The Archaeal Cell Cycle

Abstract

Since first identified as a separate domain of life in the 1970s, it has become clear that archaea differ profoundly from both eukaryotes and bacteria. In this review, we look across the archaeal domain and discuss the diverse mechanisms by which archaea control cell cycle progression, DNA replication, and cell division. While the molecular and cellular processes archaea use to govern these critical cell biological processes often differ markedly from those described in bacteria and eukaryotes, there are also striking similarities that highlight both unique and common principles of cell cycle control across the different domains of life. Since much of the eukaryotic cell cycle machinery has its origins in archaea, exploration of the mechanisms of archaeal cell division also promises to illuminate the evolution of the eukaryotic cell cycle.

Keywords: archaea; cell cycle; cell division; eukaryogenesis.

Figure 1. The evolutional diversity of archaea.

(a) A schematic tree of life showing the major phyla of archaea. The symbiotic relationship between an Asgard archaeon and an alphaproteobacterium has been suggested to have given rise to LECA. (b) Representative species from each phylum: Lokiarchaeum ossiferum, Sulfolobus acidocaldarius, Methanobrevibacter smithii, Haloferax mediterranei, and Nanoarchaeum equitans. (c) The distribution of key cell division machinery and cell cycle regulators, showing homologs present in most of the species in the corresponding group (filled circles), homologs present in specific subbranches (half-filled circles), and homologs absent in the majority of the group (empty circles). An asterisk indicates tubulin homologs that were detected in Candidatus Nitrosoarchaeum limnia and Candidatus Nitrosopumilus koreensis (Thaumarchaeota) (Yutin & Koonin 2012). The double dagger indicates that eukaryotic FtsZs are found mostly in mitochondria and chloroplasts (Osteryoung & Nunnari 2003). Abbreviations: CM, cytoplasmic membrane; Iho, Ignicoccus hospitalis; LECA, last common ancestor of eukaryotes; LUCA, last universal common ancestor; mid., midbody; Neq, N. equitans; OM, outer membrane; PP, periplasm; SL, S-layer. Images in panel b reproduced with permission from Rodrigues-Oliveira et al. (2023) (L. ossiferum), Charles-Orszag et al. (2021) (S. acidocaldarius), Ruaud et al. (2020) (M. smithii), Chen et al. (2019) (H. mediterranei) (CC BY 4.0), and Burghardt et al. (2009) (I. hospitalis and N. equitans).

Figure 2

Overview of the cell cycle in representative archaeal, bacterial, and eukaryotic cells. In bacteria, cell division is mediated by the FtsZ ring (orange) in the D phase of its life cycle following DNA replication and segregation in the C phase. TACK archaea such as Sulfolobus acidocaldarius have defined cell cycle phases similar to those of eukaryotes. Stepwise assembly and disassembly of ESCRT-III polymers CdvB (purple), CdvB1 (green), and CdvB2 (yellow) through proteasome- and Vps4-mediated mechanisms remodel the Sulfolobus membrane during cell division (Tarrason Risa et al. 2020). Cyclin-dependent kinases regulate the eukaryotic cell cycle. In animal cells, the degradation of cyclin B triggers anaphase and the separation of sister chromatids (dark blue) by microtubules (red). The division plane is then assembled across the central part of the spindle, and cytokinesis is induced via the contraction of the actomyosin ring (turquoise) to generate two daughter cells.

Figure 3. Summary of the different means of cell division in representative bacteria, eukaryotes, and archaea.

(a) In bacteria, local remodeling and de novo synthesis of the peptidoglycan cell wall together with membrane deformation by the FtsZ ring drive cell division. (b) Eukaryotes utilize an actomyosin contractile ring to power cleavage furrow formation, followed by local membrane remodeling by the ESCRT-III machinery to complete cytokinesis. (c) (Top) In archaea such as Haloferax volcanii, FtsZ-mediated division utilizes two homologs of FtsZ together with a membrane anchor, SepF. Localization of the cell shape–regulating machinery CetZ and other membrane envelope and S-layer synthesis machinery suggest a link between cell shape determination and division in these organisms. (Bottom) In Sulfolobus acidocaldarius, cell division is accomplished by the stepwise assembly and disassembly of the ESCRT-III homologs CdvB, CdvB1, and CdvB2, together with an archaeal-specific CdvA protein that forms a template ring at the site of division. Abbreviation: S-layer, surface layer.