Positioning of the Motility Machinery in Halophilic Archaea

Abstract

Bacteria and archaea exhibit tactical behavior and can move up and down chemical gradients. This tactical behavior relies on a motility structure, which is guided by a chemosensory system. Environmental signals are sensed by membrane-inserted chemosensory receptors that are organized in large ordered arrays. While the cellular positioning of the chemotaxis machinery and that of the flagellum have been studied in detail in bacteria, we have little knowledge about the localization of such macromolecular assemblies in archaea. Although the archaeal motility structure, the archaellum, is fundamentally different from the flagellum, archaea have received the chemosensory machinery from bacteria and have connected this system with the archaellum. Here, we applied a combination of time-lapse imaging and fluorescence and electron microscopy using the model euryarchaeon Haloferax volcanii and found that archaella were specifically present at the cell poles of actively dividing rod-shaped cells. The chemosensory arrays also had a polar preference, but in addition, several smaller arrays moved freely in the lateral membranes. In the stationary phase, rod-shaped cells became round and chemosensory arrays were disassembled. The positioning of archaella and that of chemosensory arrays are not interdependent and likely require an independent form of positioning machinery. This work showed that, in the rod-shaped haloarchaeal cells, the positioning of the archaellum and of the chemosensory arrays is regulated in time and in space. These insights into the cellular organization of H. volcanii suggest the presence of an active mechanism responsible for the positioning of macromolecular protein complexes in archaea. IMPORTANCE Archaea are ubiquitous single cellular microorganisms that play important ecological roles in nature. The intracellular organization of archaeal cells is among the unresolved mysteries of archaeal biology. With this work, we show that cells of haloarchaea are polarized. The cellular positioning of proteins involved in chemotaxis and motility is spatially and temporally organized in these cells. This suggests the presence of a specific mechanism responsible for the positioning of macromolecular protein complexes in archaea.

Live cell imaging of the hyperthermophilic archaeonSulfolobus acidocaldariusidentifies complementary roles for two ESCRTIII homologues in ensuring a robust and symmetric cell division

“…Live imaging is essential for the understanding of complex dynamic cellular events, such as changes in cell shape, cell division and DNA segregation. Despite such methods being well-established in bacteria and eukaryotes, live imaging has only recently been applied to the study of cell biological processes in archaea [1], where imaging of halophilic archaea has led to surprising new findings [2][3][4][5]. Live imaging of archaea remains challenging, especially when compared to bacteria, because archaea tend to be mechanically soft and several representatives are extremophiles, necessitating the development of novel techniques [1,2].…”

Lipid Anchoring of Archaeosortase Substrates and Mid-Cell Growth in Haloarchaea

“…This evidence is even more striking for coccoid bacteria, for which a single point mutation in FtsZ is able to induce cell elongation in Staphylococcus aureus (31). However, haloarchaea might have conserved at least two distinct elongation modes in addition to cell division, generating disk-like and rod-like populations (32). This scenario would also corroborate the morphological malleability of haloarchaea, being capable of assuming unusual shapes like triangles and squares (33,34).…”

An oscillating MinD protein determines the cellular positioning of the motility machinery in archaea

“…To assess if ParA/MinD homologs in archaea play a role in cellular positioning, we selected the model archaeon Haloferax volcanii, which has genetic tools and fluorescent fusion proteins available to address questions relating to intracellular organization. Recent work in H. volcanii has indicated that positioning of the motility structure, chemosensory arrays and cell division machinery is regulated by unknown mechanisms [43][44][45] . H. volcanii cells display different shapes dependent on the growth stage of the culture 43,44,46 .…”

“…Recent work in H. volcanii has indicated that positioning of the motility structure, chemosensory arrays and cell division machinery is regulated by unknown mechanisms [43][44][45] . H. volcanii cells display different shapes dependent on the growth stage of the culture 43,44,46 . Cells in early log-phase are rod-shaped and motile.…”

“…Cells in early log-phase are rod-shaped and motile. They possess chemosensory arrays at the cell membrane, and filamentous motility structures, archaella, at their surface 44 . In late stationary phase, cells have a more discoid, pleomorphic appearance.…”