1887

Abstract

Disulfide bonds confer stability and activity to proteins. Bioinformatic approaches allow predictions of which organisms make protein disulfide bonds and in which subcellular compartments disulfide bond formation takes place. Such an analysis, along with biochemical and protein structural data, suggests that many of the extremophile Crenarachaea make protein disulfide bonds in both the cytoplasm and the cell envelope. We have sought to determine the oxidative folding pathways in the sequenced genomes of the Crenarchaea, by seeking homologues of the enzymes known to be involved in disulfide bond formation in bacteria. Some Crenarchaea have two homologues of the cytoplasmic membrane protein VKOR, a protein required in many bacteria for the oxidation of bacterial DsbAs. We show that the two VKORs of assume opposite orientations in the cytoplasmic membrane, when expressed in One has its active cysteines oriented toward the periplasm (VKORo) and the other toward the cytoplasm (VKORi). Furthermore, the VKORo promotes disulfide bond formation in the cell envelope, while the VKORi promotes disulfide bond formation in the cytoplasm via a co-expressed archaeal protein PDO. Amongst the VKORs from different archaeal species, the pairs of VKORs in each species are much more closely related to each other than to the VKORs of the other species. The results suggest two independent occurrences of the evolution of the two topologically inverted VKORs in archaea. Our results suggest a mechanistic basis for the formation of disulfide bonds in the cytoplasm of Crenarchaea.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000569
2017-12-01
2019-12-06
Loading full text...

Full text loading...

/deliver/fulltext/micro/163/12/1864.html?itemId=/content/journal/micro/10.1099/mic.0.000569&mimeType=html&fmt=ahah

References

  1. Albers SV, Meyer BH. The archaeal cell envelope. Nat Rev Microbiol 2011;9:414–426 [CrossRef][PubMed]
    [Google Scholar]
  2. Bardwell JC, McGovern K, Beckwith J. Identification of a protein required for disulfide bond formation in vivo. Cell 1991;67:581–589 [CrossRef][PubMed]
    [Google Scholar]
  3. Frand AR, Kaiser CA. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell 1998;1:161–170 [CrossRef][PubMed]
    [Google Scholar]
  4. Tu BP, Ho-Schleyer SC, Travers KJ, Weissman JS. Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 2000;290:1571–1574[PubMed][Crossref]
    [Google Scholar]
  5. Derman AI, Prinz WA, Belin D, Beckwith J. Mutations that allow disulfide bond formation in the cytoplasm of Escherichia coli. Science 1993;262:1744–1747 [CrossRef][PubMed]
    [Google Scholar]
  6. Stewart EJ, Aslund F, Beckwith J. Disulfide bond formation in the Escherichia coli cytoplasm: an in vivo role reversal for the thioredoxins. Embo J 1998;17:5543–5550 [CrossRef][PubMed]
    [Google Scholar]
  7. Bessette PH, Aslund F, Beckwith J, Georgiou G. Efficient folding of proteins with multiple disulfide bonds in the Escherichia coli cytoplasm. Proc Natl Acad Sci USA 1999;96:13703–13708 [CrossRef][PubMed]
    [Google Scholar]
  8. Hatahet F, Nguyen VD, Salo KE, Ruddock LW. Disruption of reducing pathways is not essential for efficient disulfide bond formation in the cytoplasm of E. coli. Microb Cell Fact 2010;9:67 [CrossRef][PubMed]
    [Google Scholar]
  9. Lobstein J, Emrich CA, Jeans C, Faulkner M, Riggs P et al. SHuffle, a novel Escherichia coli protein expression strain capable of correctly folding disulfide bonded proteins in its cytoplasm. Microb Cell Fact 2012;11:1 [CrossRef][PubMed]
    [Google Scholar]
  10. White CL, Senkevich TG, Moss B. Vaccinia virus G4L glutaredoxin is an essential intermediate of a cytoplasmic disulfide bond pathway required for virion assembly. J Virol 2002;76:467–472 [CrossRef][PubMed]
    [Google Scholar]
  11. Ren B, Tibbelin G, de Pascale D, Rossi M, Bartolucci S et al. A protein disulfide oxidoreductase from the archaeon Pyrococcus furiosus contains two thioredoxin fold units. Nat Struct Biol 1998;5:602–611 [CrossRef][PubMed]
    [Google Scholar]
  12. Mallick P, Boutz DR, Eisenberg D, Yeates TO. Genomic evidence that the intracellular proteins of archaeal microbes contain disulfide bonds. Proc Natl Acad Sci USA 2002;99:9679–9684 [CrossRef][PubMed]
    [Google Scholar]
  13. Beeby M, O'Connor BD, Ryttersgaard C, Boutz DR, Perry LJ et al. The genomics of disulfide bonding and protein stabilization in thermophiles. PLoS Biol 2005;3:e309 [CrossRef][PubMed]
    [Google Scholar]
  14. Toth EA, Worby C, Dixon JE, Goedken ER, Marqusee S et al. The crystal structure of adenylosuccinate lyase from Pyrobaculum aerophilum reveals an intracellular protein with three disulfide bonds. J Mol Biol 2000;301:433–450 [CrossRef][PubMed]
    [Google Scholar]
  15. King NP, Lee TM, Sawaya MR, Cascio D, Yeates TO. Structures and functional implications of an AMP-binding cystathionine β-synthase domain protein from a hyperthermophilic archaeon. J Mol Biol 2008;380:181–192 [CrossRef][PubMed]
    [Google Scholar]
  16. D'Ambrosio K, Pedone E, Langella E, De Simone G, Rossi M et al. A novel member of the protein disulfide oxidoreductase family from Aeropyrum pernix K1: structure, function and electrostatics. J Mol Biol 2006;362:743–752 [CrossRef][PubMed]
    [Google Scholar]
  17. Pedone E, Limauro D, D'Alterio R, Rossi M, Bartolucci S. Characterization of a multifunctional protein disulfide oxidoreductase from Sulfolobus solfataricus. Febs J 2006;273:5407–5420 [CrossRef][PubMed]
    [Google Scholar]
  18. Aberg A, Hahne S, Karlsson M, Larsson A, Ormö M et al. Evidence for two different classes of redox-active cysteines in ribonucleotide reductase of Escherichia coli. J Biol Chem 1989;264:12249–12252[PubMed]
    [Google Scholar]
  19. Zheng M, Aslund F, Storz G. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 1998;279:1718–1722 [CrossRef][PubMed]
    [Google Scholar]
  20. Pollitt S, Zalkin H. Role of primary structure and disulfide bond formation in beta-lactamase secretion. J Bacteriol 1983;153:27–32[PubMed]
    [Google Scholar]
  21. Derman AI, Beckwith J. Escherichia coli alkaline phosphatase fails to acquire disulfide bonds when retained in the cytoplasm. J Bacteriol 1991;173:7719–7722 [CrossRef][PubMed]
    [Google Scholar]
  22. Bardwell JC, Lee JO, Jander G, Martin N, Belin D et al. A pathway for disulfide bond formation in vivo. Proc Natl Acad Sci USA 1993;90:1038–1042 [CrossRef][PubMed]
    [Google Scholar]
  23. Kadokura H, Beckwith J. Four cysteines of the membrane protein DsbB act in concert to oxidize its substrate DsbA. Embo J 2002;21:2354–2363 [CrossRef][PubMed]
    [Google Scholar]
  24. Inaba K, Takahashi YH, Fujieda N, Kano K, Miyoshi H et al. DsbB elicits a red-shift of bound ubiquinone during the catalysis of DsbA oxidation. J Biol Chem 2004;279:6761–6768 [CrossRef][PubMed]
    [Google Scholar]
  25. Dutton RJ, Boyd D, Berkmen M, Beckwith J. Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc Natl Acad Sci USA 2008;105:11933–11938 [CrossRef][PubMed]
    [Google Scholar]
  26. Hatahet F, Ruddock LW. Topological plasticity of enzymes involved in disulfide bond formation allows catalysis in either the periplasm or the cytoplasm. J Mol Biol 2013;425:3268–3276 [CrossRef][PubMed]
    [Google Scholar]
  27. Manoil C, Beckwith J. A genetic approach to analyzing membrane protein topology. Science 1986;233:1403–1408 [CrossRef][PubMed]
    [Google Scholar]
  28. Wang X, Dutton RJ, Beckwith J, Boyd D. Membrane topology and mutational analysis of Mycobacterium tuberculosis VKOR, a protein involved in disulfide bond formation and a homologue of human vitamin K epoxide reductase. Antioxid Redox Signal 2011;14:1413–1420 [CrossRef][PubMed]
    [Google Scholar]
  29. Boyd D, Traxler B, Beckwith J. Analysis of the topology of a membrane protein by using a minimum number of alkaline phosphatase fusions. J Bacteriol 1993;175:553–556 [CrossRef][PubMed]
    [Google Scholar]
  30. Michaelis S, Inouye H, Oliver D, Beckwith J. Mutations that alter the signal sequence of alkaline phosphatase in Escherichia coli. 1983;154366–374
  31. Froshauer S, Green GN, Boyd D, McGovern K, Beckwith J. Genetic analysis of the membrane insertion and topology of MalF, a cytoplasmic membrane protein of Escherichia coli. J Mol Biol 1988;200:501–511 [CrossRef][PubMed]
    [Google Scholar]
  32. Hatahet F, Boyd D, Beckwith J. Disulfide bond formation in prokaryotes: history, diversity and design. Biochim Biophys Acta 2014;1844:1402–1414 [CrossRef][PubMed]
    [Google Scholar]
  33. Boyd D, Beckwith J. The role of charged amino acids in the localization of secreted and membrane proteins. Cell 1990;62:1031–1033 [CrossRef][PubMed]
    [Google Scholar]
  34. Prinz WA, Beckwith J. Gene fusion analysis of membrane protein topology: a direct comparison of alkaline phosphatase and β-lactamase fusions. J Bacteriol 1994;176:6410–6413 [CrossRef][PubMed]
    [Google Scholar]
  35. Sääf A, Johansson M, Wallin E, von Heijne G. Divergent evolution of membrane protein topology: the Escherichia coli RnfA and RnfE homologues. Proc Natl Acad Sci USA 1999;96:8540–8544 [CrossRef][PubMed]
    [Google Scholar]
  36. Rapp M, Granseth E, Seppälä S, von Heijne G. Identification and evolution of dual-topology membrane proteins. Nat Struct Mol Biol 2006;13:112–116 [CrossRef][PubMed]
    [Google Scholar]
  37. Chen YJ, Pornillos O, Lieu S, Ma C, Chen AP et al. X-ray structure of EmrE supports dual topology model. Proc Natl Acad Sci USA 2007;104:18999–19004 [CrossRef][PubMed]
    [Google Scholar]
  38. Schulman S, Wang B, Li W, Rapoport TA. Vitamin K epoxide reductase prefers ER membrane-anchored thioredoxin-like redox partners. Proc Natl Acad Sci USA 2010;107:15027–15032 [CrossRef][PubMed]
    [Google Scholar]
  39. Hatahet F, Blazyk JL, Martineau E, Mandela E, Zhao Y et al. Altered Escherichia coli membrane protein assembly machinery allows proper membrane assembly of eukaryotic protein vitamin K epoxide reductase. Proc Natl Acad Sci USA 2015;112:15184–15189 [CrossRef][PubMed]
    [Google Scholar]
  40. Dumoulin A, Grauschopf U, Bischoff M, Thöny-Meyer L, Berger-Bächi B. Staphylococcus aureus DsbA is a membrane-bound lipoprotein with thiol-disulfide oxidoreductase activity. Arch Microbiol 2005;184:117–128 [CrossRef][PubMed]
    [Google Scholar]
  41. Kouwen TR, van der Goot A, Dorenbos R, Winter T, Antelmann H et al. Thiol-disulphide oxidoreductase modules in the low-GC Gram-positive bacteria. Mol Microbiol 2007;64:984–999 [CrossRef][PubMed]
    [Google Scholar]
  42. Heras B, Kurz M, Jarrott R, Shouldice SR, Frei P et al. Staphylococcus aureus DsbA does not have a destabilizing disulfide. A new paradigm for bacterial oxidative folding. J Biol Chem 2008;283:4261–4271 [CrossRef][PubMed]
    [Google Scholar]
  43. Alvarez AF, Rodriguez C, Georgellis D. Ubiquinone and menaquinone electron carriers represent the yin and yang in the redox regulation of the ArcB sensor kinase. J Bacteriol 2013;195:3054–3061 [CrossRef][PubMed]
    [Google Scholar]
  44. Sonnhammer EL, Eddy SR, Durbin R. Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 1997;28:405–420 [CrossRef][PubMed]
    [Google Scholar]
  45. Eddy SR. Hidden Markov models. Curr Opin Struct Biol 1996;6:361–365 [CrossRef][PubMed]
    [Google Scholar]
  46. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997;25:3389–3402 [CrossRef][PubMed]
    [Google Scholar]
  47. Altschul SF, Gertz EM, Agarwala R, Schäffer AA, Yu YK. PSI-BLAST pseudocounts and the minimum description length principle. Nucleic Acids Res 2009;37:815–824 [CrossRef][PubMed]
    [Google Scholar]
  48. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32:1792–1797 [CrossRef][PubMed]
    [Google Scholar]
  49. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007;56:564–577 [CrossRef][PubMed]
    [Google Scholar]
  50. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003;52:696–704 [CrossRef][PubMed]
    [Google Scholar]
  51. Price MN, Dehal PS, Arkin AP. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 2010;5:e9490 [CrossRef][PubMed]
    [Google Scholar]
  52. Huson DH, Richter DC, Rausch C, Dezulian T, Franz M et al. Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 2007;8:460 [CrossRef][PubMed]
    [Google Scholar]
  53. Bernsel A, Viklund H, Hennerdal A, Elofsson A. TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res 2009;37:W465–W468 [CrossRef][PubMed]
    [Google Scholar]
  54. Käll L, Krogh A, Sonnhammer EL. A combined transmembrane topology and signal peptide prediction method. J Mol Biol 2004;338:1027–1036 [CrossRef][PubMed]
    [Google Scholar]
  55. Rahman O, Cummings SP, Harrington DJ, Sutcliffe IC. Methods for the bioinformatic identification of bacterial lipoproteins encoded in the genomes of Gram-positive bacteria. World J Microbiol Biotechnol 2008;24:2377–2382 [CrossRef]
    [Google Scholar]
  56. Boyd D, Weiss DS, Chen JC, Beckwith J. Towards single-copy gene expression systems making gene cloning physiologically relevant: lambda InCh, a simple Escherichia coli plasmid-chromosome shuttle system. J Bacteriol 2000;182:842–847 [CrossRef][PubMed]
    [Google Scholar]
  57. Omasits U, Ahrens CH, Müller S, Wollscheid B. Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 2014;30:884–886 [CrossRef][PubMed]
    [Google Scholar]
  58. Brickman E, Beckwith J. Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and phi80 transducing phages. J Mol Biol 1975;96:307–316 [CrossRef][PubMed]
    [Google Scholar]
  59. Guilhot C, Jander G, Martin NL, Beckwith J. Evidence that the pathway of disulfide bond formation in Escherichia coli involves interactions between the cysteines of DsbB and DsbA. Proc Natl Acad Sci USA 1995;92:9895–9899 [CrossRef][PubMed]
    [Google Scholar]
  60. Broome-Smith JK, Spratt BG. A vector for the construction of translational fusions to TEM β -lactamase and the analysis of protein export signals and membrane protein topology. Gene 1986;49:341–349 [CrossRef][PubMed]
    [Google Scholar]
  61. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B et al. Toward automatic reconstruction of a highly resolved tree of life. Science 2006;311:1283–1287 [CrossRef][PubMed]
    [Google Scholar]
  62. Casadaban MJ, Chou J, Cohen SN. In vitro gene fusions that join an enzymatically active beta-galactosidase segment to amino-terminal fragments of exogenous proteins: Escherichia coli plasmid vectors for the detection and cloning of translational initiation signals. J Bacteriol 1980;143:971–980[PubMed]
    [Google Scholar]
  63. Kawarabayasi Y, Hino Y, Horikawa H, Yamazaki S, Haikawa Y et al. Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1. DNA Res 1999;6:83–101 [CrossRef][PubMed]
    [Google Scholar]
  64. Weiss DS, Chen JC, Ghigo JM, Boyd D, Beckwith J. Localization of FtsI (PBP3) to the septal ring requires its membrane anchor, the Z ring, FtsA, FtsQ, and FtsL. J Bacteriol 1999;181:508–520[PubMed]
    [Google Scholar]
  65. Hemmis CW, Berkmen M, Eser M, Schildbach JF. TrbB from conjugative plasmid F is a structurally distinct disulfide isomerase that requires DsbD for redox state maintenance. J Bacteriol 2011;193:4588–4597 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000569
Loading
/content/journal/micro/10.1099/mic.0.000569
Loading

Data & Media loading...

Supplements

Supplementary File 1

Supplementary File 2

PDF
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