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Correspondence 10. Dubrulle J, McGrew MJ, Pourquié O. 2001. FGF signalling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106:219–232. 11. Wolpert L, Beddington R, Brockes J, Jessell T, Lawrence P, Meyerowitz E. 1998. Principles of Development. Oxford: Oxford University Press. 12. Vincent J-P, Briscoe J. 2001. Morphogens. Current Biology 11:R851– R854. The nucleolar proteome and the (endosymbiotic) origin of the nucleus Sir, Nucleoli are essential regions of the eukaryotic nuclei where the ribosomes are assembled. The human nucleolar proteome has been studied in the last two years, leading to the identification of several hundreds of proteins.(1,2) In a recent Bioessays’ article, Staub et al.(3) characterise a large set of conserved domains in these nucleolar proteins. The search of these domains in other organisms revealed a complex pattern. Many exist in archaea, arguing for an archaeal origin of the nucleolar ‘‘core’’ machinery. A substantial bacterial contribution is also identified, while several domains are exclusively eukaryotic. These results support a chimeric origin of the nucleolus, with an ancestral core of archaeal origin supplemented with certain bacterial proteins and several proteins invented during the eukaryotic evolution. This mixed heritage is compatible with the diverse hypotheses that propose the amalgamation of archaea and bacteria to give rise to the first eukaryotes. However, these hypotheses differ in the mechanism explaining the merging of the archaeal and bacterial partners. Some propose an unspecified fusion(4) or the engulfment of an archaeon by a bacterium.(5,6) The most elaborate invoke symbioses between archaea and bacteria.(7–11) Another fundamental difference concerns the origin of the nucleus: is it a remnant of endosymbiotic archaea(5,6,10–12) or just an idiosyncratic eukaryotic invention?(7,9,13,14) Staub et al. try to answer this question using the nucleolar proteome information. They conclude that the ribosomes and the components involved in the maturation and assembly of their constituents are of archaeal origin, which excludes a bacterial endosymbiotic origin of the nucleus.(3) However, all modern hypotheses for the origin of the nucleus involve symbiotic or endosymbiotic archaea, not endosymbiotic bacteria.(5,6,10 –12) Hence, despite their claim, Staub et al.’s results are fully compatible with these hypotheses. They are reluctant to accept an origin of the nucleus from an 1144 BioEssays 26.10 Stephen J. Gaunt Department of Development & Genetics Babraham Institute, Babraham Cambridge, CB2 4AT, U.K. E-mail: [email protected] DOI 10.1002/bies.20116 Published online in Wiley InterScience (www.interscience.wiley.com). endosymbiotic archaeal ancestor, but they support their view with arguments other than the nucleolar protein domain analysis. Are their arguments sufficiently sound? The first concerns the co-existence of three different genomes and protein synthesis machineries in early eukaryotes and the problems eventually derived from the interferences between them. However, this problem is not exclusive for the hypotheses proposing an endosymbiotic origin of the nucleus. Indeed, the study of the nucleolar proteome supports a chimeric origin of eukaryotes involving at least an archaeon and a bacterium, that is, two genomes and two different protein synthesis machineries. This is not necessarily problematic, as revealed by the evolutionary history of eukaryotes. All contemporary eukaryotes have or have had mitochondria with their own genome and protein synthesis machinery. Moreover, photosynthetic eukaryotes also contain chloroplasts, derived from cyanobacterial endosymbionts with a genome and protein synthesis machinery. In the most complex cases, cryptophyte and chlorarachniophyte algae, chloroplasts derive from endosymbiotic eukaryotic algae, which possess a reduced but functional nucleus (the ‘‘nucleomorph’’). In these algae, four different genomes and protein synthesis machineries co-exist: nuclear-, mitochondrial-, chloroplast- and nucleomorph-encoded. This extreme complexity (CavalierSmith called these organisms ‘‘meta-algae’’)(15) eloquently demonstrates that the co-existence of different genomes and protein synthesis machineries is possible and can have a great evolutionary success. The second argument evoked by Staub et al. is that the available theories do not explain the energetic advantages for an endosymbiotic origin of the nucleus. Several hypotheses do not discuss any selective advantage (energetic or other) for the establishment of the endosymbiosis.(5,6) However, we have already advanced a model, the ‘‘syntrophy hypothesis’’,(10,11) starting with the establishment of a metabolic symbiosis (‘‘syntrophy’’ meaning ‘‘eating together’’) sustained by interspecies hydrogen transfer between facultative sulfatereducing proteobacteria and methanogenic archaea, a frequent symbiosis in anoxic environments.(16) For us, the ancestral nucleus (derived from the methanogen) was originally a metabolic compartment, which lost methanogenesis during its evolution. The hypothesis preferred by Staub et al. to explain eukaryogenesis, the ‘‘hydrogen hypothesis’’,(9) is also based on a hydrogen-transfer syntrophy between BioEssays 26:1144–1145, ß 2004 Wiley Periodicals, Inc. Correspondence archaea and bacteria, but it does not advance any energyrelated explanation for the origin of the nucleus. A third argument deals with structural characteristics of the nuclear membrane. As Staub et al. posit ‘‘no free-living prokaryote is separated from the environment in the same manner in which the nucleus is separated from the cytoplasm’’. This is true, but the question is also whether we should expect, after many hundred millions years of evolution, to find a nuclear membrane remaining identical to that of a free-living prokaryote. We think this is highly improbable. On the contrary, during the huge time span of eukaryotic evolution important structural changes and innovations have occurred (a clear example are the nuclear pores). Innovations exist for the mitochondria and chloroplasts (for example, specific membrane transport systems)(15,17) but they do not refute their endosymbiotic origin. No free-living algae are separated from the environment as cryptophyte and chlorarachniophyte fourmembrane chloroplasts do, but their endosymbiotic origin is beyond any doubt. Endosymbiotic hypotheses need to explain the structural peculiarities of the nuclear membrane, but the origin of the nuclear membrane and its selective advantages are also puzzling for non-endosymbiotic supporters. Finally, Staub et al. argue that nucleus replication involves membrane disintegration, something that obviously does not occur in prokaryotes. However, whilst several eukaryotic groups break down their nuclear membrane during mitosis (the so-called ‘‘open mitosis’’), many others do not (‘‘closed mitosis’’, more similar to the replication of a prokaryotic cell).(18) In some groups (e.g. green algae), both mitosis forms exist. The key question is to know which mitosis type, open or closed, is ancestral. Since both types are widespread in the eukaryotic tree, a simple inspection of their distribution across the eukaryotic phyla does not provide a clear answer. Interestingly, most hypotheses to explain the evolution of mitosis based on the characteristics of the closed and open mechanisms state that the closed mitosis predated the open one, an idea consistent with an endosymbiotic origin of the nucleus.(18) In summary, Staub et al. have carried out a very interesting analysis that sheds light on the origin and evolution of the nucleolus, but their results are compatible with very different hypotheses for the origin of the nucleus, including the endosymbiotic theories. Their arguments against a possible endosymbiotic origin can be debated and are disconnected from their observations concerning the nucleolus. The origin of the nucleus remains an open question. References Response to Moreira et al. called ‘‘hydrogen hypothesis’’.(1,2) We cannot (and did not) rule out other hypotheses but, in the following, we will explain in more detail why we favour the ‘‘hydrogen hypothesis’’ from the standpoint of nucleolus evolution. Moreira et al.’s description of our main results is partly correct: the core nucleolar protein machinery is of archaeal Sir, In our recent article about the nucleolar protein domain repertoire, we embedded a plausible scenario for nucleolus evolution into a hypothesis on eukaryote evolution, the so- BioEssays 26:1145–1147, ß 2004 Wiley Periodicals, Inc. 1. Andersen JS, Lyon CE, Fox AH, Leung AK, Lam YW, et al. 2002. Directed proteomic analysis of the human nucleolus. Curr Biol 12:1–11. 2. Scherl A, Coute Y, Deon C, Calle A, Kindbeiter K, et al. 2002. Functional proteomic analysis of human nucleolus. Mol Biol Cell 13:4100–4109. 3. Staub E, Fiziev P, Rosenthal A, Hinzmann B. 2004. Insights into the evolution of the nucleolus by an analysis of its protein domain repertoire. Bioessays 26:567–581. 4. Zillig W. 1991. Comparative biochemistry of Archaea and Bacteria. Curr Op Genet Develop 1:544–551. 5. Lake JA, Rivera MC. 1994. Was the nucleus the first endosymbiont? Proc Natl Acad Sci USA 91:2880–2881. 6. Gupta RS, Golding GB. 1996. The origin of the eukaryotic cell. Trends Biochem Sci 21:166–171. 7. Margulis L. 1970. Origin of eukaryotic cells. Yale University Press. 8. Searcy DG. 1992. Origins of mitochondria and chloroplasts from sulfurbased symbioses. In: Hartman H, Matsuno K, editors. The origin and evolution of the cell. World Scientific; pp 47–78. 9. Martin W, Müller M. 1998. The hydrogen hypothesis for the first eukaryote. Nature 392:37–41. 10. Moreira D, López-Garcı́a P. 1998. Symbiosis between methanogenic archaea and delta-Proteobacteria at the origin of eukaryotes: The syntrophic hypothesis. J Mol Evol 47:517–530. 11. López-Garcı́a P, Moreira D. 1999. Metabolic symbiosis at the origin of eukaryotes. Trends Biochem Sci 24:88–93. 12. Horiike T, Hamada K, Kanaya S, Shinozawa T. 2001. Origin of eukaryotic cell nuclei by symbiosis of Archaea in Bacteria is revealed by homologyhit analysis. Nat Cell Biol 3:210–214. 13. Martin W. 1999. A briefly argued case that mitochondria and plastids are descendants of endosymbionts, but the nuclear compartment is not. Proc R Soc Lonod 266:1387–1395. 14. Cavalier-Smith T. 2002. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52:297– 354. 15. Cavalier-Smith T. 2003. Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryoteeukaryote chimaeras (meta-algae). Philos Trans R Soc Lond B Biol Sci 358:109–134. 16. Fenchel T, Finlay BJ. 1995. Ecology and evolution in anoxic worlds. Oxford University Press. 17. Agarraberes FA, Dice JF. 2001. Protein translocation across membranes. Biochim Biophys Acta 1513:1–24. 18. Raikov IB. 1994. The diversity of forms of mitosis in Protozoa: a comparative review. Europ J Protistol 30:253–269. David Moreira Louis Ranjard Purificación López-Garcia Unité d’Ecologie, Systématique et Evolution UMR CNRS 8079, Université Paris-Sud bâtiment 360, 91405 Osay Cedex France E-mail: [email protected] DOI 10.1002/bies.20122 Published online in Wiley InterScience (www.interscience. wiley.com). BioEssays 26.10 1145