PerspectiveEvolution

Intermediate Steps

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Science  26 Nov 2010:
Vol. 330, Issue 6008, pp. 1187-1188
DOI: 10.1126/science.1196720

Identifying the origin of the prokaryote-eukaryote transition has been a long-standing and contentious issue (1, 2) with numerous hypotheses. Over the last decade, “fusion hypotheses” have dominated the field (3). Many of these propose that the fusion of two prokaryotes accounts for the seemingly chimeric nature of the eukaryote gene set. Other theories propose that eukaryotes and archaea shared an ancestor that emerged from a bacterium (4). Thus, eukaryotes may be a mosaicism, combining features (including genes) inherited from a bacterial ancestor with those developed by an archaeal-eukaryotic ancestor before the split between eukaryotes and archaea. The hypotheses and debates about ancient cellular evolution continue as our knowledge of molecular and cellular mechanisms in all three domains of life expands (5). One intriguing curiosity is a “superphylum” of bacteria whose members display features of archaea and eukaryotes. What might these unusual organisms suggest in terms of evolution? It may be that their ancestor served as a “cauldron” for the evolution of eukaryotic and archaeal features, and that the superphylum is indicative of a path of intermediate steps between such an ancestor and an archaeal-eukaryotic ancestor (before the eventual split of the two domains).

The Planctomycetes, Verrucomicrobia, Chlamydiae (PVC) superphylum is an assemblage of Gram-negative bacterial phyla that is considered a monophyletic group in various phylogenetic trees derived from molecular sequence comparison (6). Some display genetic and cellular features that are unusual for bacteria but are characteristic of eukaryotes or archaea (see the figure). This mixture of phenotypes in current PVC members raises the hypothesis that they may be related to intermediate steps of eukaryotic and archaeal origin. Examination of this mixture of phenotypes can serve as a starting point for considering whether such features originated in a PVC-related ancestor from which the common eukaryotic and archaeal branch arose.

Two major steps in eukaryotic and archaeal evolution are loss of the peptidoglycan-based cell wall of bacteria and replacement of the bacterial cytoskeletal protein FtsZ with eukaryotic tubulin. PVC members appear “intermediate” for both events. Some members synthesize peptidoglycan (Verrucomicrobia), whereas others do not (Planctomycetes and Chlamydiae) (7). Similarly, genomic information indicates that the last common ancestor of PVC bacteria possessed an FtsZ-based cell-division mechanism. However, Chlamydiae and Planctomycetes do not encode FtsZ in their genomes (7). The Prosthecobacter species (Verrucomicrobia phylum) have both FtsZ-like and tubulin-like genes (8, 9), which is unique among all bacterial phyla and has puzzled microbiologists.

Development of the endomembrane system that compartmentalizes the cytoplasm has been crucial to eukaryogenesis (10, 11), but its origin is still mysterious. The functional and molecular similarities observed between the bacterial (Gram-negative) periplasm and eukaryotic endomembrane system (the space inside the organelles) underlies the hypothesis that the latter resulted from the internalization of the former by invagination of the bacterial inner membrane (10). Again, the membrane morphologies observed in PVC members appear intermediate. The PVC periplasm (or paryphoplasm) is usually larger with a more complex organization than the bacterial periplasm. Particularly, but not only, in the planctomycete Gemmata obscuriglobus, the inner membrane forms invaginations in the cytoplasm, sometimes in close contact with the DNA, in a way that appears to be dynamic and cell cycle dependent. The presence of ribosomes lining those invaginations is reminiscent of the eukaryotic rough endoplasmic reticulum, and vesicle-like structures are observed in G. obscuriglobus. This organization is sustained by proteins that may be related to those of the eukaryotic endomembrane system (11). PVC paryphoplasms may illustrate intermediate evolutionary attempts from the bacterial periplasm to the eukaryotic endomembrane system.

Superphylum features.

The PVC superphylum of bacteria display features found in eukaryotes (Eu) and archaea (Ar). The particular feature is observed in at least one member of the indicated bacterial phylum. Methanobacteriales is an order of the Euryarchaeota that possess a pseudopeptidoglycan that differs from bacterial peptidoglycan (*). FtsZ is present in the main archaeal division of Euryarchaeota and absent from crenarchaeota (**). Budding also occurs in Proteobacteria (***). Planctomycetes (Pl), Verrucomicrobia (Ve), Chlamydiae (Ch).

Periplasm internalization could provide a plausible scenario for the acquisition of mitochondrial precursors by eukaryotes (12). According to the endosymbiotic hypothesis, symbiosis and parasitism would allow progressive adaptation of both partners to each other. Some microbial symbionts or parasites reside in the host's periplasm. For example, Bdellovibrio bacteria are located in the periplasm of Gram-negative bacteria (13). The archaeon Nanoarcheaum equitans also localizes to the periplasm of the archaeon Ignicoccus hospitalis (14). Upon internalization of the periplasm, those guests would reside in the lumen of the internalized membranes.

Endocytosis development is linked to the development of the endomembrane system. Strikingly, the planctomycete G. obscuriglobus is the only bacterium in which a related process has been reported (15), again possibly reflecting an intermediate step between bacteria and eukaryotes. This proposal also offers a plausible intermediate for the development of the archaeal membrane that contains ether-linked lipids instead of the ester linkage found in bacterial and eukaryotic lipids (16, 17). The divergent planctomycete group, the Anammox bacteria, is so far, the only organism with membranes containing both ether- and ester-linked lipids.

The PVC bacteria are indeed a curiosity and their phylogenetic location in the Tree of Life is unclear. Although these features could be the result of lateral gene transfer events, convergence, or a complex universal ancestor, their intermediate nature can be considered a more parsimonious scenario. The possibility of a fusion scenario remains disputed (18). More evolutionary scenarios are likely to unfold—and be debated—as more bacteria and archaea are discovered and characterized. Although division into three domains of life remains the norm (19), the PVC superphylum may reflect continuity between the three domains, blurring their distinction.

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