Archaeal cell surface biogenesis

Abstract

Cell surfaces are critical for diverse functions across all domains of life, from cell-cell communication and nutrient uptake to cell stability and surface attachment. While certain aspects of the mechanisms supporting the biosynthesis of the archaeal cell surface are unique, likely due to important differences in cell surface compositions between domains, others are shared with bacteria or eukaryotes or both. Based on recent studies completed on a phylogenetically diverse array of archaea, from a wide variety of habitats, here we discuss advances in the characterization of mechanisms underpinning archaeal cell surface biogenesis. These include those facilitating co- and post-translational protein targeting to the cell surface, transport into and across the archaeal lipid membrane, and protein anchoring strategies. We also discuss, in some detail, the assembly of specific cell surface structures, such as the archaeal S-layer and the type IV pili. We will highlight the importance of post-translational protein modifications, such as lipid attachment and glycosylation, in the biosynthesis as well as the regulation of the functions of these cell surface structures and present the differences and similarities in the biogenesis of type IV pili across prokaryotic domains.

Architecture and modular assembly ofSulfolobusS-layers revealed by electron cryo-tomography

“…Moreover, this protein is not membrane-integral but instead inserted to the bilayer via a C-terminal 339 lipid anchor (Fig. 7) (Pohlschroder, Pfeiffer, Schulze, & Halim, 2018). While employing only one 340 S-layer protein might be energetically more favorable, it is likely that using two increases the 341 adaptability of the S-layer surface (SlaA) without compromising the membrane anchor (SlaB).…”

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

“…First, even though there are examples of bacterial species with S-layer that carry out peptidoglycan cellwall synthesis at mid cell (6), their new S-layer material is inserted as patches distributed all around the cell (35,36). Second, lack of conservation in the protein architecture between archaeal and bacterial S-layers argue that they may have emerged independently of each other (8,37).…”

“…In both bacteria and eukaryotes, a multitude of growth modes have been characterized, with cells inserting new envelope material almost all along the cell surface (2), bipolarly (3), unipolarly (4), and in some cases, different modes can be interchangeable (5,6). In the case of archaea, which lack a peptidoglycan cell wall, glycosylated S-layer and other proteins are commonly the sole component of the cell envelope (7,8), where they typically show a 2D crystal-like arrangement. This poses an interesting problem for archaeal surface protein organization, and currently there is no data about the mechanisms of archaeal cell elongation control (9).…”

“…While many proteins are anchored to the cell surface via transmembrane (TM) domain insertion into the membrane, some are anchored through covalent N-terminal attachment of a lipid moiety (8). Recently, a novel mechanism was discovered whereby proteins are anchored to the mem-brane through a lipid moiety covalently attached to a processed C-terminus.…”

ArlCDE form the archaeal switch complex

“…Although they are functionally similar, there is no structural similarity between the filaments from Bacteria and Archaea (Berg and Anderson, 1973;Alam and Oesterhelt, 1984;Chevance and Hughes, 2008;Jarrell and Albers, 2012;Albers and Jarrell, 2018;Beeby et al, 2020). The archaeal motility structure, the archaellum, has homology to bacterial type IV pili, and it consist of ~10 Arl proteins (previously named Fla proteins) (Kalmokoff and Jarrell, 1991;Jarrell and Albers, 2012;Pohlschroder et al, 2018). The energy required for rotation is derived from ATP hydrolysis (Thomas et al, 2002;Streif et al, 2008;Reindl et al, 2013), and new protein subunits are N-terminally processed and added at the base of the growing filament (Kalmokoff and Jarrell, 1991;Bardy and Jarrell, 2003;Szabo et al, 2006).…”