Mutational and Bioinformatic Analysis of Haloarchaeal Lipobox-Containing Proteins
Identifieur interne : 000177 ( Pmc/Curation ); précédent : 000176; suivant : 000178Mutational and Bioinformatic Analysis of Haloarchaeal Lipobox-Containing Proteins
Auteurs : Stefanie Storf [États-Unis] ; Friedhelm Pfeiffer [Allemagne] ; Kieran Dilks [États-Unis] ; Zhong Qiang Chen ; Saheed Imam [États-Unis] ; Mechthild Pohlschröder [États-Unis]Source :
- Archaea [ 1472-3646 ] ; 2010.
Abstract
A conserved lipid-modified cysteine found in a protein motif commonly referred to as a lipobox mediates the membrane anchoring of a subset of proteins transported across the bacterial cytoplasmic membrane via the Sec pathway. Sequenced haloarchaeal genomes encode many putative lipoproteins and recent studies have confirmed the importance of the conserved lipobox cysteine for signal peptide processing of three lipobox-containing proteins in the model archaeon
Url:
DOI: 10.1155/2010/410975
PubMed: 20886060
PubMed Central: 2945643
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Mutational and Bioinformatic Analysis of Haloarchaeal Lipobox-Containing Proteins</title>
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<author><name sortKey="Dilks, Kieran" sort="Dilks, Kieran" uniqKey="Dilks K" first="Kieran" last="Dilks">Kieran Dilks</name>
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<author><name sortKey="Chen, Zhong Qiang" sort="Chen, Zhong Qiang" uniqKey="Chen Z" first="Zhong Qiang" last="Chen">Zhong Qiang Chen</name>
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<series><title level="j">Archaea</title>
<idno type="ISSN">1472-3646</idno>
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<front><div type="abstract" xml:lang="en"><p>A conserved lipid-modified cysteine found in a protein motif commonly referred to as a lipobox mediates the membrane anchoring of a subset of proteins transported across the bacterial cytoplasmic membrane via the Sec pathway. Sequenced haloarchaeal genomes encode many putative lipoproteins and recent studies have confirmed the importance of the conserved lipobox cysteine for signal peptide processing of three lipobox-containing proteins in the model archaeon <italic>Haloferax volcanii</italic>
. We have extended these <italic>in vivo</italic>
analyses to additional <italic>Hfx. volcanii</italic>
substrates, supporting our previous <italic>in silico</italic>
predictions and confirming the diversity of predicted <italic>Hfx. volcanii</italic>
lipoproteins. Moreover, using extensive comparative secretome analyses, we identified genes encodining putative lipoproteins across a wide range of archaeal species. While our <italic>in silico</italic>
analyses, supported by <italic>in vivo</italic>
data, indicate that most haloarchaeal lipoproteins are Tat substrates, these analyses also predict that many crenarchaeal species lack lipoproteins altogether and that other archaea, such as nonhalophilic euryarchaeal species, transport lipoproteins via the Sec pathway. To facilitate the identification of genes that encode potential haloarchaeal Tat-lipoproteins, we have developed TatLipo, a bioinformatic tool designed to detect lipoboxes in haloarchaeal Tat signal peptides. Our results provide a strong foundation for future studies aimed at identifying components of the archaeal lipoprotein biogenesis pathway.</p>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Archaea</journal-id>
<journal-id journal-id-type="publisher-id">ARCH</journal-id>
<journal-title-group><journal-title>Archaea</journal-title>
</journal-title-group>
<issn pub-type="ppub">1472-3646</issn>
<issn pub-type="epub">1472-3654</issn>
<publisher><publisher-name>Hindawi Publishing Corporation</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">20886060</article-id>
<article-id pub-id-type="pmc">2945643</article-id>
<article-id pub-id-type="doi">10.1155/2010/410975</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Mutational and Bioinformatic Analysis of Haloarchaeal Lipobox-Containing Proteins</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Storf</surname>
<given-names>Stefanie</given-names>
</name>
<xref ref-type="aff" rid="I1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pfeiffer</surname>
<given-names>Friedhelm</given-names>
</name>
<xref ref-type="aff" rid="I2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dilks</surname>
<given-names>Kieran</given-names>
</name>
<xref ref-type="aff" rid="I1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chen</surname>
<given-names>Zhong Qiang</given-names>
</name>
<xref ref-type="aff" rid="I1"><sup>1, 3</sup>
</xref>
<xref ref-type="aff" rid="I3"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Imam</surname>
<given-names>Saheed</given-names>
</name>
<xref ref-type="aff" rid="I4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pohlschröder</surname>
<given-names>Mechthild</given-names>
</name>
<xref ref-type="aff" rid="I1"><sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor1">*</xref>
</contrib>
</contrib-group>
<aff id="I1"><sup>1</sup>
Department of Biology, University of Pennsylvania, Philadelphia, PA 19104-6018, USA</aff>
<aff id="I2"><sup>2</sup>
Department of Membrane Biochemistry, Max-Planck-Institute of Biochemistry, Martinsried 82152, Germany</aff>
<aff id="I3"><sup>3</sup>
Graduate Group in Genomics and Computational Biology, University of Pennsylvania, Philadelphia, PA 19104-6018, USA</aff>
<aff id="I4"><sup>4</sup>
Program in Cellular and Molecular Biology, University of Wisconsin-Madison, Madison, WI 53706, USA</aff>
<author-notes><corresp id="cor1">*Mechthild Pohlschröder: <email>pohlschr@sas.upenn.edu</email>
</corresp>
<fn fn-type="other"><p>Academic Editor: Jerry Eichler</p>
</fn>
</author-notes>
<pmc-comment>For Archaea both ppub and collection dates generated from ppub source. beck 5/22/2009</pmc-comment>
<pub-date pub-type="collection"><year>2010</year>
</pub-date>
<pub-date pub-type="ppub"><year>2010</year>
</pub-date>
<pub-date pub-type="epub"><day>16</day>
<month>9</month>
<year>2010</year>
</pub-date>
<volume>2010</volume>
<elocation-id>410975</elocation-id>
<history><date date-type="received"><day>18</day>
<month>5</month>
<year>2010</year>
</date>
<date date-type="rev-recd"><day>4</day>
<month>7</month>
<year>2010</year>
</date>
<date date-type="accepted"><day>12</day>
<month>7</month>
<year>2010</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2010 Stefanie Storf et al.</copyright-statement>
<copyright-year>2010</copyright-year>
<license license-type="open-access"><license-p>This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<abstract><p>A conserved lipid-modified cysteine found in a protein motif commonly referred to as a lipobox mediates the membrane anchoring of a subset of proteins transported across the bacterial cytoplasmic membrane via the Sec pathway. Sequenced haloarchaeal genomes encode many putative lipoproteins and recent studies have confirmed the importance of the conserved lipobox cysteine for signal peptide processing of three lipobox-containing proteins in the model archaeon <italic>Haloferax volcanii</italic>
. We have extended these <italic>in vivo</italic>
analyses to additional <italic>Hfx. volcanii</italic>
substrates, supporting our previous <italic>in silico</italic>
predictions and confirming the diversity of predicted <italic>Hfx. volcanii</italic>
lipoproteins. Moreover, using extensive comparative secretome analyses, we identified genes encodining putative lipoproteins across a wide range of archaeal species. While our <italic>in silico</italic>
analyses, supported by <italic>in vivo</italic>
data, indicate that most haloarchaeal lipoproteins are Tat substrates, these analyses also predict that many crenarchaeal species lack lipoproteins altogether and that other archaea, such as nonhalophilic euryarchaeal species, transport lipoproteins via the Sec pathway. To facilitate the identification of genes that encode potential haloarchaeal Tat-lipoproteins, we have developed TatLipo, a bioinformatic tool designed to detect lipoboxes in haloarchaeal Tat signal peptides. Our results provide a strong foundation for future studies aimed at identifying components of the archaeal lipoprotein biogenesis pathway.</p>
</abstract>
</article-meta>
</front>
<floats-group><fig id="fig1" position="float"><label>Figure 1</label>
<caption><p>Tat and Sec signal peptides containing lipobox motifs. N-terminal regions of the precursors of (a) Tat; and (b) Sec substrates with lipoboxes (bold) predicted by at least two of the three lipoprotein prediction programs (PredLipo, LipoP and Prosite PS51257), with the exception of Hvo_1242, which was only LipoP-positive. Tat motifs (red) were predicted by TatFind, hydrophobic stretches (underlined), and SPase I cleavage sites (<italic>italics</italic>
) were predicted by Phobius. An arrow indicates the predicted SPase II cleavage sites.</p>
</caption>
<graphic xlink:href="ARCH2010-410975.001"></graphic>
</fig>
<fig id="fig2" position="float"><label>Figure 2</label>
<caption><p><italic>Hfx. volcanii</italic>
proteins Hvo_B0139 and Hvo_1242 are Tat substrates that require the lipobox cysteine for processing but not for anchoring to the cytoplasmic membrane. Western blot analyses of the wild-type (RR), twin lysine replacement mutants (KK), and cysteine to serine replacement mutants (C21S and C26S for Hvo_B0139, and Hvo_1242, resp.). All proteins expressed had C-terminal Myc-tags and were detected using anti-Myc antibodies. Comparable amounts of protein were loaded in each lane. The migration of molecular weight standards is indicated on the right. Predicted positions of precursor (p) and mature (m) proteins are indicated.</p>
</caption>
<graphic xlink:href="ARCH2010-410975.002"></graphic>
</fig>
<fig id="fig3" position="float"><label>Figure 3</label>
<caption><p>Putative Tat substrate lipoproteins Hvo_B0139, Hvo_1242, DsbA and arabinanase are translocated independent of TatAo in<italic> Hfx. volcanii</italic>
. Western blot analyses of wild-type (RR) Hvo_B0139, Hvo_1242, and DsbA (Hvo_1245) and arabinanase (Hvo_B0232) expressed in <italic>Hfx. volcanii</italic>
wild-type (WT) or TatAo deletion mutants (∆<italic>tatAo</italic>
). All proteins expressed had C-terminal Myc-tags, and were detected using anti-Myc antibodies. Comparable amounts of protein were loaded in each lane. The migration of molecular weight standards is indicated on the right. Predicted positions of precursor (p) and mature (m) proteins are indicated. For comparisons of the unprocessed and processed substrate migration see <xref ref-type="fig" rid="fig2">Figure 2</xref>
.</p>
</caption>
<graphic xlink:href="ARCH2010-410975.003"></graphic>
</fig>
<fig id="fig4" position="float"><label>Figure 4</label>
<caption><p>Cysteine to serine mutants of Hvo_1808, Hvo_1580, and Hvo_0494 are less stable than wild-type constructs but appear to be processed. Western blot analyses of wild-type proteins (WT), cysteine to serine replacement mutants (Hvo_1808C19S, Hvo_1580C24S and Hvo_0494C20S), and signal sequence deletion mutants (∆ss) of Hvo_1808. All proteins expressed had C-terminal Myc-tags except for Hvo_0494 and Hvo_0494C20S, which were C-terminally His-tagged. Myc and His-tagged proteins were detected using anti-Myc and anti-His antibodies, respectively. Comparable amounts of protein were loaded in each lane. The migration of molecular weight standards is indicated on the right. Predicted positions of precursor (p) and mature (m) proteins are indicated.</p>
</caption>
<graphic xlink:href="ARCH2010-410975.004"></graphic>
</fig>
<fig id="fig5" position="float"><label>Figure 5</label>
<caption><p>Only haloarchaeal Tat substrates are predicted to be predominantly lipoproteins. The predicted relative proportions are shown for several types of secreted proteins for halophilic and non-halophilic euryarchaeal species as well as crenarchaeal species and three species belonging to other archaeal phyla. (a) The percentage of secreted proteins that are Tat substrates. (b) The percentage of secreted proteins that are lipoproteins. (c) The percentage of Tat substrates that are lipoproteins. (d) The percentage of Sec substrates that are lipoproteins. (e) The percentage of lipoproteins that are secreted via the Tat pathway. (f) The percentage of proteins that are secreted (predicted Tat and Sec substrates with SPase I or SPase II cleavae sites). Raw data are available in Supplementary Table 4. Organisms are abbreviated as follows: haloarchaea (Hamar: <italic>Haloarcula marismortui</italic>
; Hasal: <italic>Halobacterium salinarum</italic>
; Hfvol: <italic>Haloferax volcanii</italic>
; Hqwal: <italic>Haloquadratum walsbyi</italic>
; Namag: <italic>Natrialba magadii</italic>
; Napha: <italic>Natronomonas pharaonis</italic>
), other euryarchaea (Arcfu: <italic>Archaeoglobus fulgidus</italic>
; Mmaze: <italic>Methanosarcina mazei</italic>
; Pyrfu: <italic>Pyrococcus furiosus</italic>
; Thkod: <italic>Thermococcus kodakarensis</italic>
; Methu: <italic>Methanospirillum hungatei</italic>
; Metja: <italic>Methanocaldococcus jannaschii</italic>
; Metka: <italic>Methanopyrus kandleri</italic>
; Picto: <italic>Picrophilus torridus</italic>
; Theac: <italic>Thermoplasma acidophilum</italic>
), crenarchaea (Apern: <italic>Aeropyrum pernix</italic>
; Calma: <italic>Caldivirga maquilingensis</italic>
; Hypbu: <italic>Hyperthermus butylicus</italic>
; Sulac: <italic>Sulfolobus acidocaldarius</italic>
; Sulso: <italic>Sulfolobus solfataricus</italic>
; Thneu: <italic>Thermoproteus neutrophilus</italic>
; Metse: <italic>Metallosphaera sedula</italic>
; Pyrar: <italic>Pyrobaculum arsenaticum</italic>
; Ighos: <italic>Ignicoccus hospitalis</italic>
), and other archaea (Nequi: <italic>Nanoarchaeum equitans</italic>
; Kocry: <italic>Korarchaeum cryptofilum</italic>
; Nitma: <italic>Nitrosopumilus maritimus</italic>
).</p>
</caption>
<graphic xlink:href="ARCH2010-410975.005"></graphic>
</fig>
<fig id="fig6" position="float"><label>Figure 6</label>
<caption><p>Conserved lipobox motifs of haloarchaea. Consensus motif was generated using the lipobox motifs of 400 predicted haloarchaeal Tat lipoproteins (see Supplementary Table 4). The alignment depicts the cleavage site G/A at position −1. Logos were generated using weblogo (<ext-link ext-link-type="uri" xlink:href="http://weblogo.berkeley.edu/">http://weblogo.berkeley.edu/</ext-link>
).</p>
</caption>
<graphic xlink:href="ARCH2010-410975.006"></graphic>
</fig>
</floats-group>
</pmc>
</record>
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