Multiple Secondary Origins of the Anaerobic Lifestyle in Eukaryotes T

Phil. Trans. R. Soc. B (2006) 361, 1055–1067 doi:10.1098/rstb.2006.1844 Published online 3 May 2006 Multiple secondary origins of the anaerobic lifestyle in eukaryotes T. Martin Embley* Division of Biology, The Devonshire Building, University of Newcastle upon Tyne, NE1 7RU, UK Classical ideas for early eukaryotic evolution often posited a period of anaerobic evolution producing a nucleated phagocytic cell to engulf the mitochondrial endosymbiont, whose presence allowed the host to colonize emerging aerobic environments. This idea was given credence by the existence of contemporary anaerobic eukaryotes that were thought to primitively lack mitochondria, thus providing examples of the type of host cell needed. However, the groups key to this hypothesis have now been shown to contain previously overlooked mitochondrial homologues called hydrogenosomes or mitosomes; organelles that share common ancestry with mitochondria but which do not carry out aerobic respiration. Mapping these data on the unfolding eukaryotic tree reveals that secondary adaptation to anaerobic habitats is a reoccurring theme among eukaryotes. The apparent ubiquity of mitochondrial homologues bears testament to the importance of the mitochondrial endosymbiosis, perhaps as a founding event, in eukaryotic evolution. Comparative study of different mitochondrial homologues is needed to determine their fundamental importance for contemporary eukaryotic cells. Keywords: mitochondria; hydrogenosomes; mitosomes; anaerobic eukaryote evolution 1. INTRODUCTION Despite the plausibility of the above scenario we will Many classical theories for eukaryotic origins suggested probably never know why two disparate ancient cells that eukaryotes originated under anaerobic conditions, came, and then stayed, together. Consequently, and were primitively without mitochondria (e.g. opinions are diverse concerning the ecological context Goksoyr 1967; Cavalier-Smith 1983b). A member of and selective advantages for host and endosymbiont this anaerobic eukaryotic community is posited to have (e.g. John & Whatley 1975; Martin & Mu¨ ller subsequently phagocytosed a eubacterium that could 1998; Cavalier-Smith 2002; Embley & Martin 2006). carry out aerobic respiration and which subsequently What does seem well founded is that the resulting became an endosymbiont ( John & Whatley 1975). The host–endosymbiont consortium forged the common presence of this eubacterial endosymbiont allowed the ancestor of all of the mitochondrion-containing host to colonize aerobic environments. A variety of eukaryotes that are seen today. Thus, a single common mechanisms have been suggested as to why this should origin for all mitochondria is supported by phyloge- be so; the most popular, and one that features in a netic analyses of the genes encoded by mitochondrial variety of different formulations for mitochondrial genomes (Yang et al. 1985; Gray et al. 2004). The origins (Woese 1977; Martin & Mu¨ller 1998; Vellai anaerobic eukaryotes that did not participate in the et al. 1998; Kurland & Andersson 2000), being the mitochondrial endosymbiosis, have been posited either removal of cytosolic oxygen by the endosymbionts’ to have gone extinct, due to an inability to deal respiratory activity. The feasibility of this idea, at least with rising oxygen levels or some other catastrophe as a mechanism, is supported by a modern analogue (Philippe & Adoutte 1998; Vellai et al. 1998), or to have among contemporary ciliate protozoa. Strombidium persisted in anaerobic habitats to the present day purpureum lives in anaerobic marine sands and contains (Cavalier-Smith 1983b; Margulis et al. 2005). facultatively aerobic photosynthetic endosymbiotic The persistence hypothesis is plausible for several bacteria. In the light, Strombidium avoids even traces reasons. Anaerobic habitats have existed throughout of oxygen (less than 1% atmospheric saturation) and Earth’s history and they harbour anaerobic bacteria, the endosymbionts probably use host substrates for providing food for phagotrophic eukaryotes. Extinction anoxygenic photosynthesis. In the dark, the ciliates, in the microbial world may also be rare because of large population sizes, ease of dispersal and the occurrence protected against O2-toxicity by the endosymbionts’ aerobic respiration, accumulate in water with a partial of resistant stages (Fenchel 1993). Even transient anaerobic habitats generally possess protist inhabitants. pressure of O2 of 1–4% atmospheric saturation (Fenchel & Bernard 1993a,b; Bernard & Fenchel As ancient oxygen levels rose, the occupants of 1994). anaerobic habitats on the margins of the aerobic world would actually benefit from the reduced carbon derived from oxygenic photosynthesis. In modern *[email protected] situations, the activities of oxygenic phototrophs One contribution of 14 to a Discussion Meeting Issue ‘Major steps in often provide the reducing power, in the form of cell evolution’. organic material, to maintain anoxic environments; 1055 q 2006 The Royal Society 1056 T. Martin Embley Multiple origins of anaerobic eukaryotes contemporary anaerobic life is most rich in the vicinity for which it was formulated, have been extensively of aerobic life (Fenchel & Finlay 1995). In conclusion, reviewed (Embley et al. 2003b; van der Giezen et al. there are no compelling reasons drawn from con- 2005; Embley & Martin 2006), so only a few points will temporary ecosystems, to suppose that primitively be made here in relation to each type of evidence and to amitochondriate eukaryotes, if they ever existed, controversies, where they exist, surrounding the would have gone extinct simply because they did not interpretation of these data. participate in the mitochondrial endosymbiosis. All of the best-studied archezoans have now been The persistence hypothesis was supported by the shown to contain host–nuclear-encoded genes of discovery of contemporary eukaryotes that apparently putative mitochondrial ancestry (table 1). That is, lacked mitochondria. These eukaryotes, called Arche- they contain genes that encode proteins that in aerobes zoa to indicate that the absence of mitochondria was a typically function in mitochondria and, when the primitive state, not a derived state resulting from proteins are subjected to phylogenetic analysis, they secondary loss, included Entamoeba, Giardia, Tricho- form a monophyletic group with the alpha-proteobac- monas and Microsporidia, and their various close teria. This is the group of bacteria from which the relatives (Cavalier-Smith 1983a,b). As well as not mitochondrial endosymbiont is held to have originated having mitochondria, these species were thought to based upon analyses of genes that are encoded by lack other features common to most eukaryotes, mitochondrial genomes (Yang et al. 1985; Gray et al. including Golgi dictyosomes and peroxisomes, sup- 2001). One criticism of using the genes in table 1 to porting their early emerging status (Cavalier-Smith reject the Archezoa hypothesis is that none of them 1987a; Patterson & Sogin 1992). Archezoa or have ever been found on a mitochondrial genome Hypochondria as they were also known (Patterson & (Gray et al. 2004; Gray 2005). Such a location, which is Sogin 1992), thus became models for studying early found for some of the proteins involved in oxidative eukaryotic evolution and the features of the first phosphorylation, the canonical function of aerobic eukaryotic cells. Some suggested that the peculiar mitochondria, would make a direct link between gene features of Archezoa could also be a derived state and organelle. To explain the localization of genes of (Wolters 1991; Siddall et al. 1992), caused, or perhaps mitochondrial ancestry on host nuclear genomes, it is facilitated, by the adaptation of Archezoa to their necessary to posit that they were transferred from the parasitic or anaerobic lifestyles. But that debate was endosymbiont genome to the host nuclear genome unresolved because there was no clear comparative during the process of transforming endosymbiont into evidence that convincingly linked the Archezoa to an organelle ( John & Whatley 1975; Viale & Arakaki eukaryotic groups that possessed mitochondria or the 1994). This process has been called endosymbiotic other debated features. gene transfer and it is still ongoing (Timmis et al. The Archezoa hypothesis was founded in compara- 2004). For example, among plants there are examples tive cytology as a taxonomic hypothesis designed to where particular genes appear on the mitochondrial draw attention to a group of eukaryotes which might genome in some lineages, but in other lineages they are provide a glimpse into a pre-mitochondrial phase of encoded by the host nuclear genome (Adams & Palmer eukaryotic evolution (Cavalier-Smith 1983a,b). It was 2003). Despite the need to invoke such gene transfer, thus enormously useful as a guide to study. It gained the hypothesis that the genes in table 1 came from the considerable support when the first phylogenetic trees mitochondrial endosymbiont is probably now the based upon molecular sequence data (Vossbrinck et al. standard interpretation of these data (Boorstein et al. 1987; Sogin et al. 1989; Leipe et al. 1993; Hashimoto 1994; Viale & Arakaki 1994; Clark & Roger 1995). et al. 1997) did indeed place key archezoans before It has also been suggested that archezoans could other eukaryotes with mitochondria. Doubts were have acquired the genes in table 1 from a source other expressed about the veracity of these trees (e.g. Wolters than the mitochondrial

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