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Dispatch R315 Organelle origins: Energy-producing symbionts in early eukaryotes? Mitchell L. Sogin The discovery that Trichomonas vaginalis, an early diverging protist that lacks mitochondria but has energy-producing hydrogenosomes, makes bacteriallike heat shock proteins suggests that symbionts ancestral to mitochondria and hydrogenosomes were present at early stages of eukaryote evolution. Address: Bay-Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, Massachusetts 02543, USA. Electronic identifier: 0960-9822-007-R0315 are micro-aerophilic, and most have adopted parasitic lifestyles; none contains a recognizable mitochondrion, but trichomonads possess hydrogenosomes. This suggested that, if the rRNA-based trees were accurate reflections of evolutionary history, then inventories of the ancestral features of early eukaryotes should not include mitochondria. Four recent studies of heat shock proteins [5–8] challenge this view of mitochondrial origins. The hydrogenosomes of Trichomonas vaginalis contain heat shock proteins similar to those found in mitochondria; these organelles may be descendants of the ‘first mitochondria’ [9]. Current Biology 1997, 7:R315–R317 © Current Biology Ltd ISSN 0960-9822 The transition from a prokaryotic to a eukaryotic cell architecture generated one of the largest discontinuities in our evolutionary history. Unlike bacteria and archaebacteria, eukaryotes retain their genetic information, replication and transcription machinery within a nuclear envelope, and have an endomembrane-mediated system of protein sorting and transport. Most eukaryotes compartmentalize aerobic energy metabolism within mitochondria, the only exceptions being amitochondriate protists, which produce energy by fermentation in the cytoplasm or within organelles called hydrogenosomes (Fig. 1) [1]. The innovation of energy-producing organelles forever altered metabolism in the eukaryotic line of descent. To understand when this occurred, it is necessary to know the phylogenetic distribution of protists that lack mitochondria, as well as the placement of eukaryotes that contain hydrogenosomes. The origins of mitochondria and plastids are inextricably tied to symbiotic relationships between eukaryotes and particular bacterial groups. Ultrastructural, biochemical and molecular sequence data all show that mitochondria share a common evolutionary history with members of the alphadivision of purple photosynthetic bacteria (a-proteobacteria), and that cyanobacteria were the progenitors of Figure 1 Nearly thirty-five years ago, the introduction of electron microscopy and new techniques for exploring ultrastructure radically transformed views of protist evolution. Instead of three or four classes of protists, sixty or seventy major lineages were recognized. The relative branching patterns of these lineages, however, remained speculative until the construction of molecular trees [2]. The ensuing studies, largely based on sequences of ribosomal RNAs (rRNAs), confirmed the ultrastructure classifications, but also provided quantitative measures of genetic relatedness that can be used to infer relative branching orders. Three protist groups, the diplomonads, microsporidia and trichomonads, are basal to all other eukaryotes [3]. Their divergence is followed by a series of independent protist branchings, and then by the nearly simultaneous divergence of animals, plants, fungi and several other protist groups. These suddenly diverging taxa form the ‘crown’ of the eukaryotic tree [4]. The earliest diverging eukaryotes A hydrogenosome of Trichomonas foetus, a close relative of the protist T. vaginalis discussed in the text, showing the characteristic marginal plate (m) and dense core (c). (Photograph courtesy M. Müller and H. Shio, reproduced with permission from [11].) R316 Current Biology, Vol 7 No 5 plastids. (Support for the endosymbiotic origins of other organelles, such as basal bodies, is more tenuous.) Here, I shall discuss the origin of hydrogenosomes in micro-aerotolerant protists and what that might tell us about the presence or absence of mitochondria in the earliestbranching eukaryotes. Hydrogenosomes are factories for anaerobic energy production. They use the enzymes pyruvate:ferredoxin oxidoreductase and hydrogenase — which are characteristic of anaerobic bacteria — and the substrates pyruvate or malate to produce ATP, acetate, carbon dioxide and large amounts of hydrogen [1]. These organelles are doublemembrane structures which divide by fission, lack DNA and contain approximately 300 different proteins. Organisms that contain hydrogenosomes are unlike other eukaryotes, as they are amitochondriate and generally live as facultative anaerobes. Yet their numerous ultrastructural and biochemical similarities suggest that hydrogenosomes and mitochondria have a shared evolutionary history. Alternatively, these common features might be superficial: hydrogenosomes may have arisen from independent endosymbioses between anaerobic bacteria and eukaryotes. To differentiate between these various possibilities, several research groups [5–8] have searched the Trichomonas vaginalis genome for coding regions that encode proteins related to those found in mitochondria. They looked in particular for genes encoding proteins related to the three main types of mitochondrial heat shock protein (Hsp) — Hsp10, Hsp60 and Hsp70 — because sequences of these genes are particularly useful for inferring bacterial phylogeny. As trichomonads contain hydrogenosomes but not mitochondria, the identification of Hsp genes encoding hydrogenosome Hsps related to those of mitochondria would constitute evidence that these energy-producing organelles have a shared common ancestry. Some Hsp genes are induced by environmental stress, others encode molecular chaperones that stabilize partially folded proteins during their translation or intracellular transport. Hsp genes are present in bacterial and nuclear genomes, but not in those of eukaryotic organelles or (with the exception of Hsp70) archaebacteria; the Hsps that localize to eukaryotic organelles are nuclear-encoded and transported to their appropriate destinations. Bacteria and archaebacteria have a single Hsp70 gene, but eukaryotes generally have multiple Hsp70 genes encoding distinct proteins that localize in the endoplasmic reticulum, cytosol and mitochondria or hydrogenosomes. The assumption is that nuclear genes for organellar proteins migrated from the organellar genome at some point during eukaryotic evolution after the acquisition of the endosymbiont from which the organelle is thought to be derived. If mitochondria and hydrogenosomes have a common evolutionary history, the genes encoding their Hsps should be phylogenetically related. The presence of mitochondrionlike Hsp genes in deeper branches of the eukaryotic tree would provide presumptive evidence that the earliest diverging eukaryotes had mitochondria. This argument has been applied to the amitochondriate Entamoebae, which is presumed to be on a lineage of protists that once had mitochondrion-like organelles [10]. By taking advantage of conserved sequences in Hsp genes, putative homologues from T. vaginalis have now been cloned, sequenced and subjected to phylogenetic analysis [5–8]. In all cases, a battery of inference techniques place the trichomonad Hsp sequences on the lineage that contains mitochondria. For example, tree topologies that unite mitochondrial and trichomonad hydrogenosome Hsp60s are statistically robust; the Hsp60 trees also show specific relationships between mitochondria and rickettsial members of the a-proteobacteria. Similarly, the Hsp70 trees demonstrate a convincing relationship between of the trichomonad hydrogenosomes with mitochondria, but not with a-proteobacteria. Mitochondria and hydrogenosomes must thus have a common evolutionary history — but at what point did their lineages diverge? Hydrogenosomes may have evolved from an endosymbiont that was ancestral to mitochondria [8], but this seems unlikely because hydrogenosomes are present in anaerobic fungi and rumen ciliates. In phylogenetic trees based on molecular data, the anaerobic fungi and rumen ciliates are ‘crown group’ taxa which diverged well after the endosymbiotic event that produced eukaryotic mitochondria. Hydrogenosomes were thus present in late-diverging, as well as early-diverging, eukaryotes. This means that, if we interpret all hydrogenosomes as being derived from an ancestral symbiont that also gave rise to mitochondria, the transition from symbiont to hydrogenosomes or to mitochondria would have occured many times. It seems more likely that hydrogenosomes are, in fact, highly reduced and modified descendants of mitochondria. A second possibility is that two or more independent endosymbiotic events occurred, one giving rise to the trichomonad hydrogenosomes and the other the mitochondria found in extant eukaryotes. The two endosymbionts would have been different, but closely related, a-proteobacteria. This would explain the similarity between mitochondrial and trichomonad Hsp genes. The trichomonad endosymbiont might have been transient and merely allowed transfer of several bacterial genes, including those for heat shock proteins, to the nuclear genome. Bacterial symbionts occur in many phylogenetically diverse protists including amitochondriate pelobionts and the diplomonad Giardia lamblia. Endosymbiosis clearly did not occur just once during the evolution of eukaryotes; this process continues today, and sometimes even Dispatch involves two different species of eukaryote. Whenever endosymbiotic relationships are established, a window of opportunity is opened for transferring genetic information between genome compartments. This mechanism could explain how Hsp genes entered the nuclear genome of early diverging lineages such as the trichomonads. R317 medical and economical importance of these amitochondriate, parasitic protists. There may be earlier-diverging eukaryotes, perhaps living in anaerobic or extreme environments, awaiting discovery and placement in phylogenetic frameworks. Will they too have molecular evidence of hydrogenosomes or mitochondria? References A third possibility is that hydrogenosomes are highly reduced descendants of mitochondria. This implies mitochondria were present before the divergence of trichomonads. If these energy-producing organelles were present in the earliest branches of the eukaryotic tree, we would expect congruence between Hsp phylogenies and other nuclear gene trees. The Hsp10 data base is too small to address this issue, and the Hsp70 gene trees are not well resolved. Furthermore, the Hsp70 trees do not demonstrate a specific relationship between the mitochondrial lineage and a particular division of a-proteobacteria. The Hsp60 gene phylogeny shows better resolution with a sparse branching pattern that resembles the eukaryotic rRNA phylogenies and also provides modest support for the view that mitochondria and a-proteobacteria have a common evolutionary history. The sequencing of more Hsp genes may eventually clarify the number of endosymbiotic events that led to the formation of mitochondria and hydrogenosomes. With the data already available, however, we can make reasonable estimates about relative timing for the origins of energy producing organelles. The introduction of mitochondria and/or hydrogenosomes into the eukaryotic cell must have occurred after the nuclear lineage had diverged from the prokaryotic world. If this were not the case, genes for mitochondrial proteins would be more similar to ‘bona fide’ eukaryotic genes than to genes of bacteria or archaebacteria (the latter are now considered to be a sister group to all eukaryotes). Hsp and rRNA sequences provide convincing evidence that organellar genes are more closely related to their prokaryotic, than their eukaryotic, counterparts. The discovery of mitochondrion-like Hsp genes in earlydiverging, amitochondriate eukaryotes is only suggestive evidence that mitochondria were present in the last common ancestor of all extant eukaryotes. The origins of the trichomonad hydrogenosome and mitochondrial Hsp genes are presumably tied to one or more endosymbiotic events. Some of those events, however, could have occurred just after the separation of diplomonads from other amitchondriate taxa; the branching patterns for the deepest-diverging eukaryotic taxa are still unresolved. Furthermore, we do not know the identity of the earliestdiverging eukaryotic lineages. That we know the phylogenetic position of trichomonads, diplomonads and microsporidia is a historical accident, guided by the 1. Müller M: The hydrogenosome. J Gen Microbiol 1993, 139:2879–2889. 2. Patterson DJ, Sogin ML: Eukaryote origins and protistan diversity. In The Origin and Evolution of Prokaryotic and Eukaryotic Cells. Edited by Hartman H, Matsuno K. New Jersey: World Scientific Publishing Company; 1992:13–46. 3. Leipe D, Gunderson JH, Nerad TA, Sogin ML: Small subunit ribosomal RNA of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol Biochem Parasitol 1993, 59:41–48. 4. Knoll AH: The early evolution of eukaryotes: a geological perspective. Science 1992, 256:622–627. 5. Horner DS, Hirt RP, Kilvington S, Lloyd D, Embley TM: Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc R Soc London [Biol] 1996, 263:1053–1059. 6. Bui ETN, Bradley PJ, Johnson PJ: A common evolutionary origin for mitochondria and hydrogenosomes. Proc Natl Acad Sci USA 1996, 93:9651–9656. 7. Germot A, Philippe H, Guyader HL: Presence of a mitochondrialtype 70-kDa heat shock protein in Trichomonas vaginalis suggests a very early mitochondrial endosymbiosis in eukaryotes. Proc Natl Acad Sci USA 1996. 93:14614–14617. 8. Roger AJ, Clark CG, Doolittle WF: A possible mitochondrial gene in the early-branching amitochondriate protist Trichomonas vaginalis. Proc Natl Acad Sci USA 1996. 93:14618–14622. 9. Müller M: Evolutionary origins of trichomonad hydrogenosomes. Parasitol Today 1997, in press. 10. Clark CG, Roger AJ: Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc Natl Acad Sci USA 1995, 92:6518–6521. 11. Müller M: The hydrogenosome. In The Eukaryotic Microbial Cell. Society for General Microbiology Symposium 30. Edited by Gooday GW, Lloyd D, Trinci APJ. Cambridge, UK: Cambridge University Press; 1980:127–142.