Multidimensional View of the Bacterial Cytoskeleton

Abstract

bThe perspective of the cytoskeleton as a feature unique to eukaryotic organisms was overturned when homologs of the eukaryotic cytoskeletal elements were identified in prokaryotes and implicated in major cell functions, including growth, morphogenesis, cell division, DNA partitioning, and cell motility. FtsZ and MreB were the first identified homologs of tubulin and actin, respectively, followed by the discovery of crescentin as an intermediate filament-like protein. In addition, new elements were identified which have no apparent eukaryotic counterparts, such as the deviant Walker A-type ATPases, bactofilins, and several novel elements recently identified in streptomycetes, highlighting the unsuspected complexity of cytostructural components in bacteria. In vivo multidimensional fluorescence microscopy has demonstrated the dynamics of the bacterial intracellular world, and yet we are only starting to understand the role of cytoskeletal elements. Elucidating structure-function relationships remains challenging, because core cytoskeletal protein motifs show remarkable plasticity, with one element often performing various functions and one function being performed by several types of elements. Structural imaging techniques, such as cryo-electron tomography in combination with advanced light microscopy, are providing the missing links and enabling scientists to answer many outstanding questions regarding prokaryotic cellular architecture. Here we review the recent advances made toward understanding the different roles of cytoskeletal proteins in bacteria, with particular emphasis on modern imaging approaches.

Taxonomy, Physiology, and Natural Products of Actinobacteria

“…Streptomycetes probably have a much more elaborate cytoskeleton than most other bacteria, which may be explained by their hyphal rather than planktonic growth (319). Besides the tubulin homolog FtsZ and the actin-like proteins MreB and Mbl (320,321), a large number of proteins with coiled-coil structural elements occur in these bacteria, and evidence is accumulating regarding their important role in growth, cell shape, and morphogenesis (319,(322)(323)(324).…”

“…Besides the tubulin homolog FtsZ and the actin-like proteins MreB and Mbl (320,321), a large number of proteins with coiled-coil structural elements occur in these bacteria, and evidence is accumulating regarding their important role in growth, cell shape, and morphogenesis (319,(322)(323)(324). The protein FilP forms intermediate filament-like structures that contribute to mechanical stress resistance (322).…”

The Dispersed Archaeal Eukaryome and the Complex Archaeal Ancestor of Eukaryotes

“…The cytoskeleton looms large in the discussion of the origin of eukaryotes, primarily because actin filaments play the central role in phagocytosis, the process that is thought to be critical for the engulfment of the proto-mitochondrial endosymbiont by its elusive future host (Cavalier-Smith 2009). For years, Bacteria and Archaea have been thought to encode only distant homologs of actin and tubulin, the proteins of the MreB/FtsA and FtsZ families, respectively, that perform essential functions in the septation of bacterial and some archaeal cells (Cabeen and Jacobs-Wagner 2010;Celler et al 2013). However, analysis of the expanding archaeal genome collection overturned this perspective.…”

The Cellular Chassis as the Basis for New Functionalities: Shortcomings and Requirements

“…In the same way, several scaffolds are used to produce the overall shape of the bacteria, which can be spherical, elongated, helicoïdal, branched, etc. (Celler et al 2013). Remarkably, there may be a link between shape and distribution of specific genes in the genome (Tamames et al 2001).…”