Evolution of the cytoskeleton

Abstract

SummaryThe eukaryotic cytoskeleton appears to have evolved from ancestral precursors related to prokaryotic FtsZ and MreB. FtsZ and MreB show 40−50% sequence identity across different bacterial and archaeal species. Here I suggest that this represents the limit of divergence that is consistent with maintaining their functions for cytokinesis and cell shape. Previous analyses have noted that tubulin and actin are highly conserved across eukaryotic species, but so divergent from their prokaryotic relatives as to be hardly recognizable from sequence comparisons. One suggestion for this extreme divergence of tubulin and actin is that it occurred as they evolved very different functions from FtsZ and MreB. I will present new arguments favoring this suggestion, and speculate on pathways. Moreover, the extreme conservation of tubulin and actin across eukaryotic species is not due to an intrinsic lack of variability, but is attributed to their acquisition of elaborate mechanisms for assembly dynamics and their interactions with multiple motor and binding proteins. A new structure-based sequence alignment identifies amino acids that are conserved from FtsZ to tubulins. The highly conserved amino acids are not those forming the subunit core or protofilament interface, but those involved in binding and hydrolysis of GTP. Historical introduction Discoveries of the prokaryotic cytoskeletonBefore 1990, the cytoskeleton was thought to have evolved only in eukaryotes. Relatives or homologs of actin, tubulin or intermediate filaments were unknown in bacteria or archaea. There were sporadic reports of candidates for bacterial actin and tubulin in the 1970s and 1980s but, apart from some intriguing images of microtubules in certain bacteria,(1) these turned out to be wrong and/or were not followed up.The first suggestions of a bacterial homolog of tubulin appeared in 1992. Three groups independently discovered that the bacterial cell division protein FtsZ bound and hydrolyzed GTP, as does tubulin, and had a seven-amino-acid sequence, GGGTGTG, virtually identical to the "tubulin signature sequence".(2-4) Mukherjee and Lutkenhaus(37) then extended the sequence alignment to find a dozen additional amino acids that were completely conserved in FtsZ and in α, β and γ tubulins. They also showed that FtsZ assembled in vitro into filamentous structures. Erickson et al. (5) found that FtsZ assembled into protofilaments that could adopt two conformations, straight and curved, similar to the straight protofilaments of the microtubule wall and the tubulin rings that peel away from microtubules during disassembly. Any question of homology was resolved when tubulin and FtsZ were found to have virtually identical structures at the level of protein folding.(6,7)If one looks for bacterial relatives of tubulin or actin using a simple computer search for sequence similarity, nothing will be found. In 1992 Bork et al.(8) used a sophisticated structurebased sequence alignment, and they discovered that bacteria did have genes related to actin. Actin is...

The Chloroplast Tubulin Homologs FtsZA and FtsZB from the Red Alga Galdieria sulphuraria Co-assemble into Dynamic Filaments

“…Bacteria are rarely larger in diameter than ϳ1 m, whereas chloroplasts are typically ϳ5 m (35). The Z ring assembled from a single FtsZ may be able to function only up to ϳ1 m diameter (36). The second FtsZ may somehow give flexibility to initiate assembly and constriction at a much larger diameter.…”

GTP-dependent Heteropolymer Formation and Bundling of Chloroplast FtsZ1 and FtsZ2

“…FtsZ proteins are widely believed to be the evolutionary progenitors of eukaryotic ␣-and ␤-tubulin (7,8,57), and the discovery of two FtsZ types in chloroplasts raised the question of whether they might have a similar functional relationship (15,25). The demonstration that FtsZ1 and FtsZ2 are capable of polymerizing independently of one another (Refs.…”

Lessons from bacterial homolog of tubulin, FtsZ for microtubule dynamics

“…The evolution of cytoskeleton from FtsZ to microtubules has been discussed previously (Erickson 2007). Being extremely divergent from their precursor protein FtsZ, tubulins show a high level of conservation across modern eukaryotic species while bacterial FtsZ shows 40-50% sequence identity across species.…”

“…Being extremely divergent from their precursor protein FtsZ, tubulins show a high level of conservation across modern eukaryotic species while bacterial FtsZ shows 40-50% sequence identity across species. FtsZ is considered to be an ancient protein and the division mechanism carried out in the first cellular forms was suggested to be carried out by FtsZ (Davis 2002, Erickson 2007. The process was successful enough to be retained in the modern species of bacteria and archaea (Davis 2002, Erickson 2007.…”