Deep Questions in the Tree of Life

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Science  28 Sep 2007:
Vol. 317, Issue 5846, pp. 1875-1876
DOI: 10.1126/science.1149593

Agenome sequence might provide answers to major questions about the biology and evolutionary history of an organism. Alternatively, it might reveal more problems than solutions, and its true value then lies in identifying what questions to ask. Perhaps the most interesting genomes do both: They are a panacea and a Pandora's box. On page 1921 in this issue, Morrison et al. (1) describe such a genome from the diplomonad protist Giardia lamblia, a human intestinal parasite. The compact Giardia genome is replete with information ranging from the simplicity of its molecular systems to how the parasite interacts with its environment. However, the evolutionary history of Giardia is not so clearly written in the genome, reigniting a smoldering debate about the origin of Giardia and its relationship to other eukaryotes.

The evolution of Giardia has commanded a level of attention matched by few other organisms because it differs from the “textbook” eukaryote in many ways. Most notably, there are no mitochondria in Giardia or its relatives, in keeping with its tolerance for low levels of oxygen (2). The absence of this organelle took on new significance with the Archezoa hypothesis, which proposed that Giardia (and certain other protists) diverged from other eukaryotes before the endosymbiotic origin of mitochondria, and was therefore ancient and primitively amitochondriate (3). Early molecular phylogenies supported this view, placing Giardia and other Archezoa at the base of eukaryotic evolution (4, 5). The case seemed closed: Giardia arose from the prokaryote-eukaryote transition, one of the greatest transformations in evolution.

Eukaryotic evolution. The hypothetical evoultionary tree consists of five “supergroups” based on several kinds of evidence (15). The branching order of supergroups is unresolved, implying that the relationships are unknown rather than a simultaneous radiation. CM indicates the presence of cryptic mitochondria (hydrogenosomes or mitosomes). A question mark indicates that no organelle has yet been found.

The Archezoa hypothesis proved too good to be true. Nuclear genes phylogenetically related to mitochondrial homologs were discovered in Archezoa, including Giardia (4, 5). The protein products of such genes have been localized to double membrane-bounded organelles (hydrogenosomes or mitosomes) in all major Archezoan groups, and similar structures were found in distantly related eukaryotes (see the figure). Some of these organelles and their metabolic activities are well characterized (e.g., Trichomonas hydrogenosomes), but the functions of other cryptic organelles remain elusive (e.g., Entamoeba mitosomes). In Giardia, proteins involved in iron-sulfur cluster assembly and protein folding appear closely related to mitochondrial homologs and localize to a relict mitosome (6, 7). Interestingly, the Giardia genome contains little else of identifiable mitochondrial ancestry: No other functions can be predicted and protein-import complexes are reduced or highly divergent (1, 8).

The other implication of the Archezoa hypothesis—that Giardia is an early branching eukaryote—has attracted even more controversy. The “deep” position of some Archezoa has been convincingly undermined by showing that they belong elsewhere in the phylogenetic tree, the clearest case being the relationship between microsporidia and fungi (5). For Giardia, such a specific alternative is not so clear-cut, but the genome may provide clues. Diplomonads may belong to a group of protists known as excavates, specifically related to Parabasalia such as Trichomonas (9, 10). Like Trichomonas, the Giardia genome does not encode myosin (which is rarely absent from eukaryotic genomes) and encodes a bacterial arginine metabolism pathway, supporting a close relationship. This does not preclude an early divergence for both Giardia and parabasalids, for this depends on where the root of the eukaryotic tree lies, which is difficult to resolve. Indeed, there are doubts about how phylogenetic reconstruction methods can determine this root, given the unequal rates of sequence evolution and great genetic distance between eukaryotes and prokaryotes (11). There are also difficulties inherent in reconstructing the history of divergent genes with current phylogenetic methods, and large amounts of data that violate evolutionary models can generate well-supported errors (12). Morrison et al. show high levels of divergence in much of the Giardia genome, so although the genome may contain data to reconstruct Giardia's history, it will be a challenge to use it.

The outcome of this debate affects not only our understanding of early eukaryotic evolution, but also our view of Giardia biology. Simple characteristics could be primitive or derived via reduction, alternatives with very different meanings. The simplicity of Giardia's molecular systems differs from that of known derived parasites (1, 13). However, different lineages can follow different reductive paths (14), so determining Giardia's origins independently of its simplicity is essential. Given the depth of these questions, the new life that Morrison et al. have breathed into the debates is welcome, and will ensure continued attention on both a fascinating cell and the origin of eukaryotes.


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