Archaeal bundling pili of Pyrobaculum calidifontis reveal similarities between archaeal and bacterial biofilms

Abstract

While biofilms formed by bacteria have received great attention due to their importance in pathogenesis, much less research has been focused on the biofilms formed by archaea. It has been known that extracellular filaments in archaea, such as type IV pili, hami, and cannulae, play a part in the formation of archaeal biofilms. We have used cryo-electron microscopy to determine the atomic structure of a previously uncharacterized class of archaeal surface filaments from hyperthermophilic Pyrobaculum calidifontis. These filaments, which we call archaeal bundling pili (ABP), assemble into highly ordered bipolar bundles. The bipolar nature of these bundles most likely arises from the association of filaments from at least two different cells. The component protein, AbpA, shows homology, both at the sequence and structural level, to the bacterial protein TasA, a major component of the extracellular matrix in bacterial biofilms, contributing to biofilm stability. We show that AbpA forms very stable filaments in a manner similar to the donor-strand exchange of bacterial TasA fibers and chaperone-usher pathway pili where a β-strand from one subunit is incorporated into a β-sheet of the next subunit. Our results reveal likely mechanistic similarities and evolutionary connection between bacterial and archaeal biofilms, and suggest that there could be many other archaeal surface filaments that are as yet uncharacterized.

Donor-strand exchange drives assembly of the TasA scaffold in Bacillus subtilis biofilms

“…Further studies into the TasA/TapA system will be needed to understand in detail the mechanisms of assembly of TasA fibres compared to Gram-negative pili, which employ Chaperone-Usher systems or proteolytic cleavage for assembly 30 , 31 . Interestingly, very recent studies have demonstrated that fibres in extremophile archaea also are donor-strand-complemented 38 , 39 , with some archaeal systems even structurally related to TasA 39 , which suggests that donor-strand assembly is a ubiquitous strategy for the assembly of highly stable fibres.…”

“…Nevertheless, our experiments show the importance of a loop (containing residues 174–177) extending away from the fibre surface in mediating these interactions. Interestingly, in a recent study on a TasA-like system (archaeal bundling pili (ABP)) in hyperthermophilic archaea 39 , fibres formed ordered, six-fibre bundles. We detected bundles of variable sizes for TasA, which also appear more flexible.…”

TapA acts as specific chaperone in TasA filament formation by strand complementation

“…ThT-stainable fibrils were investigated by solid-state NMR ( 10 ), and in parallel to this study nonamyloid filaments by cryo-EM ( 18 ) were studied at a resolution of 3.5 Å. Furthermore, a structural relationship between archaeal and bacterial biofilms was suggested on the basis of a 4.0 Å cryo-EM structure of Pyrobaculum calidifontis bundling pili ( 19 ).…”

Archaeal DNA-import apparatus is homologous to bacterial conjugation machinery

“…We have previously shown that Pyrobaculum calidifontis , a hyperthermophilic archaeon of the order Thermoproteales 40 , which lacks both Ced and Ups systems, is prone to aggregation mediated by bundling pili related to TasA-like fibers, a major component of the biofilm matrix in many bacteria 41 . We thus explored whether P. calidifontis cells produce pili which could be involved in DNA transfer.…”