Response to Theissen and Martin

This evolutionarily and functionally sharp distinction between organelles and endosymbionts — protein import, or not — was crisply articulated by CavalierSmith and Lee [9]. It has proven to be exquisitely robust. Unless the Paulinella endosymbiont can be shown to possess a protein import apparatus, it is just another member in a long list of known cases of endosymbionts: the proteobacterial endosymbionts of insects such as Buchnera, Wigglesworthia, and Wolbachia [5,6,10], the methanogenic endosymbionts of anaerobic ciliates [11], the nitrogenfixing symbionts in the diatom Rhopalodia [12], the chemosynthetic endosymbiont consortia of gutless tubeworms [13], the cyanobacterial endosymbionts of sponges [14], and endosymbionts that live within other prokaryotes [15] — to name just very few examples. The rate-limiting step in the transition from endosymbionts to organelles would appear to be the origin of the protein import machinery itself [9]: the TIM and TOM complexes of mitochondria [7] and the TIC and TOC complexes of plastids [8]. The origin of those complexes allowed each organelle to specifically import proteins synthesized in the host’s cytosol, thereby allowing the endosymbionts to relinquish their prokaryotic genes without relinquishing their prokaryotic biochemistry. Calling the Paulinella endosymbiont a plastid or an organelle might make a story more exciting, but at the cost of scientific accuracy. Some proteobacterial endosymbionts of aphids have genomes smaller than those of some plastids [16]. Would anyone call those endosymbionts ‘mitochondria’? Hardly. For the same reasons, we should not call the Paulinella endosymbionts ‘plastids’ any more than we should say that sponges [14] have ‘plastids’. There is a difference between endosymbionts and organelles. References 1. Archibald, J.M. (2006). Endosymbiosis: Double-take on plastid origins. Curr. Biol. 16, R690–R692. 2. Yoon, H.S., Reyes-Prieto, A., Melkonian, M., Bhattacharya, D. (2006). Minimal plastid evolution in the Paulinella endosymbiont. Curr. Biol. 16, R670– R672. 3. Rodriguez-Ezpeleta, N., and Philippe, H. (2006). Plastid origin: Replaying the tape. Curr. Biol. 16, R54–R56. 4. Marin B, Nowack E.C.M., Melkonian, M. (2005). A plastid in the making: Evidence for a second primary endosymbiosis. Protist, Vol. 156, 425–432. 5. Zientz, E., Dandekar, T., and Gross, R. (2004). Metabolic interdependence of obligate intracellular bacteria and their insect hosts. Microbiol. Mol. Biol. Rev. 68, 745–770. 6. Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y., and Ishikawa, H. (2000). Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407, 81–86. 7. Dolezal, P., Likic, V., Tachezy, J. and Lithgow, T. (2006). Evolution of the molecular machines for protein import into mitochondria. Science 313, 314-318. 8. Soll, J. and Schleiff, E. (2004). Protein import into chloroplasts. Nat. Rev. Mol. Cell Biol. 5, 198–208. 9. Cavalier-Smith, T., and Lee, J.J. (1985). Protozoa as hosts for endosymbioses and the conversion of symbionts into organelles. J. Protozool. 32, 376–379. 10. Wu, M., Sun, L., Vamathevan, J., Riegler, M., Deboy, R., Brownlie, J., McGraw, E., Mohamoud, Y., Lee, P., Berry, K. et al. (2004). The genome sequence and evolution of the reproductive parasite Wolbachia pipientis wMel: a streamlined -Proteobacterium massively infected with mobile genetic elements. PLoS Biol. 2, 327–341. 11. Embley, T.M. and Finlay, B.J. (1993). Systematic and morphological diversity of endosymbiotic methanogens in anaerobic ciliates. Antonie Van Leeuwenhoek 64, 261–271. 12. Prechtl, J., Kneip, C., Lockhart, P., Wenderoth, K. and Maier, U.G. (2004). Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. Mol. Biol. Evol. 21, 1477–1481. 13. Woyke, T., Teeling, H., Ivanova, N.N., Hunteman, M., Richter, M., Gloeckner, F.O., Boffelli, D., Anderson, I.J., Barry, K.W., Shapiro, et al. (2006). Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443, 950–955. 14. Thacker, R.W. (2005). Impacts of shading on sponge-Cyanobacteria symbioses: A comparison between host-specific and generalist associations. Integr. Comp. Biol. 45, 369–376. 15. Wujek, D.E. (1979). Intracellular bacteria in the blue-green-alga Pleurocapsa minor. Trans. Am. Micros. Soc. 98, 143–145. 16. Nakabachi, A., Yamashita, A., Toh, H., Ishikawa, H., Dunbar, H.E., Moran, N.A., Hattori M. (2006). The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314, 267.