Microorganisms of the third domain of life, Archaea, are important to
biotechnology and the environment, yet relatively little is known of their
physiology and cell biology. Archaea have a prokaryotic cell structure, but are
genetically more related to eukaryotes than bacteria. Our work has focused on
the tubulin super-family of proteins that constitute the cytoskeleton in
eukaryotic cells, and the cell division apparatus in bacteria. Interestingly, whereas
bacterial cells contain a single tubulin-family member called FtsZ, many
archaea encode multiple homologs. We show here that two
of the eight homologs present in the model archaeon Haloferax volcanii are essential for normal cell division. Remarkably,
however, deletion and double-deletion strains can be maintained indefinitely,
despite the apparent complete absence of a cytokinetic mechanism and the
development of very large misshapen cells. By developing GFP-tagging approaches
for this species, combined with super-resolution and time-lapse video-microscopy,
we revealed a dynamic pattern of cell division in which planes of cell division
are established orthogonally in successive cell cycles.
The remaining
six tubulin-family homologs in H.
volcanii were not required for cell division. They are members of a
distinct uncharacterized family that show greater similarity to eukaryotic
tubulins. We discovered that one of these proteins, named
CetZ, controls the development of H.
volcanii cells from a pleomorphic cell type to a elongated rod-shaped form
required for cell motility. Such a role in dynamic
control of cell shape is reminiscent of tubulin’s role in regulating eukaryotic cell
structure and has not been observed previously in prokaryotes to our knowledge.
This new function and our crystal structures of CetZ proteins in single
and proto-filament form suggest that the CetZ protein family represents a missing
link in the evolutionary history of the eukaryotic tubulins and bacterial FtsZs.