University of Groningen Signal Peptides of Secreted

CORE Metadata, citation and similar papers at core.ac.uk Provided by University of Groningen University of Groningen Signal peptides of secreted proteins of the archaeon Sulfolobus solfataricus: a genomic survey Albers, S.V.; Driessen, A.J.M. Published in: Archives of Microbiology DOI: 10.1007/s00203-001-0386-y IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2002 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Albers, S. V., & Driessen, A. J. M. (2002). Signal peptides of secreted proteins of the archaeon Sulfolobus solfataricus: a genomic survey: a genomic survey. Archives of Microbiology, 177(3), 209 - 216. https://doi.org/10.1007/s00203-001-0386-y Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 12-11-2019 Arch Microbiol (2002) 177:209–216 DOI 10.1007/s00203-001-0386-y MINI-REVIEW Sonja-Verena Albers · Arnold J. M. Driessen Signal peptides of secreted proteins of the archaeon Sulfolobus solfataricus: a genomic survey Received: 21 August 2001 / Revised: 31 October 2001 / Accepted: 15 November 2001 / Published online: 11 January 2002 © Springer-Verlag 2002 Abstract Analysis of the recently completed genome se- ratus of S. solfataricus. Here, we briefly discuss bacterial quence of the thermoacidophilic archaeon Sulfolobus sol- and eukaryal secretion mechanisms and substrates and use fataricus reveals that about 4.2% of its proteome consists this information to classify the identified and putative se- of putative secretory proteins with signal peptides. This creted proteins of S. solfataricus that are present in its includes members of the four major classes of signal pep- proteome. tides: secretory signal peptides, twin-arginine signal pep- In gram-negative bacteria, the general secretion system tides, possible lipoprotein precursors, and type IV pilin directs proteins to the periplasmic space and the outer signal peptides. The latter group is surprisingly large membrane (Pugsley 1993). Various other secretion mech- compared to the size of the groups in other organisms and anisms are involved in the delivery of macromolecules to seems to be used predominately for a subset of extracellu- the extracellular medium, a process that involves a trans- lar substrate-binding proteins. location step across the outer membrane. These systems are classified in four groups (Nunn 1999). Type I secre- Keywords Sulfolobus solfataricus · Archaea · Signal tion systems consists of three proteins including an peptide · Secretion · Type IV pilin signal peptide · ATPase that belongs to the ABC-type of transporters. This Sugar-binding protein system mediates the translocation of proteins across the inner and outer membrane without the accumulation of a periplasmic intermediate. The type II secretion system is Introduction formed by over 12 subunits that reside in the inner and outer membrane. This system handles the translocation of Sulfolobus solfataricus is an obligate aerobic archaeon periplasmic substrate intermediates prior to their translo- that grows either litoautotrophically or chemoheterotro- cation across the outer membrane (Sandkvist 2001). Type phically in hot (about 80°C) and acidic (pH 2–4) environ- III secretion systems are involved in eukaryotic host inva- ments. S. solfataricus P2 originates from a solfataric field sion mechanisms and are complicated structures with up near Naples, Italy (Zillig et al. 1980), and its genome se- to 30 subunits. These systems include an injection device quence has recently been determined (She et al. 2001). As that delivers macromolecules directly from the bacterial a model organism for the domain of crenarchaeotes, its cytoplasm into the host cells (Tamano et al. 2000). Type mechanisms of cell cycle, DNA replication, chromosomal IV secretion systems are involved in various processes integration, transcription and translation have been stud- such as single-stranded DNA transport into host cells (the ied extensively. Furthermore its membrane-spanning tetra- Vir system of Agrobacterium tumefaciens), toxin secre- ether lipids, metabolic routes and sugar degradation path- tion and pilin biogenesis (Christie 2001). Some of the ways are unique (Schönheit et al. 1995). Only limited data components of the type IV secretion machinery, in partic- are available on the secreted proteins and secretory appa- ular the subunits of the macromolecule-conducting pore in the outer membrane, exhibit striking similarities with type II secretion systems. Also subunits of the type IV pilin biogenesis apparatus that are involved in twitching S.-V. Albers · A.J.M. Driessen (✉) motility share homology with components of the type II Department of Microbiology, secretome (Wall et al. 1999). Secretion of proteins across Groningen Biomolecular Sciences and Biotechnology Institute, the S-layer of archaea has barely been addressed experi- University of Groningen, Kerklaan 30, 9751 NN Haren, The Netherlands mentally. Although the S-layer contains pores with a di- e-mail: [email protected], ameter of 4–5 nm, it is not known if these structures con- Tel.: +31-5036-32164, Fax: +31-5036-32154 duct protein movements in an active or passive sense. In- 210 terestingly, archaea contain homologues of PilT, the mo- tor protein of the type IV pilin biogenesis apparatus, and of the VirB proteins involved in type IV secretion. Structure and function of signal peptides Proteins translocated across the cytoplasmic membrane of bacteria, the thylakoid membrane in plant chloroplasts, and the endoplasmic reticulum (ER) membrane of eukaryotes are all synthesized as precursors with an amino-terminal signal peptide. These signal peptides are functionally ex- changeable between the different organisms (von Heijne 1990), and although their amino acid composition show lit- tle similarity, three different domains can be distinguished (von Heijne 1990) (Pugsley 1993). The N-domain contains basic amino acid residues. In bacteria, the net positive charge of this domain is thought to orient the N-terminus in the cytoplasm according to the ∆ψ, which in most organisms is inside negative (Andersson et al. 1994). The N-domain also interacts electrostatically with negatively charged phospholipids in the lipid bilayer during translocation (de Vrije et al. 1990) and with the translocation ATPase SecA. The H-domain is a stretch of about 10–15 hydrophobic residues that tends to fold into α-helical conformation in the membrane. A glycine or proline residue is often found in the middle of the H-domain and has been proposed to promote the insertion of the signal peptide into the membrane by forming a hairpin-like structure. Unlooping of this hairpin may result in the insertion of the complete signal peptide (de Vrije et al. 1990). The H-domain is followed by the short polar C-domain, which contains the recognition Fig.1 The different classes of signal peptides found in Sulfolobus solfataricus. The length of the domains N, H and C is given and site for the signal peptidase. Recent studies have shown the arrow indicates the cleavage site. + Positive charges, black box that the composition of the C-domain determines the accu- hydrophobic residues racy of cleavage by type I signal peptidases (SPase), and not the length or even the presence of the H-domain (Car- los et al. 2000). After proteolytic cleavage by a signal pep- Class 4 signal peptides constitute a heterogeneous group tidase, the mature protein is released from the membrane of signal peptides such as the signals that direct the secre- for further folding and assembly. The signal peptide is de- tion of small antimicrobial peptides via ABC transporters. graded by signal peptide peptidases. Amino-terminal bacterial signal peptides can be di- vided into at least four different classes dependent on the Distribution of signal peptide classes signal peptidase recognition site (Fig.1). Class 1 consists in Sulfolobus solfataricus of the typical signal peptides, which are mostly cleaved by the type I signal peptidases (SPases) (Tjalsma et al. This section describes the results of an analysis of the 2000). A subclass of these signal peptides contains a “twin- S. solfataricus genome which was screened for the distribu- arginine” motif, which directs these proteins to a different tion of the various classes of signal peptides. To identify translocation pathway, the Tat pathway (Berks et al. and classify putative secreted proteins, the complete 2000). This pathway is mostly involved in the transloca- genome database (http://www-archbac.u-psud.fr/projects/ tion of folded redox proteins with bound co-factor. Class sulfolobus/) was analyzed by a neural network-based method 2 signal peptides exhibit a typical domain with an invari- and a hidden Markov model (http://www.cbs.dtu.dk/services/ ant cysteine that is lipid-modified prior to the cleavage by SignalP/) trained on both eukaryotic and gram-positive type II SPases. The resulting lipoprotein remains an- and gram-negative bacterial signal peptide datasets. Poly- chored to the cytoplasmic membrane after cleavage. Class topic membrane proteins were excluded from the analysis, 3 signal peptides include the type IV pilin-like peptides. but membrane proteins containing only one amino-termi- Prepilins are cleaved between the N- and the H-domain, nal transmembrane segment may be falsely predicted as leaving the H-domain attached to the mature pilin.

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