Surface resistance to SSVs and SIRVs in pilin deletions of Sulfolobus islandicus

Abstract

Characterizing the molecular interactions of viruses in natural microbial populations offers insights into virus–host dynamics in complex ecosystems. We identify the resistance of Sulfolobus islandicus to Sulfolobus spindle‐shaped virus (SSV9) conferred by chromosomal deletions of pilin genes, pilA1 and pilA2 that are individually able to complement resistance. Mutants with deletions of both pilA1 and pilA2 or the prepilin peptidase, PibD, show the reduction in the number of pilins observed in TEM and reduced surface adherence but still adsorb SSV9. The proteinaceous outer S‐layer proteins, SlaA and SlaB, are not required for adsorption nor infection demonstrating that the S‐layer is not the primary receptor for SSV9 surface binding. Strains lacking both pilins are resistant to a broad panel of SSVs as well as a panel of unrelated S. islandicus rod‐shaped viruses (SIRVs). Unlike SSV9, we show that pilA1 or pilA2 is required for SIRV8 adsorption. In sequenced Sulfolobus strains from around the globe, one copy of each pilA1 and pilA2 is maintained and show codon‐level diversification, demonstrating their importance in nature. By characterizing the molecular interactions at the initiation of infection between S. islandicus and two different types of viruses we hope to increase the understanding of virus–host interactions in the archaeal domain.

The structures of two archaeal type IV pili illuminate evolutionary relationships

“…1a, b). Consequently, the filaments appear to serve as the primary receptors for SSRV1 and PFV2, as has been demonstrated for some other archaeal viruses [16][17][18] .…”

“…For instance, mass-spectrometry analysis of a crude sample typically yields too many potential candidate proteins for unequivocal identification, whereas some proteins are not amenable to standard tryptic digestion, as has been shown recently for the pili of S. islandicus 26 . Pili appear to be a common receptor for hyperthermophilic archaeal viruses and have been previously shown to be recognized by rudiviruses SIRV2 and SIRV8 16,17 , and turrivirus STIV 18 . Here we have shown that members of yet another family of archaeal viruses, the Tristromaviridae, also bind to the host cells via T4P.…”

“…Although the full spectrum of functions played by archaeal T4P is yet to be uncovered, they are known to mediate adhesion to various biotic and abiotic surfaces, and play an important role in DNA exchange, intercellular communication and biofilm formation 14,15 . Furthermore, T4P serve as receptors for certain hyperthermophilic archaeal viruses, including Sulfolobus islandicus rod-shaped viruses 2 and 8 (SIRV2 and SIRV8, respectively; family Rudiviridae) 16,17 and Sulfolobus turreted icosahedral virus (STIV; family Turriviridae) 18 .…”

Cellular and genomic properties ofHaloferax gibbonsiiLR2-5, the host of euryarchaeal virus HFTV1

“…Filamentous surface structures are well known primary anchor points for several viruses infecting bacteria (Poranen et al, 2002;Mäntynen et al, 2019). Recent data suggests that a few crenarchaeal viruses also tether to filamentous surface structures (Quemin et al, 2013;Hartman et al, 2019;Rowland et al, 2020). A hallmark of archaeal surface structures is the widespread similarity to bacterial type IV pili.…”

The network structure and eco-evolutionary dynamics of CRISPR-induced immune diversification

“…This experimental and theoretical evidence for advantages of surface modification may entail strong fitness costs under natural conditions because mutations in surface receptors such as those in flagella or pili can be detrimental for microbial movement and biofilm formation [21]. Investigations of natural populations have indeed shown that surface resistance is costly in the wild [27,28]. These observations underlie the need for complementing experimental approaches by developing theory on the kinds of 'macroscopic', whole system, diversity patterns expected under 'microscopic' CRISPR-induced coevolutionary processes.…”