1887

Abstract

The zoonotic pathogen NCTC 11168 uses a complex set of electron transport chains to ensure growth with a variety of electron donors and alternative electron acceptors, some of which are known to be important for host colonization. Many of the key redox proteins essential for electron transfer in this bacterium have N-terminal twin-arginine translocase (TAT) signal sequences that ensure their transport across the cytoplasmic membrane in a folded state. By comparisons of 2D gels of periplasmic extracts, gene fusions and specific enzyme assays in wild-type, mutant and complemented strains, we experimentally verified the TAT dependence of 10 proteins with an N-terminal twin-arginine motif. NrfH, which has a TAT-like motif (LRRKILK), was functional in nitrite reduction in a mutant, and was correctly rejected as a TAT substrate by the and TatP prediction programs. However, the hydrogenase subunit HydA is also rejected by , but was shown to be TAT-dependent experimentally. The YedY homologue Cj0379 is the only TAT translocated molybdoenzyme of unknown function in ; we show that a mutant is deficient in chicken colonization and has a nitrosative stress phenotype, suggestive of a possible role for Cj0379 in the reduction of reactive nitrogen species in the periplasm. Only two potential TAT chaperones, NapD and Cj1514, are encoded in the genome. Surprisingly, despite homology to TorD, Cj1514 was shown to be specifically required for the activity of formate dehydrogenase, not trimethylamine -oxide reductase, and was designated FdhM.

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2010-10-01
2019-09-18
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References

  1. Atack, J. M., Harvey, P., Jones, M. A. & Kelly, D. J. ( 2008; ). The Campylobacter jejuni thiol peroxidases Tpx and Bcp both contribute to aerotolerance and peroxide-mediated stress resistance but have distinct substrate specificities. J Bacteriol 190, 5279–5290.[CrossRef]
    [Google Scholar]
  2. Bachmann, J., Bauer, B., Zwicker, K., Ludwig, B. & Anderka, O. ( 2006; ). The Rieske protein from Paracoccus denitrificans is inserted into the cytoplasmic membrane by the twin-arginine translocase. FEBS J 273, 4817–4830.[CrossRef]
    [Google Scholar]
  3. Baylis, C. L., McFee, S., Martin, K. W., Humphrey, T. J. & Betts, R. P. ( 2000; ). Comparison of three enrichment media for the isolation of Campylobacter spp from foods. J Appl Microbiol 89, 884–891.[CrossRef]
    [Google Scholar]
  4. Bendtsen, J. D., Nielsen, H., Widdick, D., Palmer, T. & Brunak, S. ( 2005; ). Prediction of twin-arginine signal peptides. BMC Bioinformatics 6, 167.[CrossRef]
    [Google Scholar]
  5. Berks, B. C. ( 1996; ). A common export pathway for proteins binding complex redox cofactors? Mol Microbiol 22, 393–404.[CrossRef]
    [Google Scholar]
  6. Berks, B. C., Palmer, T. & Sargent, F. ( 2003; ). The Tat protein translocation pathway and its role in microbial physiology. Adv Microb Physiol 47, 187–254.
    [Google Scholar]
  7. Berks, B. C., Palmer, T. & Sargent, F. ( 2005; ). Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr Opin Microbiol 8, 174–181.[CrossRef]
    [Google Scholar]
  8. Brokx, S. J., Rothery, R. A., Zhang, G., Ng, D. P. & Weiner, J. H. ( 2005; ). Characterization of an Escherichia coli sulfite oxidase homologue reveals the role of a conserved active site cysteine in assembly and function. Biochemistry 44, 10339–10348.[CrossRef]
    [Google Scholar]
  9. Bronstein, P., Marrichi, M. & DeLisa, M. P. ( 2004; ). Dissecting the twin-arginine translocation pathway using genome-wide analysis. Res Microbiol 155, 803–810.[CrossRef]
    [Google Scholar]
  10. Chan, C. S., Chang, L., Rommens, K. L. & Turner, R. J. ( 2009; ). Differential Interactions between Tat-specific redox enzyme peptides and their chaperones. J Bacteriol 191, 2091–2101.[CrossRef]
    [Google Scholar]
  11. De Buck, E., Vranckx, L., Meyen, E., Maes, L., Vandersmissen, L., Anne, J. & Lammertyn, E. ( 2007; ). The twin-arginine translocation pathway is necessary for correct membrane insertion of the Rieske Fe/S protein in Legionella pneumophila. FEBS Lett 581, 259–264.[CrossRef]
    [Google Scholar]
  12. De Buck, E., Lammertyn, E. & Anne, J. ( 2008; ). The importance of the twin-arginine translocation pathway for bacterial virulence. Trends Microbiol 16, 442–453.[CrossRef]
    [Google Scholar]
  13. Dilks, K., Rose, R. W., Hartmann, E. & Pohlschroder, M. ( 2003; ). Prokaryotic utilisation of the twin-arginine translocation pathway: a genomic survey. J Bacteriol 185, 1478–1483.[CrossRef]
    [Google Scholar]
  14. Elvers, K. T., Wu, G., Gilberthorpe, N. J., Poole, R. K. & Park, S. F. ( 2004; ). Role of an inducible single-domain hemoglobin in mediating resistance to nitric oxide and nitrosative stress in Campylobacter jejuni and Campylobacter coli. J Bacteriol 186, 5332–5341.[CrossRef]
    [Google Scholar]
  15. Gaskin, D. J. H., Van Vliet, A. H. M. & Pearson, B. M. ( 2007; ). The Campylobacter genetic toolbox: development of tractable and generally applicable genetic techniques for Campylobacter jejuni. Zoon Publ Health 54 (Suppl. 1), 101.
    [Google Scholar]
  16. Genest, O., Neumann, M., Seduk, F., Stocklein, W., Mejean, V., Leimkuhler, S. & Iobbi-Nivol, C. ( 2008; ). Dedicated metallochaperone connects apoenzyme and molybdenum cofactor biosynthesis components. J Biol Chem 283, 21433–21440.[CrossRef]
    [Google Scholar]
  17. Genest, O., Mejean, V. & Iobbi-Nivol, C. ( 2009; ). Multiple roles of TorD-like chaperones in the biogenesis of molybdoenzymes. FEMS Microbiol Lett 297, 1–9.[CrossRef]
    [Google Scholar]
  18. Gohlke, U., Pullan, L., McDevitt, C. A., Porcelli, I., de Leeuw, E., Palmer, T., Saibil, H. R. & Berks, B. C. ( 2005; ). The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. Proc Natl Acad Sci U S A 102, 10482–10486.[CrossRef]
    [Google Scholar]
  19. Graubner, W., Schierhorn, A. & Bruser, T. ( 2007; ). DnaK plays a pivotal role in Tat targeting of CueO and functions beside SlyD as a general Tat signal binding chaperone. J Biol Chem 282, 7116–7124.
    [Google Scholar]
  20. Guccione, E., Hitchcock, A., Hall, S. J., Mulholland, F., Shearer, N., van Vliet, A. H. & Kelly, D. J. ( 2010; ). Reduction of fumarate, mesaconate and crotonate by Mfr, a novel oxygen-regulated periplasmic reductase in Campylobacter jejuni. Environ Microbiol 12, 576–591.[CrossRef]
    [Google Scholar]
  21. Hall, S. J., Hitchcock, A., Butler, C. S. & Kelly, D. J. ( 2008; ). A Multicopper oxidase (Cj1516) and a CopA homologue (Cj1161) are major components of the copper homeostasis system of Campylobacter jejuni. J Bacteriol 190, 8075–8085.[CrossRef]
    [Google Scholar]
  22. Hendrixson, D. R. & DiRita, V. J. ( 2004; ). Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol Microbiol 52, 471–484.[CrossRef]
    [Google Scholar]
  23. Hinsley, A. P., Stanley, N. R., Palmer, T. & Berks, B. C. ( 2001; ). A naturally occurring bacterial Tat signal peptide lacking one of the ‘invariant’ arginine residues of the consensus targeting motif. FEBS Lett 497, 45–49.[CrossRef]
    [Google Scholar]
  24. Holmes, K., Mulholland, F., Pearson, B. M., Pin, C., McNicholl-Kennedy, J., Ketley, J. M. & Wells, J. M. ( 2005; ). Campylobacter jejuni gene expression in response to iron limitation and the role of Fur. Microbiology 151, 243–257.[CrossRef]
    [Google Scholar]
  25. Hughes, M. N. ( 1999; ). Relationships between nitric oxide, nitroxyl ion, nitrosonium cation and peroxynitrite. Biochim Biophys Acta 1411, 263–272.[CrossRef]
    [Google Scholar]
  26. Ilbert, M., Mejean, V., Giudici-Orticoni, M. T., Samama, J. P. & Iobbi-Nivol, C. ( 2003; ). Involvement of a mate chaperone (TorD) in the maturation pathway of molybdoenzyme TorA. J Biol Chem 278, 28787–28792.[CrossRef]
    [Google Scholar]
  27. Ize, B., Porcelli, I., Lucchini, S., Hinton, J. C., Berks, B. C. & Palmer, T. ( 2004; ). Novel phenotypes of Escherichia coli tat mutants revealed by global gene expression and phenotypic analysis. J Biol Chem 279, 47543–47554.[CrossRef]
    [Google Scholar]
  28. Jack, R. L., Buchanan, G., Dubini, A., Hatzixanthis, K., Palmer, T. & Sargent, F. ( 2004; ). Coordinating assembly and export of complex bacterial proteins. EMBO J 23, 3962–3972.[CrossRef]
    [Google Scholar]
  29. Jackson, R. J., Elvers, K. T., Lee, L. J., Gidley, M. D., Wainwright, L. M., Lightfoot, J., Park, S. F. & Poole, R. K. ( 2007; ). Oxygen reactivity of both respiratory oxidases in Campylobacter jejuni: the cydAB genes encode a cyanide-resistant, low-affinity oxidase that is not of the cytochrome bd type. J Bacteriol 189, 1604–1615.[CrossRef]
    [Google Scholar]
  30. Jacobs-Reitsma, W., Lyths, U. & Wagenaar, J. ( 2008; ). Campylobacter in the food supply. In Campylobacter, 3rd edn. Edited by Nachamkin, I., Szymanski, C. M. & Blaser, M. J.. Washington, DC: American Society for Microbiology.
    [Google Scholar]
  31. Jones, M. A., Marston, K. L., Woodall, C. A., Maskell, D. J., Linton, D., Karlyshev, A. V., Dorrell, N., Wren, B. W. & Barrow, P. A. ( 2004; ). Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect Immun 72, 3769–3776.[CrossRef]
    [Google Scholar]
  32. Joshi, M. V., Mann, S. G., Antelmann, H., Widdick, D. A., Fyans, J. K., Chandra, G., Hutchings, M. I., Toth, I., Hecker, M. & other authors ( 2010; ). The twin arginine protein transport pathway exports multiple virulence proteins in the plant pathogen Streptomyces scabies. Mol Microbiol 77, 252–271.[CrossRef]
    [Google Scholar]
  33. Juhnke, H. D., Hiltscher, H., Nasiri, H. R., Schwalbe, H. & Lancaster, C. R. ( 2009; ). Production, characterization and determination of the real catalytic properties of the putative ‘succinate dehydrogenase’ from Wolinella succinogenes. Mol Microbiol 71, 1088–1101.[CrossRef]
    [Google Scholar]
  34. Karlyshev, A. V. & Wren, B. W. ( 2005; ). Development and application of an insertional system for gene delivery and expression in Campylobacter jejuni. Appl Environ Microbiol 71, 4004–4013.[CrossRef]
    [Google Scholar]
  35. Karlyshev, A. V., Linton, D., Gregson, N. A. & Wren, B. W. ( 2002; ). A novel paralagous gene family involved in phase-variable flagella mediated motility in Campylobacter jejuni. Microbiology 148, 473–480.
    [Google Scholar]
  36. Kelly, D. J. ( 2008; ). Complexity and versatility in the physiology and metabolism of Campylobacter jejuni. In Campylobacter, 3rd edn. Edited by Nachamkin, I., Szymanski, C. M. & Blaser, M. J.. Washington, DC: American Society for Microbiology.
    [Google Scholar]
  37. Leon-Kempis Mdel, R., Guccione, E., Mulholland, F., Williamson, M. P. & Kelly, D. J. ( 2006; ). The Campylobacter jejuni PEB1a adhesin is an aspartate/glutamate-binding protein of an ABC transporter essential for microaerobic growth on dicarboxylic amino acids. Mol Microbiol 60, 1262–1275.[CrossRef]
    [Google Scholar]
  38. Li, H., Chang, L., Howell, J. M. & Turner, R. J. ( 2010; ). DmsD, a Tat system specific chaperone, interacts with other general chaperones and proteins involved in the molybdenum cofactor biosynthesis. Biochim Biophys Acta 1804, 1301–1309.[CrossRef]
    [Google Scholar]
  39. Loschi, L., Brokx, S. J., Hills, T. L., Zhang, G., Bertero, M. G., Lovering, A. L., Weiner, J. H. & Strynadka, N. C. ( 2004; ). Structural and biochemical identification of a novel bacterial oxidoreductase. J Biol Chem 279, 50391–50400.[CrossRef]
    [Google Scholar]
  40. Maillard, J., Spronk, C. A., Buchanan, G., Lyall, V., Richardson, D. J., Palmer, T., Vuister, G. W. & Sargent, F. ( 2007; ). Structural diversity in twin-arginine signal peptide-binding proteins. Proc Natl Acad Sci U S A 104, 15641–15646.[CrossRef]
    [Google Scholar]
  41. Markwell, M. A., Haas, S. M., Bieber, L. L. & Tolbert, N. E. ( 1978; ). A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87, 206–210.[CrossRef]
    [Google Scholar]
  42. Mickael, C. S., Lam, P. K., Berberov, E. M., Allan, B., Potter, A. A. & Koster, W. ( 2010; ). Salmonella enterica serovar Enteritidis tatB and tatC mutants are impaired in Caco-2 cell invasion in-vitro and show reduced systemic spread in chickens. Infect Immun 78, 3493–3505.[CrossRef]
    [Google Scholar]
  43. Myers, J. D. & Kelly, D. J. ( 2005; ). A sulphite respiration system in the chemoheterotrophic human pathogen Campylobacter jejuni. Microbiology 151, 233–242.[CrossRef]
    [Google Scholar]
  44. Nachamkin, I., Yang, X. H. & Stern, N. J. ( 1993; ). Role of Campylobacter jejuni flagella as colonization factors for three-day-old chicks: analysis with flagellar mutants. Appl Environ Microbiol 59, 1269–1273.
    [Google Scholar]
  45. Ochsner, U. A., Snyder, A., Vasil, A. I. & Vasil, M. L. ( 2002; ). Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis. Proc Natl Acad Sci U S A 99, 8312–8317.[CrossRef]
    [Google Scholar]
  46. Oresnik, I. J., Ladner, C. L. & Turner, R. J. ( 2001; ). Identification of a twin-arginine leader-binding protein. Mol Microbiol 40, 323–331.[CrossRef]
    [Google Scholar]
  47. Pajaniappan, M., Hall, J. E., Cawthraw, S. A., Newell, D. G., Gaynor, E. C., Fields, J. A., Rathbun, K. M., Agee, W. A., Burns, C. M. & other authors ( 2008; ). A temperature-regulated Campylobacter jejuni gluconate dehydrogenase is involved in respiration-dependent energy conservation and chicken colonization. Mol Microbiol 68, 474–491.[CrossRef]
    [Google Scholar]
  48. Palmer, T., Sargent, F. & Berks, B. C. ( 2005; ). Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol 13, 175–180.[CrossRef]
    [Google Scholar]
  49. Parkhill, J., Wren, B. W., Mungall, K., Ketley, J. M., Churcher, C., Basham, D., Chillingworth, T., Davies, R. M., Feltwell, T. & other authors ( 2000; ). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665–668.[CrossRef]
    [Google Scholar]
  50. Pitcher, R. S. & Watmough, N. J. ( 2004; ). The bacterial cytochrome cbb3 oxidases. Biochim Biophys Acta 1655, 388–399.[CrossRef]
    [Google Scholar]
  51. Pittman, M. S., Elvers, K. T., Lee, L., Jones, M. A., Poole, R. K., Park, S. F. & Kelly, D. J. ( 2007; ). Growth of Campylobacter jejuni on nitrate and nitrite: electron transport to NapA and NrfA via NrfH and distinct roles for NrfA and the globin Cgb in protection against nitrosative stress. Mol Microbiol 63, 575–590.[CrossRef]
    [Google Scholar]
  52. Pommier, J., Mejean, V., Giordano, G. & Iobbi-Nivol, C. ( 1998; ). TorD, a cytoplasmic chaperone that interacts with the unfolded trimethylamine N-oxide reductase enzyme (TorA) in Escherichia coli. J Biol Chem 273, 16615–16620.[CrossRef]
    [Google Scholar]
  53. Rajashekara, G., Drozd, M., Gangaiah, D., Jeon, B., Liu, Z. & Zhang, Q. ( 2009; ). Functional characterization of the twin-arginine translocation system in Campylobacter jejuni. Foodborne Pathog Dis 6, 935–945.[CrossRef]
    [Google Scholar]
  54. Ray, N., Oates, J., Turner, R. J. & Robinson, C. ( 2003; ). DmsD is required for the biogenesis of DMSO reductase in Escherichia coli but not for the interaction of the DmsA signal peptide with the Tat apparatus. FEBS Lett 534, 156–160.[CrossRef]
    [Google Scholar]
  55. Rodrigue, A., Chanal, A., Beck, K., Muller, M. & Wu, L. F. ( 1999; ). Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial tat pathway. J Biol Chem 274, 13223–13228.[CrossRef]
    [Google Scholar]
  56. Rose, R. W., Bruser, T., Kissinger, J. C. & Pohlschroder, M. ( 2002; ). Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol Microbiol 45, 943–950.[CrossRef]
    [Google Scholar]
  57. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
    [Google Scholar]
  58. Santini, C. L., Ize, B., Chanal, A., Muller, M., Giordano, G. & Wu, L. F. ( 1998; ). A novel sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J 17, 101–112.[CrossRef]
    [Google Scholar]
  59. Sargent, F., Berks, B. C. & Palmer, T. ( 2002; ). Assembly of membrane-bound respiratory complexes by the Tat protein-transport system. Arch Microbiol 178, 77–84.[CrossRef]
    [Google Scholar]
  60. Sellars, M. J., Hall, S. J. & Kelly, D. J. ( 2002; ). Growth of Campylobacter jejuni supported by respiration of fumarate, nitrate, nitrite, trimethylamine-N-oxide, or dimethyl sulfoxide requires oxygen. J Bacteriol 184, 4187–4196.[CrossRef]
    [Google Scholar]
  61. Smart, J. P., Cliff, M. J. & Kelly, D. J. ( 2009; ). A role for tungsten in the biology of Campylobacter jejuni: tungstate stimulates formate dehydrogenase activity and is transported via an ultra-high affinity ABC system distinct from the molybdate transporter. Mol Microbiol 74, 742–757.[CrossRef]
    [Google Scholar]
  62. Sommerlad, S. M. & Hendrixson, D. R. ( 2007; ). Analysis of the roles of FlgP and FlgQ in flagellar motility of Campylobacter jejuni. J Bacteriol 189, 179–186.[CrossRef]
    [Google Scholar]
  63. Stanley, N. R., Findlay, K., Berks, B. C. & Palmer, T. ( 2001; ). Escherichia coli strains blocked in Tat-dependent protein export exhibit pleiotropic defects in the cell envelope. J Bacteriol 183, 139–144.[CrossRef]
    [Google Scholar]
  64. Stingl, K., Schauer, K., Ecobichon, C., Labigne, A., Lenormand, P., Rousselle, J. C., Namane, A. & de Reuse, H. ( 2008; ). In vivo interactome of Helicobacter pylori urease revealed by tandem affinity purification. Mol Cell Proteomics 7, 2429–2441.[CrossRef]
    [Google Scholar]
  65. Taveirne, M. E., Sikes, M. L. & Olson, J. W. ( 2009; ). Molybdenum and tungsten in Campylobacter jejuni: their physiological role and identification of separate transporters regulated by a single ModE-like protein. Mol Microbiol 74, 758–771.[CrossRef]
    [Google Scholar]
  66. Thomas, M. T., Shepherd, M., Poole, R. K., van Vliet, A. H. M., Kelly, D. J. & Pearson, B. M. ( 2010; ). Two respiratory enzyme systems in Campylobacter jejuni NCTC 11168 contribute to growth on l-lactate. Environ Microbiol (in press ).
    [Google Scholar]
  67. Turner, R. J., Papish, A. L. & Sargent, F. ( 2004; ). Sequence analysis of bacterial redox enzyme maturation proteins (REMPs). Can J Microbiol 50, 225–238.[CrossRef]
    [Google Scholar]
  68. van Mourik, A., Bleumink-Pluym, N. M., van Dijk, L., van Putten, J. P. & Wosten, M. M. ( 2008; ). Functional analysis of a Campylobacter jejuni alkaline phosphatase secreted via the Tat export machinery. Microbiology 154, 584–592.[CrossRef]
    [Google Scholar]
  69. van Vliet, A. H. M., Wooldridge, K. G. & Ketley, J. M. ( 1998; ). Iron-responsive gene regulation in a Campylobacter jejuni fur mutant. J Bacteriol 180, 5291–5298.
    [Google Scholar]
  70. Wagenaar, J. A., Jacobs-Reitsma, W., Hofshagen, M. & Newell, D. ( 2008; ). Poultry colonisation with Campylobacter and its control at the primary production level. In Campylobacter, 3rd edn. Edited by Nachamkin, I., Szymanski, C. M. & Blaser, M. J.. Washington, DC: American Society for Microbiology.
    [Google Scholar]
  71. Wang, Y. & Taylor, D. E. ( 1990; ). Chloramphenicol resistance in Campylobacter coli: nucleotide sequence, expression, and cloning vector construction. Gene 94, 23–28.[CrossRef]
    [Google Scholar]
  72. Watmough, N. J., Butland, G., Cheesman, M. R., Moir, J. W., Richardson, D. J. & Spiro, S. ( 1999; ). Nitric oxide in bacteria: synthesis and consumption. Biochim Biophys Acta 1411, 456–474.[CrossRef]
    [Google Scholar]
  73. Weerakoon, D. R. & Olson, J. W. ( 2008; ). The Campylobacter jejuni NADH:ubiquinone oxidoreductase (complex I) utilizes flavodoxin rather than NADH. J Bacteriol 190, 915–925.[CrossRef]
    [Google Scholar]
  74. Weerakoon, D. R., Borden, N. J., Goodson, C. M., Grimes, J. & Olson, J. W. ( 2009; ). The role of respiratory donor enzymes in Campylobacter jejuni host colonization and physiology. Microb Pathog 47, 8–15.[CrossRef]
    [Google Scholar]
  75. Weingarten, R. A., Grimes, J. L. & Olson, J. W. ( 2008; ). Role of Campylobacter jejuni respiratory oxidases and reductases in host colonization. Appl Environ Microbiol 74, 1367–1375.[CrossRef]
    [Google Scholar]
  76. Weingarten, R. A., Taveirne, M. E. & Olson, J. W. ( 2009; ). The dual-functioning fumarate reductase is the sole succinate:quinone reductase in Campylobacter jejuni and is required for full host colonization. J Bacteriol 191, 5293–5300.[CrossRef]
    [Google Scholar]
  77. Workun, G. J., Moquin, K., Rothery, R. A. & Weiner, J. H. ( 2008; ). Evolutionary persistence of the molybdopyranopterin-containing sulfite oxidase protein fold. Microbiol Mol Biol Rev 72, 228–248.[CrossRef]
    [Google Scholar]
  78. Zhang, J. W., Butland, G., Greenblatt, J. F., Emili, A. & Zamble, D. B. ( 2005; ). A role for SlyD in the Escherichia coli hydrogenase biosynthetic pathway. J Biol Chem 280, 4360–4366.[CrossRef]
    [Google Scholar]
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