Symbiosis

, Volume 58, Issue 1–3, pp 127–133 | Cite as

Conservative sorting in the muroplasts of Cyanophora paradoxa: a reevaluation based on the completed genome sequence

  • Jürgen M. Steiner
  • Debashish Bhattacharya
  • Wolfgang Löffelhardt
Article

Abstract

After primary endosymbiosis, massive gene transfer occurred from the genome of the cyanobacterial endosymbiont to the nucleus of the protist host cell. In parallel, a specific protein import apparatus arose for reimport of many, but not all products of the genes moved to the nuclear genome. Presequences evolved to allow recognition of plastid proteins at the envelope and their translocation to the stroma. However, plastids (and cyanobacteria) also comprise five other subcompartments. Protein sorting to the cyanobacterial thylakoid membrane, the thylakoid lumen, the inner envelope membrane, the periplasmic space, and the outer envelope membrane is achieved by prokaryotic protein translocases recognizing, e.g., signal sequences. The “conservative sorting” hypothesis postulates that these translocases remained functional in endosymbiotic organelles and obtained their passengers not only from imported proteins but also from proteins synthesized in organello. For proteins synthesized in the cytosol, a collaboration of the general import apparatus and the former prokaryotic translocase is necessary which is often reflected by the use of bipartite presequences, e.g., stroma targeting peptide and signal peptide. For plants, this concept has been experimentally proven and verified. The muroplasts from Cyanophora paradoxa, that have several features more in common with cyanobacteria than with plastids, were analyzed with the availability of the recently completed nuclear genome sequence. Interesting findings include the absence of the post-translational signal recognition particle pathway, dual Sec translocases in thylakoid and inner envelope membranes that are produced from a single set of genes, and a co-translational signal recognition pathway operating without a 4.5S RNA component.

Keywords

Cyanophora paradoxa Glaucophyta Muroplasts Conservative sorting 

Notes

Acknowledgments

Support from the “Fonds zur Förderung der wissenschaftlichen Forschung” (P19683, to W.L.) is gratefully acknowledged. We are indebted to M.A. Rosenblad (Gothenburg) for communicating data prior to publication.

References

  1. Albiniak AM, Baglieri J, Robinson C (2012) Targeting of lumenal proteins across the thylakoid membrane. J Exp Bot 63:1689–1698PubMedCrossRefGoogle Scholar
  2. Aldridge C, Spence E, Kirkilionis L, Frigerio MA, Robinson C (2008) The Tat-dependent targeting of Rieske iron-sulfur proteins to both the plasma and thylakoid membranes in the cyanobacterium Synechocystis PCC6803. Mol Microbiol 70:140–150PubMedCrossRefGoogle Scholar
  3. Bölter B, Soll J, Schulz A, Hinnah S, Wagner R (1998) Origin of a chloroplast protein importer. Proc Natl Acad Sci U S A 95:15831–15836PubMedCrossRefGoogle Scholar
  4. Cline K, Dabney-Smith C (2008) Plastid protein import and sorting: different paths to the same compartments. Curr Opin Plant Biol 11:585–592PubMedCrossRefGoogle Scholar
  5. Flachmann R, Michalowski CB, Löffelhardt W, Bohnert HJ (1993) SecY, an integral subunit of the bacterial preprotein translocase is encoded by a plastid genome. J Biol Chem 268:7514–7519PubMedGoogle Scholar
  6. Göhre V, Ossenbühl F, Crevecoeur M, Eichacker LA, Rochaix J-D (2006) One of two Alb3 proteins is essential for the assembly of the photosystems and for cell survival in Chlamydomonas. Plant Cell 18:1454–1466PubMedCrossRefGoogle Scholar
  7. Gross J, Bhattacharya D (2009) Revaluating the evolution of the Toc and Tic protein translocons. Trends Plant Sci 14:13–20PubMedCrossRefGoogle Scholar
  8. Grudnik P, Bange G, Sinning I (2009) Protein targeting by the signal recognition particle. Biol Chem 390:775–782PubMedCrossRefGoogle Scholar
  9. Hartl FU, Schmidt B, Wachter E, Weiss H, Neupert W (1986) Transport into mitochondria and intramitochondrial sorting of the Fe/S protein of ubiquinol-cytochrome c reductase. Cell 47:939–951PubMedCrossRefGoogle Scholar
  10. Howe CJ, Floyd KA (2001) Chloroplast and mitochondrial type I signal peptidases. In: Dalbey R, Sigman DS (eds) Co- and posttranslational proteolysis of proteins, The Enzymes vol XXII. Academic, San Diego, pp 101–125Google Scholar
  11. Howe CJ, Packer JCL (1998) Algal plastid genomes encode homologues of the SRP-associated RNA. Mol Microbiol 27:508–510PubMedGoogle Scholar
  12. Hsu S-C, Endow JK, Ruppel NJ, Roston RL, Baldwin AJ, Inoue K (2011) Functional diversification of thylakoidal processing peptidases in Arabidopsis thaliana. PLoS ONE 6(11):e27258PubMedCrossRefGoogle Scholar
  13. Löffelhardt W, Bohnert HJ, Bryant DA (1997) The complete sequence of the Cyanophora paradoxa cyanelle genome (Glaucocystophyceae). Pl Syst Evol [Suppl] 11:149–162CrossRefGoogle Scholar
  14. Mant A, Woolhead CA, Moore M, Henry R, Robinson C (2001) Insertion of PsaK into the thylakoid membrane in a “horseshoe” conformation occurs in the absence of signal recognition particle, nucleoside triphosphates, or functional albino3. J Biol Chem 276:36200–36206PubMedCrossRefGoogle Scholar
  15. Matsuzaki M et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae. Nature 428:653–657PubMedCrossRefGoogle Scholar
  16. Mehner D, Osadnik H, Lünsdorf H, Brüser T (2012) The Tat system for membrane translocation of folded proteins recruits the membrane-stabilizing Psp machinery in Escherichia coli. J Biol Chem 287:27834–27842PubMedCrossRefGoogle Scholar
  17. Nakai M, Sugita D, Omata T, Endo T (1993) SecY protein is localized in both the cytoplasmic and thylakoid membranes in the cyanobacterium Synechococcus PCC 7942. Biochem Biophys Res Commun 193:228–234PubMedCrossRefGoogle Scholar
  18. Natale P, Brüser T, Driessen AJM (2008) Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane: distinct translocases and mechanisms. Biochim Biophys Acta 1778:1735–1756PubMedCrossRefGoogle Scholar
  19. Ossenbühl F, Inaba-Sulpice M, Meurer J, Soll J, Eichacker L (2006) The Synechocystis sp. PCC 6803 Oxa1 homolog is essential for membrane integration of reaction center precursor protein pD1. Plant Cell 18:2236–2246PubMedCrossRefGoogle Scholar
  20. Price DC, Chan CX, Yoon HS, Yang EC, Qiu H, Weber APM, Schwacke R, Gross J, Blouin NA, Lane C, Reyes-Prieto A, Durnford DG, Neilson JAD, Lang BF, Burger G, Steiner JM, Löffelhardt W, Meuser JE, Posewitz MC, Ball S, Arias MC, Henrissat B, Coutinho PM, Rensing SA, Symeonidi A, Doddapaneni H, Green BR, Rajah VD, Boore J, Bhattacharya D (2012) Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335:843–847PubMedCrossRefGoogle Scholar
  21. Rensing SA, Maier U-G (1994) The SecY protein family: comparative analysis and phylogenetic relationships. Mol Phyl Evol 3:187–191CrossRefGoogle Scholar
  22. Richter CV, Bals T, Schünemann D (2010) Component interactions, regulation and mechanisms of chloroplast signal recognition particle-dependent protein transport. Eur J Cell Biol 89:965–973PubMedCrossRefGoogle Scholar
  23. Rodríguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G, Löffelhardt W, Bohnert HJ, Philippe H, Lang BF (2005) Monophyly of primary photosynthetic eukaryotes: green plants, red algae and glaucophytes. Curr Biol 15:1325–1330PubMedCrossRefGoogle Scholar
  24. Rosenblad MA, Larsen N, Samuelsson T, Zwieb C (2009) Kinship in the SRP RNA family. RNA Biol 6:508–516PubMedCrossRefGoogle Scholar
  25. Skalitzky CA, Martin JR, Harwood JH, Beirne JJ, Adamczyk BJ, Heck GR, Cline K, Fernandez DE (2011) Plastids contain a second Sec translocase system with essential functions. Plant Physiol 155:354–369PubMedCrossRefGoogle Scholar
  26. Smeekens S, Weisbeek P, Robinson C (1990) Protein transport into and within chloroplasts. Trends Biochem Sci 15:73–76PubMedCrossRefGoogle Scholar
  27. Steiner JM, Serrano A, Allmaier G, Jakowitsch J, Löffelhardt W (2000) Cytochrome c 6 from Cyanophora paradoxa: Characterization of the protein and the cDNA of the precursor and import into isolated cyanelles. Europ J Biochem 267:4232–4241PubMedGoogle Scholar
  28. Steiner JM, Köcher T, Nagy C, Löffelhardt W (2002) Chloroplast SecE: evidence for spontaneous insertion into the thylakoid membrane. Biochem Biophys Res Commun 293:747–752PubMedCrossRefGoogle Scholar
  29. Steiner JM, Yusa F, Pompe JA, Löffelhardt W (2005a) Homologous protein import machineries in chloroplasts and cyanelles. Plant J 44:646–652PubMedCrossRefGoogle Scholar
  30. Steiner JM, Berghöfer J, Yusa F, Pompe JA, Klösgen RB, Löffelhardt W (2005b) Conservative sorting in a primitive plastid: the cyanelle of Cyanophora paradoxa. FEBS J 272:987–998PubMedCrossRefGoogle Scholar
  31. Tissier C, Woolhead CA, Robinson C (2002) Unique structural determinants in the signal peptides of ‘spontaneously’ inserting thylakoid membrane proteins. Europ J Biochem 269:3131–3141PubMedCrossRefGoogle Scholar
  32. Tripathi LP, Sowdhamini R (2006) Cross genome comparisons of serine proteases in Arabidopsis and rice. BMC Genomics 7:200PubMedCrossRefGoogle Scholar
  33. Tripp J, Inoue K, Keegstra K, Froehlich JE (2007) A novel serine/prolinerich domain in combination with a transmembrane domain is required for the insertion of AtTic40 into the inner envelope membrane of chloroplasts. Plant J 52:824–838PubMedCrossRefGoogle Scholar
  34. Vothknecht UC, Otters S, Hennig R, Schneider D (2011) Vipp 1: a very important protein in plastids?! J Exp Bot 63:1699–1712PubMedCrossRefGoogle Scholar
  35. Wunder T, Martin R, Löffelhardt W, Schleiff E, Steiner JM (2007) The invariant phenylalanine of precursor proteins discloses the importance of Omp85 for protein translocation into cyanelles. BMC Evol Biol 7:236PubMedCrossRefGoogle Scholar
  36. Yusa F, Steiner JM, Löffelhardt W (2008) Evolutionary conservation of dual Sec translocases in the cyanelles of Cyanophora paradoxa. BMC Evol Biol 8:304PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Jürgen M. Steiner
    • 1
  • Debashish Bhattacharya
    • 2
  • Wolfgang Löffelhardt
    • 3
  1. 1.Department of Biology/Plant PhysiologyMartin-Luther-University Halle-WittenbergHalleGermany
  2. 2.Department of Ecology, Evolution, and Natural Resources and Institute of Marine and Coastal SciencesRutgers UniversityNew BrunswickUSA
  3. 3.Max F. Perutz Laboratories, Department of Biochemistry and Cell BiologyUniversity of ViennaViennaAustria

Personalised recommendations