Identification of Diverse Archaeal Proteins with Class III Signal Peptides Cleaved by Distinct Archaeal Prepilin Peptidases

Szabó, Zalán; Stahl, Adriana Oliveira; Albers, Sonja‐Verena; Kissinger, Jessica C.; Driessen, Arnold J. M.; Pohlschröder, Mechthild

doi:10.1128/jb.01547-06

Cited by 149 publications

(247 citation statements)

References 44 publications

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“…Sso3138, Sso3139, and Sso3140 were predicted to be primarily located extracellularly (see Fig. S1 in the supplemental material), correlating with a previous prediction of the presence of class III signal peptides at their N termini (26). Among these, Sso3140 was confirmed to be a membrane-associated protein in a proteomics study (27).…”

Section: Sirv2 Entry In Sulfolobussupporting

confidence: 55%

Unveiling Cell Surface and Type IV Secretion Proteins Responsible for Archaeal Rudivirus Entry

Deng

Bhoobalan-Chitty

et al. 2014

J Virol

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Sulfolobus mutants resistant to archaeal lytic virus Sulfolobus islandicus rod-shaped virus 2 (SIRV2) were isolated, and mutations were identified in two gene clusters, cluster sso3138 to sso3141 and cluster sso2386 and sso2387, encoding cell surface and type IV secretion proteins, respectively. The involvement of the mutations in the resistance was confirmed by genetic complementation. Blocking of virus entry into the mutants was demonstrated by the lack of early gene transcription, strongly supporting the idea of a role of the proteins in SIRV2 entry.T o date, relatively few archaeal viruses have been characterized, and most of those that have been characterized infect acidothermophilic members of the order Sulfolobales. Despite their limited number of around 50 species, they exhibit considerably greater morphological diversity than the more extensively characterized bacteriophages, about 95% of which show head-tail morphologies. Archaeal viruses, in contrast, exhibit fusiform shapes, often with one or two tails, bottle shapes, bearded-globular forms, and a wide variety of rod-like and filamentous morphotypes which often carry small terminal appendages (1-3). This morphological diversity suggests that the archaeal viruses may employ a variety of mechanisms to enter their hosts, but current insights into entry mechanisms are limited to an OppA transporter protein, Sso1273, possibly providing a receptor site for the Acidianus two-tailed virus (ATV) in Sulfolobus solfataricus P2 (4). And very recently, microscopic studies suggested that Sulfolobus islandicus rod-shaped virus 2 (SIRV2) enters the host cell by attaching and moving through a pilus-like filament; however, the nature of the structure and the identity of the involved proteins remain elusive (5).Sulfolobus solfataricus P2 is an acidothermophilic crenarchaeon that can host a wide range of archaeal viruses, many of which are propagated stably (1, 3, 6). Moreover, few of the viruses appear to induce cell lysis, possibly reflecting a need to minimize contact with the harsh hot acidic environment. However, recent studies have identified a few viruses that can enter a lytic phase, including the Sulfolobus turreted icosahedral virus (STIV), the two-tailed fusiform (ATV), and, more recently, the rudivirus SIRV2 (7-9).SIRV2 is classified in the family Rudiviridae together with other well-characterized viruses, including SIRV1 (10, 11), ARV1 (12) and SRV1, (13), all of which are rod shaped and lack an envelope, and their genomes consist of linear double-stranded DNA with covalently closed ends (10,14,15). In a recent microarray analysis of S. solfataricus infected with SIRV2, we demonstrated that the viral genes were activated at different times and that mainly stressresponse host genes and those implicated in vesicle formation were downregulated (16). The results also illustrated that SIRV2 infection at a multiplicity of infection (MOI) of 30 resulted in growth inhibition of S. solfataricus 5E6 (16). In the present experiment, the culture was infected at a lower...

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Section: Sirv2 Entry In Sulfolobussupporting

confidence: 55%

Unveiling Cell Surface and Type IV Secretion Proteins Responsible for Archaeal Rudivirus Entry

Deng

Bhoobalan-Chitty

et al. 2014

J Virol

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“…Genome sequence analysis in search of type IV pilin-like signal peptides led to the identification of a number of type IV pilin-like genes, MMP0233 (encoding a protein with a predicted molecular mass of 14.4 kDa, with the signal peptide), MMP0236 (encoding a protein with a predicted molecular mass of 14.2 kDa, with the signal peptide), and MMP0237 (encoding a protein with a predicted molecular mass of 17.3 kDa, with the signal peptide), in a single gene cluster (58). In the cases of MMP0233 and MMP0237, it was also previously demonstrated that both proteins were processed by the type IV prepilin peptidase homologue EppA found in the same gene cluster, further supporting their assignment as type IV pilins (58).…”

Section: Resultsmentioning

confidence: 99%

“…Evidence has been presented that in Haloferax volcanii, the PibD equivalent also processes flagellins and pilin-like proteins (65). However, in M. maripaludis, there is a dedicated second peptidase, EppA, for pilin processing that is separate from the flagellin-processing enzyme FlaK (58). In S. solfataricus, transcription of the pilus locus is strongly upregulated, with the number of pili on the surface of the cells greatly enhanced, upon treatment of cells with UV light (26)(27)(28).…”

mentioning

confidence: 99%

“…When M. maripaludis pili were isolated and examined by electron cryomicroscopy, they were found to have a structure unlike that of any other known bacterial pili, with two subunit packing arrangements found to coexist within the same filament (72). In silico analysis and signal peptide processing assays were used to identify a locus in M. maripaludis that contained several genes encoding proteins with predicted and, in some cases, demonstrated class III signal peptides that were suggested to be likely candidates for pilus structural proteins (58). In addition, a number of other proteins were identified from the FlaFind PERL program analysis of the genome as likely possessing class III signal peptides.…”

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confidence: 99%

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Genetic and Mass Spectrometry Analyses of the Unusual Type IV-Like Pili of the ArchaeonMethanococcus maripaludis

Nair

et al. 2011

J Bacteriol

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The structure of pili from the archaeon Methanococcus maripaludis is unlike that of any bacterial pili. However, genetic analysis of the genes involved in the formation of these pili has been lacking until this study. Pili were isolated from a nonflagellated (⌬flaK) mutant and shown by sodium dodecyl sulfate-polyacrylamide gel electrophoresis to consist primarily of subunits with an apparent molecular mass of 17 kDa. In-frame deletions were created in three genes, MMP0233, MMP0236, and MMP0237, which encode proteins with bacterial type IV pilin-like signal peptides previously identified by in silico methodology as likely candidates for pilus structural proteins. Deletion of MMP0236 or MMP0237 resulted in mutant cells completely devoid of pili on the cell surface, while deletion of the third pilin-like gene, MMP0233, resulted in cells greatly reduced in the number of pili on the surface. Complementation with the deleted gene in each case returned the cells to a piliated state. Surprisingly, mass spectrometry analysis of purified pili identified the major structural pilin as another type IV pilin-like protein, MMP1685, whose gene is located outside the first pilus locus. This protein was found to be glycosylated with an N-linked branched pentasaccharide glycan. Deletion and complementation analysis confirmed that MMP1685 is required for piliation.

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“…1), denoted "type III" (379) to distinguish it from the type I (recognized by signal peptidase I) and type II (characteristic of lipoproteins) signal sequences. Canonical type I and type II signal sequences are cleaved at the exterior of the cytoplasmic membrane, C-terminal to a stretch of hydrophobic residues.…”

Section: The Signature Type III Signal Sequencementioning

confidence: 99%

Type IV Pilin Proteins: Versatile Molecular Modules

Giltner

Nguyen

Burrows

2012

Microbiol Mol Biol Rev

410

519

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SUMMARYType IV pili (T4P) are multifunctional protein fibers produced on the surfaces of a wide variety of bacteria and archaea. The major subunit of T4P is the type IV pilin, and structurally related proteins are found as components of the type II secretion (T2S) system, where they are called pseudopilins; of DNA uptake/competence systems in both Gram-negative and Gram-positive species; and of flagella, pili, and sugar-binding systems in the archaea. This broad distribution of a single protein family implies both a common evolutionary origin and a highly adaptable functional plan. The type IV pilin is a remarkably versatile architectural module that has been adopted widely for a variety of functions, including motility, attachment to chemically diverse surfaces, electrical conductance, acquisition of DNA, and secretion of a broad range of structurally distinct protein substrates. In this review, we consider recent advances in this research area, from structural revelations to insights into diversity, posttranslational modifications, regulation, and function.

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Identification of Diverse Archaeal Proteins with Class III Signal Peptides Cleaved by Distinct Archaeal Prepilin Peptidases

Cited by 149 publications

References 44 publications

Unveiling Cell Surface and Type IV Secretion Proteins Responsible for Archaeal Rudivirus Entry

Unveiling Cell Surface and Type IV Secretion Proteins Responsible for Archaeal Rudivirus Entry

Genetic and Mass Spectrometry Analyses of the Unusual Type IV-Like Pili of the ArchaeonMethanococcus maripaludis

Type IV Pilin Proteins: Versatile Molecular Modules

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