An archaeal origin for the actin cytoskeleton: Implications for eukaryogenesis

Abstract

A hallmark of the eukaryotic cell is the actin cytoskeleton, involved in a wide array of processes ranging from shape determination and phagocytosis to intracellular transport and cytokinesis. Recently, we reported the discovery of an actin-based cytoskeleton also in Archaea. The archaeal actin ortholog, Crenactin, was shown to belong to a conserved operon, Arcade (actin-related cytoskeleton in Archaea involved in shape determination), encoding an additional set of cytoskeleton-associated proteins. Here, we elaborate on the implications of these findings for the evolutionary relation between archaea and eukaryotes, with particular focus on the possibility that eukaryotic actin and actin-related proteins have evolved from an ancestral archaeal actin gene. Archaeal actin could thus have played an important role in cellular processes essential for the origin and early evolution of the eukaryotic lineage. Further exploration of uncharacterized archaeal lineages is necessary to find additional missing pieces in the evolutionary trajectory that ultimately gave rise to present-day organisms.

Figure 1.

An archaeal actin ortholog. Schematic overview of actin protein family phylogeny, demonstrating strong support (bootstrap value 97) for common ancestry of archaeal Crenactin and eukaryotic actin proteins. The tree was generated as described previously, except that distant members (MreB and Hsp70) of the actin protein family were omitted and novel archaeal sequences were added (Crenactin orthologs from ‘Ca. Caldiarchaeum subterraneum’, Vulcanisaeta distributa, Vulcanisaeta moutnovskia and Thermoproteus uzoniensis). For clarity, the actin, ParM/ALPs and MamK clades are displayed as triangles (for full details of included sequences, see³). The gray shading highlights the Crenactin clade and, for each species, the gene organization of the arcade gene cluster is indicated, with the genes encoding Arcadin-1 (rkd-1), Crenactin (cren-1), Arcadin-2 (rkd-2), Arcadin-3 (rkd-3) and Arcadin-4 (rkd-4) depicted in orange, blue, green, magenta and orange, respectively. The tree was rooted according to the topology obtained previously, with bootstrap values shown for branches with a support above 70 (out of 100 replicates). Sequences are denoted by species name and gene identifier, with crenarchaeal, korarchaeal and aigarchaeal Crenactin orthologs indicated in green, red and blue fonts, respectively. Note that the Crenactin ortholog of the aigarchaeon ‘Ca. Caldiarchaeum subterraneum’ represents the deepest branch in the Crenactin tree, although with low support.

Figure 2.

Eukaryotic signature genes in archaeal phyla. Schematic overview of established, as well as inferred, archaeal phyla, with Crenarchaeota, Thaumarchaeota, Korarchaeota and the recently proposed Aigarchaeota forming a monophyletic group putatively including eukaryotes (red font), with the bacterial root depicted as an arrow. Comparative analysis of archaeal genomes has revealed the presence of eukaryotic signature proteins within these phyla, as indicated by the shading pattern: red, actin; blue, ubiquitin-type protein modifier system; yellow, Cdv (ESCRT-III-like) cell division machinery; purple, eukaryotic RNA polymerase-subunit RPB8 (RpoG); orange, eukaryotic RNA polymerase III subunit RPC34; green, eukaryotic transcription elongation factor Elf1; turquoise, eukaryotic-type topoisomerase 1B. Open (white) circles indicate absence of a given ortholog. Note that actin and Cdv proteins are present in a subset of crenarchaeal genomes, displaying an anti-correlated phylogenetic distribution, as indicated by the partly shaded circles.