicb.2015.00665
Alves, Mónica N, et al. "Characterization of the periplasmic redox network that sustains the versatile anaerobic metabolism of Shewanella oneidensis MR-1." Frontiers in microbiology vol. 6 (2015): 665. doi: https://doi.org/10.3389/fmicb.2015.00665
Alves MN, Neto SE, Alves AS, Fonseca BM, Carrêlo A, Pacheco I, Paquete CM, Soares CM, Louro RO. Characterization of the periplasmic redox network that sustains the versatile anaerobic metabolism of Shewanella oneidensis MR-1. Front Microbiol. 2015 Jun 29;6:665. doi: 10.3389/fmicb.2015.00665. eCollection 2015. PMID: 26175726; PMCID: PMC4484225.
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Front Microbiol. 2015 Jun 29;6:665. doi: 10.3389/fmicb.2015.00665. eCollection 2015.

Characterization of the periplasmic redox network that sustains the versatile anaerobic metabolism of Shewanella oneidensis MR-1.

Frontiers in microbiology

Mónica N Alves, Sónia E Neto, Alexandra S Alves, Bruno M Fonseca, Afonso Carrêlo, Isabel Pacheco, Catarina M Paquete, Cláudio M Soares, Ricardo O Louro

Affiliations

  1. Inorganic Biochemistry and NMR Laboratory, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa Oeiras, Portugal.

PMID: 26175726 PMCID: PMC4484225 DOI: 10.3389/fmicb.2015.00665

Abstract

The versatile anaerobic metabolism of the Gram-negative bacterium Shewanella oneidensis MR-1 (SOMR-1) relies on a multitude of redox proteins found in its periplasm. Most are multiheme cytochromes that carry electrons to terminal reductases of insoluble electron acceptors located at the cell surface, or bona fide terminal reductases of soluble electron acceptors. In this study, the interaction network of several multiheme cytochromes was explored by a combination of NMR spectroscopy, activity assays followed by UV-visible spectroscopy and comparison of surface electrostatic potentials. From these data the small tetraheme cytochrome (STC) emerges as the main periplasmic redox shuttle in SOMR-1. It accepts electrons from CymA and distributes them to a number of terminal oxidoreductases involved in the respiration of various compounds. STC is also involved in the electron transfer pathway to reduce nitrite by interaction with the octaheme tetrathionate reductase (OTR), but not with cytochrome c nitrite reductase (ccNiR). In the main pathway leading the metal respiration STC pairs with flavocytochrome c (FccA), the other major periplasmic cytochrome, which provides redundancy in this important pathway. The data reveals that the two proteins compete for the binding site at the surface of MtrA, the decaheme cytochrome inserted on the periplasmic side of the MtrCAB-OmcA outer-membrane complex. However, this is not observed for the MtrA homologues. Indeed, neither STC nor FccA interact with MtrD, the best replacement for MtrA, and only STC is able to interact with the decaheme cytochrome DmsE of the outer-membrane complex DmsEFABGH. Overall, these results shown that STC plays a central role in the anaerobic respiratory metabolism of SOMR-1. Nonetheless, the trans-periplasmic electron transfer chain is functionally resilient as a consequence of redundancies that arise from the presence of alternative pathways that bypass/compete with STC.

Keywords: Shewanella oneidensis MR-1; dissociation constant; electron transfer; electrostatics; extracellular respiration; paramagnetic NMR; periplasmic cytochromes

References

  1. Appl Environ Microbiol. 2009 Aug;75(16):5209-17 - PubMed
  2. Appl Environ Microbiol. 2013 Feb;79(4):1150-9 - PubMed
  3. Nucleic Acids Res. 2009 Jan;37(Database issue):D387-92 - PubMed
  4. FEMS Microbiol Rev. 2002 Aug;26(3):285-309 - PubMed
  5. J Bioenerg Biomembr. 2008 Oct;40(5):493-9 - PubMed
  6. Nat Rev Cancer. 2007 Mar;7(3):202-11 - PubMed
  7. Metallomics. 2011 Apr;3(4):344-8 - PubMed
  8. ISME J. 2015 Aug;9(8):1802-11 - PubMed
  9. Biochemistry. 1990 Nov 6;29(44):10219-25 - PubMed
  10. J Biol Inorg Chem. 2012 Apr;17(4):647-62 - PubMed
  11. Bioinformatics. 2006 Jan 15;22(2):195-201 - PubMed
  12. J Bacteriol. 2002 Feb;184(3):846-8 - PubMed
  13. Structure. 2010 Oct 13;18(10):1233-43 - PubMed
  14. J Biol Chem. 2003 Jul 25;278(30):27758-65 - PubMed
  15. Science. 1988 Jun 3;240(4857):1319-21 - PubMed
  16. Annu Rev Microbiol. 2007;61:237-58 - PubMed
  17. Lett Appl Microbiol. 1997 Sep;25(3):162-8 - PubMed
  18. Mol Microbiol. 2010 Aug;77(4):995-1008 - PubMed
  19. J Biol Inorg Chem. 2007 Sep;12(7):1083-94 - PubMed
  20. Nat Rev Microbiol. 2008 Aug;6(8):592-603 - PubMed
  21. J Am Chem Soc. 2011 Oct 26;133(42):16861-7 - PubMed
  22. FEBS J. 2011 May;278(9):1391-400 - PubMed
  23. Appl Environ Microbiol. 2001 Jul;67(7):3236-44 - PubMed
  24. Biotechniques. 2005 Feb;38(2):297-9 - PubMed
  25. Nat Rev Microbiol. 2006 Jul;4(7):497-508 - PubMed
  26. J Biol Chem. 2005 Mar 4;280(9):7925-31 - PubMed
  27. J Biol Inorg Chem. 2009 Mar;14(3):375-85 - PubMed
  28. Biochemistry. 2009 Dec 8;48(48):11390-8 - PubMed
  29. Biol Chem. 2004 Oct;385(10):875-83 - PubMed
  30. Biochim Biophys Acta. 2010 Sep;1797(9):1563-72 - PubMed
  31. Acc Chem Res. 2003 Oct;36(10):723-30 - PubMed
  32. Nat Struct Mol Biol. 2004 Oct;11(10):1023-4 - PubMed
  33. Mol Microbiol. 2007 Jul;65(1):1-11 - PubMed
  34. Science. 2012 Aug 10;337(6095):686-90 - PubMed
  35. Proc Natl Acad Sci U S A. 2009 Dec 29;106(52):22169-74 - PubMed
  36. Eur J Biochem. 1995 Sep 1;232(2):522-7 - PubMed
  37. Biochem J. 2013 Jan 1;449(1):101-8 - PubMed
  38. Anal Biochem. 1984 Feb;136(2):509-14 - PubMed
  39. Annu Rev Microbiol. 1994;48:311-43 - PubMed
  40. J Am Chem Soc. 2002 Oct 2;124(39):11737-45 - PubMed
  41. FEBS Lett. 2005 May 23;579(13):2891-6 - PubMed
  42. Biochemistry. 2003 Jun 17;42(23):7068-76 - PubMed
  43. Biochim Biophys Acta. 1995 Dec 12;1232(3):97-173 - PubMed
  44. Biochemistry. 2003 Aug 12;42(31):9491-7 - PubMed
  45. Front Microbiol. 2012 Feb 21;3:56 - PubMed
  46. Biochim Biophys Acta. 1959 Jul;34:255-6 - PubMed
  47. Biochemistry. 2012 Dec 21;51(51):10175-85 - PubMed
  48. Biochim Biophys Acta. 2009 Feb;1787(2):113-20 - PubMed
  49. Biochem J. 2012 Jun 15;444(3):465-74 - PubMed
  50. Nat Biotechnol. 2002 Nov;20(11):1118-23 - PubMed
  51. Mol Microbiol. 2012 Jul;85(2):201-12 - PubMed
  52. J Bacteriol. 2000 Jan;182(1):67-75 - PubMed
  53. FEBS Lett. 2007 Aug 7;581(20):3805-8 - PubMed

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