A Conserved Structure and Function of the YidC Homologous Protein Slr1471 from Synechocystis sp. PCC 6803

  • GathmannI, Sven (Institute fur Biochemie und Molekularbiologie, Zentrum fur Biochemie und Molekulare Zellforschung) ;
  • Rupprecht, Eva (Institute fur Biochemie und Molekularbiologie, Zentrum fur Biochemie und Molekulare Zellforschung) ;
  • Kahmann, Uwe (Fakultat fur Biologie, Universitat Bielefeld) ;
  • Schneider, Dirk (Institute fur Biochemie und Molekularbiologie, Zentrum fur Biochemie und Molekulare Zellforschung)
  • Published : 2008.06.30

Abstract

In this article, we show that the orf slr1471 from Synechocystis sp. PCC 6803 codes for a functional member of the YidC/Alb3/Oxa1 protein family, and the encoded protein has a transmembrane topology with a common core structure. Using specific antibodies raised against the Synechocystis YidC homologous protein, we further show that the Synechocystis YidC protein appears to be predominantly localized in the cyanobacterial cytoplasmic membrane. The impact of the described findings for synthesis of membrane proteins and for protein sorting within cyanobacterial cells is discussed.

Keywords

References

  1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2
  2. Bonnefoy, N., F. Chalvet, P. Hamel, P. P. Slonimski, and G. Dujardin. 1994. OXA1, a Saccharomyces cerevisiae nuclear gene whose sequence is conserved from prokaryotes to eukaryotes controls cytochrome oxidase biogenesis. J. Mol. Biol. 239: 201-212 https://doi.org/10.1006/jmbi.1994.1363
  3. du Plessis, D. J. F., N. Nouwen, and A. J. M. Driessen. 2006. Subunit a of cytochrome o oxidase requires both YidC and SecYEG for membrane insertion. J. Biol. Chem. 281: 12248- 12252 https://doi.org/10.1074/jbc.M600048200
  4. Engels, A., U. Kahmann, H. G. Ruppel, and E. K. Pistorius. 1997. Isolation, partial characterization and localization of a dihydrolipoamide dehydrogenase from the cyanobacterium Synechocystis PCC 6803. Biochim. Biophys. Acta 1340: 33-44 https://doi.org/10.1016/S0167-4838(97)00025-3
  5. Facey, S. J., S. A. Neugebauer, S. Krauss, and A. Kuhn. 2007. The mechanosensitive channel protein MscL is targeted by the SRP to the novel YidC membrane insertion pathway of Escherichia coli. J. Mol. Biol. 365: 995-1004 https://doi.org/10.1016/j.jmb.2006.10.083
  6. Fulgosi, H., L. Gerdes, S. Westphal, C. Glockmann, and J. Soll. 2002. Cell and chloroplast division requires ARTEMIS. Proc. Natl. Acad. Sci. USA 99: 11501-11506
  7. Hell, K., J. Herrmann, E. Pratje, W. Neupert, and R. A. Stuart. 1997. Oxa1p mediates the export of the N- and C-termini of pCoxII from the mitochondrial matrix to the intermembrane space. FEBS Lett. 418: 367-370 https://doi.org/10.1016/S0014-5793(97)01412-9
  8. Jiang, F., M. Chen, L. Yi, J. W. de Gier, A. Kuhn, and R. E. Dalbey. 2003. Defining the regions of Escherichia coli YidC that contribute to activity. J. Biol. Chem. 278: 48965- 48972 https://doi.org/10.1074/jbc.M307362200
  9. Jiang, F., L. Yi, M. Moore, M. Chen, T. Rohl, K. J. Van Wijk, J. W. De Gier, R. Henry, and R. E. Dalbey. 2002. Chloroplast YidC homolog Albino3 can functionally complement the bacterial YidC depletion strain and promote membrane insertion of both bacterial and chloroplast thylakoid proteins. J. Biol. Chem. 277: 19281-19288 https://doi.org/10.1074/jbc.M110857200
  10. Jo, C., H. Kim, and S. A. Jo. 2002. Application of the recombination of $\beta$-lactamase gene to PCR-based site-directed mutagenesis. Biotechniques 33: 284-288
  11. Kaneko, T., S. Sato, H. Kotani, A. Tanaka, E. Asamizu, Y. Nakamura, et al. 1996. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3: 109-136 https://doi.org/10.1093/dnares/3.3.109
  12. Klinkert, B., F. Ossenbuhl, M. Sikorski, S. Berry, L. Eichacker, and J. Nickelsen. 2004. PratA, a periplasmic tetratricopeptide repeat protein involved in biogenesis of photosystem II in Synechocystis sp. PCC 6803. J. Biol. Chem. 279: 44639-44644 https://doi.org/10.1074/jbc.M405393200
  13. Kuhn, A., R. Stuart, R. Henry, and R. E. Dalbey. 2003. The Alb3/Oxa1/YidC protein family: Membrane-localized chaperones facilitating membrane protein insertion? Trends Cell Biol. 13: 510-516 https://doi.org/10.1016/j.tcb.2003.08.005
  14. Laan, M., N. P. Nouwen, and A. J. Driessen. 2005. YidC - an evolutionary conserved device for the assembly of energytransducing membrane protein complexes. Curr. Opin. Microbiol. 8: 182-187 https://doi.org/10.1016/j.mib.2005.02.004
  15. Luirink, J., T. Samuelsson, and J. W. de Gier. 2001. YidC/ Oxa1p/Alb3: Evolutionarily conserved mediators of membrane protein assembly. FEBS Lett. 501: 1-5 https://doi.org/10.1016/S0014-5793(01)02616-3
  16. Moslavac, S., R. Bredemeier, O. Mirus, B. Granvogl, L. A. Eichacker, and E. Schleiff. 2005. Proteomic analysis of the outer membrane of Anabaena sp. strain PCC 7120. J Proteome Res. 4: 1330-1338 https://doi.org/10.1021/pr050044c
  17. Ossenbühl, F., M. Inaba-Sulpice, J. Meurer, J. Soll, and L. A. Eichacker. 2006. The Synechocystis sp. PCC 6803 Oxa1 homolog is essential for membrane integration of reaction center precursor protein pD1. Plant Cell 18: 2236-2246 https://doi.org/10.1105/tpc.106.043646
  18. Rippka, R., J. Deruelles, J. B. Waterbury, M. Herdman, and R. Y. Stanier. 1979. Generic assignments, strains histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111: 1-61 https://doi.org/10.1099/00221287-111-1-1
  19. Saaf, A., M. Monne, J. W. de Gier, and G. von Heijne. 1998. Membrane topology of the 60-kDa Oxa1p homologue from Escherichia coli. J. Biol. Chem. 273: 30415-30418 https://doi.org/10.1074/jbc.273.46.30415
  20. Sambrook, J. and D. W. Russel. 2001. Molecular Cloning: A Laboratory Manual, Cold Spring Habour Laboratory Press, Cold Sping Harbor, New York
  21. Samuelson, J. C., M. Chen, F. Jiang, I. Moller, M. Wiedmann, A. Kuhn, G. J. Phillips, and R. E. Dalbey. 2000. YidC mediates membrane protein insertion in bacteria. Nature 406: 637-641 https://doi.org/10.1038/35020586
  22. Spence, E., S. Bailey, A. Nenninger, S. G. Moller, and C. Robinson. 2004. A homolog of Albino3/OxaI is essential for thylakoid biogenesis in the cyanobacterium Synechocystis sp. PCC6803. J. Biol. Chem. 279: 55792-55800 https://doi.org/10.1074/jbc.M411041200
  23. Sundberg, E., J. G. Slagter, I. Fridborg, S. P. Cleary, C. Robinson, and G. Coupland. 1997. ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9: 717-730 https://doi.org/10.1105/tpc.9.5.717
  24. van Bloois, E., S. Nagamori, G. Koningstein, R. S. Ullers, M. Preuss, B. Oudega, N. Harms, H. R. Kaback, J. M. Herrmann, and J. Luirink. 2005. The Sec-independent function of Escherichia coli YidC is evolutionary-conserved and essential. J. Biol. Chem. 280: 12996-13003 https://doi.org/10.1074/jbc.M414094200
  25. van der Laan, M., P. Bechtluft, S. Kol, N. Nouwen, and A. J. M. Driessen. 2004. F1F0 ATP synthase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis. J. Cell Biol. 165: 213-222 https://doi.org/10.1083/jcb.200402100
  26. Yen, M. R., K. T. Harley, Y. H. Tseng, and M. H. Saier Jr. 2001. Phylogenetic and structural analyses of the oxa1 family of protein translocases. FEMS Microbiol. Lett. 204: 223-231 https://doi.org/10.1111/j.1574-6968.2001.tb10889.x
  27. Yi, L., F. Jiang, M. Chen, B. Cain, A. Bolhuis, and R. E. Dalbey. 2003. YidC is strictly required for membrane insertion of subunits a and c of the F1F0 ATP synthase and SecE of the SecYEG translocase. Biochemistry 42: 10537-10544 https://doi.org/10.1021/bi034309h
  28. Zak, E., B. Norling, R. Maitra, F. Huang, B. Andersson, and H. B. Pakrasi. 2001. The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. Proc. Natl. Acad. Sci. USA 98: 13443-13448