The evolution of the cytoskeleton

Abstract

The cytoskeleton is a system of intracellular filaments crucial for cell shape, division, and function in all three domains of life. The simple cytoskeletons of prokaryotes show surprising plasticity in composition, with none of the core filament-forming proteins conserved in all lineages. In contrast, eukaryotic cytoskeletal function has been hugely elaborated by the addition of accessory proteins and extensive gene duplication and specialization. Much of this complexity evolved before the last common ancestor of eukaryotes. The distribution of cytoskeletal filaments puts constraints on the likely prokaryotic line that made this leap of eukaryogenesis.

Figure 1.

Homology between prokaryotic and eukaryotic cytoskeletal filaments. Despite low levels of sequence similarity, the homologous cytoskeletal proteins FtsZ/TubZ/tubulin (top) and MreB/ParM/actin (bottom) have considerable conservation of folding and also longitudinal interaction. ParM and actin form similar helical filaments, but with opposite chirality (Orlova et al., 2007). Structures of filament subunits are derived from the following Protein Data Bank accession numbers: 1W5A (FtsZ; Oliva et al., 2004), 1JFF (α/β-tubulin; Löwe et al., 2001), 1JCG (MreB; van den Ent et al., 2001), and 1YAG (actin; Vorobiev et al., 2003).

Figure 2.

Bacterial, archaeal, and eukaryotic cytoskeletons. Schematic representations are shown for a small number of model organisms from each of the three domains of life (A–C), showing the organization of the cytoskeleton in dividing and nondividing cells (right and left of each pair, respectively). Homologous filaments are colored similarly. Also shown is the possible organization of the cytoskeleton in the LECA (D), highlighting the ancestral families of microtubule motors.

Figure 3.

The distribution of key components of the cytoskeleton across the tree of life. Filled circle indicates presence of an identifiable member of a protein family in an organism; open circle indicates absence/not found. Organisms are identified by genera only and are grouped into higher taxonomic groups. Emiliania huxleyi has not been placed into one of the eukaryotic taxonomic groups in reflection of uncertainty as to the placement of Haptophyta. “MreB” includes MreB-like (Mbl/MreBH) sequences, which colocalize with MreB and are very similar in sequence (Carballido-López and Errington, 2003; Carballido-López et al., 2006). The archaeal sequences identified as MreB using the arCOG technique (arCOG04656; Makarova et al., 2007, 2010) have a closer affinity to Hsp70 sequences and are not included. Archaeal crenactin (*) is orthologous to the single common ancestor of eukaryotic actin and ARPs (Yutin et al., 2009; Ettema et al., 2011), but has been entered as actin for clarity. The distributions of the large number of prokaryotic actin-like proteins other than MreB and FtsA (such as AlfA, Alp6/7/8) are not included here because of current difficulties in resolution of individual families (Derman et al., 2009; Yutin et al., 2009). There are possible orthologues of MinD in Euryarchaeota (Leipe et al., 2002), but their true membership is still unclear.