Isolation of an ftsZ homolog from the archaebacterium Halobacterium salinarium: implications for the evolution of FtsZ and tubulin

Abstract

We have isolated a homolog of the cell division gene ftsZ from the extremely halophilic archaebacterium Halobacterium salinarium. The predicted protein of 39 kDa is divergent relative to eubacterial homologs, with 32% identity to Escherichia coli FtsZ. No other eubacterial cell division gene homologs were found adjacent to H. salinarium ftsZ. Expression of the ftsZ gene region in H. salinarium induced significant morphological changes leading to the loss of rod shape. Phylogenetic analysis demonstrated that the H. salinarium FtsZ protein is more related to tubulins than are the FtsZ proteins of eubacteria, supporting the hypothesis that FtsZ may have evolved into eukaryotic tubulin.FtsZ is an essential cell division protein in Escherichia coli and Bacillus subtilis (3, 9) and appears to be conserved among eubacteria (8). It polymerizes to form a circumferential ring at the division site, constricting at the leading edge of the invaginating septum that will eventually separate the two daughter cells (6,26). FtsZ both shares biochemical properties with and has structural similarities to eukaryotic tubulins. Both bind and hydrolyze GTP, polymerize to form tubules in a GTP-dependent manner, and are involved in cytoskeletal processes in the cell during cell division (7,10,31,32,37). All identified FtsZ proteins from eubacteria contain a conserved N terminus that carries the tubulin-like GTP-binding motif and a hydrophilic, variable C terminus.Although the role of FtsZ in cytokinesis differs from the actin-mediated cytokinesis in eukaryotic cells, the biochemical and amino acid sequence data have led to the proposal that FtsZ is a prokaryotic version of tubulin (14). Since the origins of the eukaryotic cytoskeleton are unknown, an intriguing hypothesis is that FtsZ evolved into tubulin. Since it is believed that the archaea and eucarya diverged after the divergence of archaea from bacteria, then identification of an FtsZ protein in an archaebacterial species might shed light on this evolutionary question (18,21). Because archaebacteria in general have a prokaryotic cellular organization similar to that of eubacteria, it is reasonable to propose that their cell division requires an FtsZ homolog derived from the common ancestor of all living cells (44).To gain insight into FtsZ evolution and diversity, we have isolated and determined the nucleotide sequence of an ftsZ gene from the extremely halophilic archaebacterium Halobacterium salinarium, which grows as long, rod-shaped cells. We show that H. salinarium ftsZ is remarkably similar to the eubacterial versions, particularly in the region most similar to tubulins. An alignment of the H. salinarium FtsZ sequence with those of eubacterial FtsZ proteins and tubulins suggests that H. salinarium FtsZ is more related to tubulin than are the eubacterial FtsZs, supporting the idea that tubulin may have evolved from FtsZ. We also show that H. salinarium ftsZ is not flanked by genes normally found adjacent to several known eubacterial ftsZ genes. Finally, we show that expression...

Dominant C‐terminal deletions of FtsZ that affect its ability to localize in Caulobacter and its interaction with FtsA

“…The most widespread and highly conserved of the cell division proteins is the GTP-binding protein FtsZ. FtsZ has been identified in a large number of bacteria, in Archaea, and in Arabidopsis thaliana (Osteryoung and Vierling, 1995;Baumann and Jackson, 1996;Bult et al, 1996;Margolin et al, 1996;Wang and Lutkenhaus, 1996a,b;Lutkenhaus and Addinall, 1997). It is thought that eukaryotic organelles and prokaryotes carry out cell division in a FtsZ-dependent manner.…”

Assembly of the cell division protein FtsZ into ladder‐like structures in the aerial hyphae of Streptomyces coelicolor

“…FtsZ is a tubulin-like protein that polymerizes in a GTP-dependent manner to form a ring at the site of incipient septation (de Boer et al, 1992;RayChaudhuri and Park, 1992;Bramhill and Thompson, 1994;Mukherjee and Lutkenhaus, 1994). It plays a pivotal role in the process of cytokinesis in bacteria, and homologues of FtsZ have been found in all prokaryotes that have been investigated for its presence (Lutkenhaus, 1993;Dharmatilake and Kendrick, 1994;McCormick et al, 1994;Baumann and Jackson, 1996;Bult et al, 1996;Margolin et al, 1996;Quardokus et al, 1996;Wang and Lutkenhaus, 1996).…”

Chloroplast Division in Higher Plants Requires Members of Two Functionally Divergent Gene Families with Homology to Bacterial ftsZ

“…The ftsZ gene was originally identified in a temperature-sensitive mutant of Escherichia coli that formed bacterial filaments at the restrictive temperature due to incomplete septum formation (Lutkenhaus et al, 1980), hence the designation fts (for filamenting temperature-sensitive). FtsZ is a rate-limiting cytoskeletal component of the cell division apparatus in prokaryotes (Ward and Lutkenhaus, 1985; Baumann and Jackson, 1996;Margolin et al, 1996;Wang and Lutkenhaus, 1996), assembling at the nascent division site into a contractile ring just inside the cytoplasmic membrane (Bi and Lutkenhaus, 1991;Lutkenhaus and Addinall, 1997).…”

“…The ftsZ gene was originally identified in a temperature-sensitive mutant of Escherichia coli that formed bacterial filaments at the restrictive temperature due to incomplete septum formation (Lutkenhaus et al, 1980), hence the designation fts (for filamenting temperature-sensitive). FtsZ is a rate-limiting cytoskeletal component of the cell division apparatus in prokaryotes (Ward and Lutkenhaus, 1985; Baumann and Jackson, 1996;Margolin et al, 1996;Wang and Lutkenhaus, 1996), assembling at the nascent division site into a contractile ring just inside the cytoplasmic membrane (Bi and Lutkenhaus, 1991;Lutkenhaus and Addinall, 1997).Recent studies have revealed that FtsZ is a structural homolog and possibly the evolutionary progenitor of the eukaryotic tubulins (Erickson, 1995(Erickson, , 1998de Pereda et al, 1996;Erickson et al, 1996;Lowe and Amos, 1998), and it can undergo dynamic GTP-dependent assembly into long polymers in vitro (de Boer et al, 1992a;RayChaudhuri and Park, 1992;Mukherjee et al, 1993; Bramhill and Thompson, 1994; Lutkenhaus, 1994, 1998; Bramhill, 1997;Yu and Margolin, 1997). In a previous study (Osteryoung and Vierling, 1995), we identified an FtsZ gene ( AtFtsZ1-1 ) from Arabidopsis whose putative product exhibited between 40 and 50% amino acid identity with most of its prokaryotic counterparts.…”