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Thursday, 8 December 2011

Bacterial origin to our cytoskeleton?

FtsZ is the (almost) ubiquitous protein forming rings or pseudo-rings involved in bacterial division, while tubulin is the main eukaryotic cytoskeleton. The nature of the relationship and order of evolution between FtsZ and tubulin is unclear. It is clear that all tubulins evolved from a common ancestor shared with the bacterial FtsZ. In a beautiful article, Pilhofer and Jense (PLoS Biology 2011) add new evidences suggesting an ancient relationship between bacterial tubulin homologues and the eukaryotic ones. The discovery of bacterial tubulin in several Prosthecobacter, members of the Verrucomicrobia phylum, came as a surprise. The two genes, btubA and B are present in most, but not all, Prosthecobacter species. This diffuse pattern is similar to other eukaryotic or archaeal features found in PVC members. However, the function of BtubA/B in Prosthecobacter is unclear since they coexist with FtsZ also present in the proteome of those species. Is FtsZ also involved in cell division in Prosthecobacter is another question that would be fascinating to answer, as it has been shown that FtsZ can have divergent roles, not all of them involved in division, discussed in a previous post, Non FtsZ based division in Thaumarchaea, although in this case in archaea. It had been previously suggested that the bacterial tubulin genes were the results of lateral gene transfer, mainly based on genomic organization. On the other side, shaperon-less folding, weak associations (all presumably ancient properties) and sequence features argued against LGT and in favor of an ancient ancestral relationship between the proteins. Pilhofer et al. first realised the most comprehensive phylogenetic analysis of the tubulin family and failed to detect any stable associations between the bacterial and any eukaryotic tubulin subfamilies. They then undertook electron microscopy to show that BtubA/B form microtubules in bateria. They beautifully show that the bacterial microtubules are composed of only five protofilaments, unlike the eukaryotic ones that contain 13.
Figure 4. Structural model of “bacterial microtubules.”
(A) 2-D schematic of the proposed architecture of bacterial microtubules built from BtubA (dark-blue) and BtubB (light-blue). Protofilaments are numbered 1–5. (B) 3-D comparison of the architectures of a bacterial microtubule (left; BtubA in dark-blue; BtubB in light-blue) and a 13-protofilament eukaryotic microtubule (right; β-tubulin in black; α-tubulin in white). Seams and start-helices are indicated as in (A). doi:10.1371/journal.pbio.1001213.g004
This is to me the most compelling evidence to date against the LGT hypothesis. They thus suggest that the following scenario:
It therefore appears that in tubulin evolution, heterodimer formation correlated with tube formation and the five-protofilament, one-start helix was the simplest and earliest microtubule architecture realized, which later evolved into the larger eukaryotic microtubule ... An alternative "vertical evolution" hypothesis is that btubAB was present in the last common ancestor of Verrucomicrobia, but the genes were simply lost by the other members of the phylum.
Illustrated in this picture:
Figure 7. Model for the evolution of BtubA/B.
Tubulins, FtsZ, FtsZ-like, and TubZ all evolved from a common ancestor with the likely properties listed [5],[9],[58][61]. In contrast to the bacterial FtsZ, FtsZ-like, and TubZ proteins, the last common tubulin ancestor appears to have evolved to form heterodimers (consisting of “A”- and “B”-tubulins) with properties that enabled tube formation. Modern α- and β-tubulin further localized the activating T7 and short S9, S10 loop into different subunits, developed a need for chaperones, and began to form larger, ~13-protofilament microtubules. In contrast, BtubA and BtubB retained ancient features shared by FtsZ such as chaperone independence, weak dimerization, and both an activating T7 loop and short S9, S10 loop in both subunits [17],[19],[21]. The smaller, five-protofilament, one-start-helical architecture of the bacterial microtubule is therefore likely a primordial form. The ancestry of the other supplemental tubulins γ through κ is unclear, except that θ- and κ-tubulins derived from β and α, respectively. doi:10.1371/journal.pbio.1001213.g007

This is not unlike the presence of many features inferred to have been present in the last PVC common ancestor, and then subsequently lost in various members, as suggested in the Devos & Reynaud publications Science Perspective (2010) and Proc. Royal Soc. B (2011). As stated by the authors,
It is presently debated whether an ancient Planctomycetes-Verrucomicrobia-Chlamydiae bacterium was involved in the evolution of eukaryotes, but if so, such a relationship would be consistent with bMTs preceding modern eukaryotic MTs.
All in all, this suggest a bacterial origin to our cytoskeleton.

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