Genes for the major structural components of Thermotogales species' togas revealed by proteomic and evolutionary analyses of OmpA and OmpB homologs
The unifying structural characteristic of members of the bacterial order Thermotogales is their toga, an unusual cell envelope that includes a loose-fitting sheath around each cell. Only two toga-associated structural proteins have been purified and characterized in Thermotoga maritima: the anchor p...
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| description | The unifying structural characteristic of members of the bacterial order Thermotogales is their toga, an unusual cell envelope that includes a loose-fitting sheath around each cell. Only two toga-associated structural proteins have been purified and characterized in Thermotoga maritima: the anchor protein OmpA1 (or Ompα) and the porin OmpB (or Ompβ). The gene encoding OmpA1 (ompA1) was cloned and sequenced and later assigned to TM0477 in the genome sequence, but because no peptide sequence was available for OmpB, its gene (ompB) was not annotated. We identified six porin candidates in the genome sequence of T. maritima. Of these candidates, only one, encoded by TM0476, has all the characteristics reported for OmpB and characteristics expected of a porin including predominant β-sheet structure, a carboxy terminus porin anchoring motif, and a porin-specific amino acid composition. We highly enriched a toga fraction of cells for OmpB by sucrose gradient centrifugation and hydroxyapatite chromatography and analyzed it by LC/MS/MS. We found that the only porin candidate that it contained was the TM0476 product. This cell fraction also had β-sheet character as determined by circular dichroism, consistent with its enrichment for OmpB. We conclude that TM0476 encodes OmpB. A phylogenetic analysis of OmpB found orthologs encoded in syntenic locations in the genomes of all but two Thermotogales species. Those without orthologs have putative isofunctional genes in their place. Phylogenetic analyses of OmpA1 revealed that each species of the Thermotogales has one or two OmpA homologs. T. maritima has two OmpA homologs, encoded by ompA1 (TM0477) and ompA2 (TM1729), both of which were found in the toga protein-enriched cell extracts. These annotations of the genes encoding toga structural proteins will guide future examinations of the structure and function of this unusual lineage-defining cell sheath. |
| doi_str_mv | 10.1371/journal.pone.0040236 |
| format | Article |
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Only two toga-associated structural proteins have been purified and characterized in Thermotoga maritima: the anchor protein OmpA1 (or Ompα) and the porin OmpB (or Ompβ). The gene encoding OmpA1 (ompA1) was cloned and sequenced and later assigned to TM0477 in the genome sequence, but because no peptide sequence was available for OmpB, its gene (ompB) was not annotated. We identified six porin candidates in the genome sequence of T. maritima. Of these candidates, only one, encoded by TM0476, has all the characteristics reported for OmpB and characteristics expected of a porin including predominant β-sheet structure, a carboxy terminus porin anchoring motif, and a porin-specific amino acid composition. We highly enriched a toga fraction of cells for OmpB by sucrose gradient centrifugation and hydroxyapatite chromatography and analyzed it by LC/MS/MS. We found that the only porin candidate that it contained was the TM0476 product. This cell fraction also had β-sheet character as determined by circular dichroism, consistent with its enrichment for OmpB. We conclude that TM0476 encodes OmpB. A phylogenetic analysis of OmpB found orthologs encoded in syntenic locations in the genomes of all but two Thermotogales species. Those without orthologs have putative isofunctional genes in their place. Phylogenetic analyses of OmpA1 revealed that each species of the Thermotogales has one or two OmpA homologs. T. maritima has two OmpA homologs, encoded by ompA1 (TM0477) and ompA2 (TM1729), both of which were found in the toga protein-enriched cell extracts. These annotations of the genes encoding toga structural proteins will guide future examinations of the structure and function of this unusual lineage-defining cell sheath.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0040236</identifier><identifier>PMID: 22768259</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Algorithms ; Amino acid composition ; Amino Acid Sequence ; Amino acids ; Anchoring ; Annotations ; Bacteria ; Bacterial Outer Membrane Proteins - genetics ; Bacterial Outer Membrane Proteins - isolation & purification ; Base Sequence ; Biological evolution ; Biology ; Cell Membrane - genetics ; Centrifugation ; Centrifugation, Density Gradient ; Chromatography ; Circular Dichroism ; Cladistic analysis ; Dichroism ; Durapatite ; E coli ; Enrichment ; Environmental Molecular Sciences Laboratory ; Evolution ; Evolution, Molecular ; Genes ; Genes, Bacterial - genetics ; Genomes ; Genomics ; Homology ; Hydroxyapatite ; Hydroxyapatites ; Laboratories ; Likelihood Functions ; Molecular Sequence Data ; Nucleotide sequence ; Phylogenetics ; Phylogeny ; Porins ; Porins - chemistry ; Porins - genetics ; Protein Multimerization ; Proteins ; Proteomics - methods ; Sequence Homology, Nucleic Acid ; Species ; Species Specificity ; Structural proteins ; Structure-function relationships ; Sucrose ; Sugar ; Synteny ; Synteny - genetics ; Thermotoga maritima - cytology ; Thermotoga maritima - genetics ; User interface</subject><ispartof>PLoS One, 7(6):e40236, 2012-06, Vol.7 (6), p.e40236-e40236</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Petrus et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Petrus et al. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c719t-63a3fd01d1302f03d19d670b120063b164107a370228e5cb0331a9438f262b323</citedby><cites>FETCH-LOGICAL-c719t-63a3fd01d1302f03d19d670b120063b164107a370228e5cb0331a9438f262b323</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3387000/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3387000/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23865,27923,27924,53790,53792,79371,79372</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22768259$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/1054455$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><contributor>Badger, Jonathan H.</contributor><creatorcontrib>Petrus, Amanda K</creatorcontrib><creatorcontrib>Swithers, Kristen S</creatorcontrib><creatorcontrib>Ranjit, Chaman</creatorcontrib><creatorcontrib>Wu, Si</creatorcontrib><creatorcontrib>Brewer, Heather M</creatorcontrib><creatorcontrib>Gogarten, J Peter</creatorcontrib><creatorcontrib>Pasa-Tolic, Ljiljana</creatorcontrib><creatorcontrib>Noll, Kenneth M</creatorcontrib><creatorcontrib>Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)</creatorcontrib><title>Genes for the major structural components of Thermotogales species' togas revealed by proteomic and evolutionary analyses of OmpA and OmpB homologs</title><title>PLoS One, 7(6):e40236</title><addtitle>PLoS One</addtitle><description>The unifying structural characteristic of members of the bacterial order Thermotogales is their toga, an unusual cell envelope that includes a loose-fitting sheath around each cell. Only two toga-associated structural proteins have been purified and characterized in Thermotoga maritima: the anchor protein OmpA1 (or Ompα) and the porin OmpB (or Ompβ). The gene encoding OmpA1 (ompA1) was cloned and sequenced and later assigned to TM0477 in the genome sequence, but because no peptide sequence was available for OmpB, its gene (ompB) was not annotated. We identified six porin candidates in the genome sequence of T. maritima. Of these candidates, only one, encoded by TM0476, has all the characteristics reported for OmpB and characteristics expected of a porin including predominant β-sheet structure, a carboxy terminus porin anchoring motif, and a porin-specific amino acid composition. We highly enriched a toga fraction of cells for OmpB by sucrose gradient centrifugation and hydroxyapatite chromatography and analyzed it by LC/MS/MS. We found that the only porin candidate that it contained was the TM0476 product. This cell fraction also had β-sheet character as determined by circular dichroism, consistent with its enrichment for OmpB. We conclude that TM0476 encodes OmpB. A phylogenetic analysis of OmpB found orthologs encoded in syntenic locations in the genomes of all but two Thermotogales species. Those without orthologs have putative isofunctional genes in their place. Phylogenetic analyses of OmpA1 revealed that each species of the Thermotogales has one or two OmpA homologs. T. maritima has two OmpA homologs, encoded by ompA1 (TM0477) and ompA2 (TM1729), both of which were found in the toga protein-enriched cell extracts. These annotations of the genes encoding toga structural proteins will guide future examinations of the structure and function of this unusual lineage-defining cell sheath.</description><subject>Algorithms</subject><subject>Amino acid composition</subject><subject>Amino Acid Sequence</subject><subject>Amino acids</subject><subject>Anchoring</subject><subject>Annotations</subject><subject>Bacteria</subject><subject>Bacterial Outer Membrane Proteins - genetics</subject><subject>Bacterial Outer Membrane Proteins - isolation & purification</subject><subject>Base Sequence</subject><subject>Biological evolution</subject><subject>Biology</subject><subject>Cell Membrane - genetics</subject><subject>Centrifugation</subject><subject>Centrifugation, Density Gradient</subject><subject>Chromatography</subject><subject>Circular Dichroism</subject><subject>Cladistic analysis</subject><subject>Dichroism</subject><subject>Durapatite</subject><subject>E coli</subject><subject>Enrichment</subject><subject>Environmental Molecular Sciences Laboratory</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Genes</subject><subject>Genes, Bacterial - genetics</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Homology</subject><subject>Hydroxyapatite</subject><subject>Hydroxyapatites</subject><subject>Laboratories</subject><subject>Likelihood Functions</subject><subject>Molecular Sequence Data</subject><subject>Nucleotide sequence</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Porins</subject><subject>Porins - chemistry</subject><subject>Porins - genetics</subject><subject>Protein Multimerization</subject><subject>Proteins</subject><subject>Proteomics - methods</subject><subject>Sequence Homology, Nucleic Acid</subject><subject>Species</subject><subject>Species Specificity</subject><subject>Structural proteins</subject><subject>Structure-function 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for the major structural components of Thermotogales species' togas revealed by proteomic and evolutionary analyses of OmpA and OmpB homologs</title><author>Petrus, Amanda K ; Swithers, Kristen S ; Ranjit, Chaman ; Wu, Si ; Brewer, Heather M ; Gogarten, J Peter ; Pasa-Tolic, Ljiljana ; Noll, Kenneth M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c719t-63a3fd01d1302f03d19d670b120063b164107a370228e5cb0331a9438f262b323</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Algorithms</topic><topic>Amino acid composition</topic><topic>Amino Acid Sequence</topic><topic>Amino acids</topic><topic>Anchoring</topic><topic>Annotations</topic><topic>Bacteria</topic><topic>Bacterial Outer Membrane Proteins - genetics</topic><topic>Bacterial Outer Membrane Proteins - isolation & purification</topic><topic>Base Sequence</topic><topic>Biological 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(Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS One, 7(6):e40236</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Petrus, Amanda K</au><au>Swithers, Kristen S</au><au>Ranjit, Chaman</au><au>Wu, Si</au><au>Brewer, Heather M</au><au>Gogarten, J Peter</au><au>Pasa-Tolic, Ljiljana</au><au>Noll, Kenneth M</au><au>Badger, Jonathan H.</au><aucorp>Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genes for the major structural components of Thermotogales species' togas revealed by proteomic and evolutionary analyses of OmpA and OmpB homologs</atitle><jtitle>PLoS One, 7(6):e40236</jtitle><addtitle>PLoS One</addtitle><date>2012-06-29</date><risdate>2012</risdate><volume>7</volume><issue>6</issue><spage>e40236</spage><epage>e40236</epage><pages>e40236-e40236</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The unifying structural characteristic of members of the bacterial order Thermotogales is their toga, an unusual cell envelope that includes a loose-fitting sheath around each cell. Only two toga-associated structural proteins have been purified and characterized in Thermotoga maritima: the anchor protein OmpA1 (or Ompα) and the porin OmpB (or Ompβ). The gene encoding OmpA1 (ompA1) was cloned and sequenced and later assigned to TM0477 in the genome sequence, but because no peptide sequence was available for OmpB, its gene (ompB) was not annotated. We identified six porin candidates in the genome sequence of T. maritima. Of these candidates, only one, encoded by TM0476, has all the characteristics reported for OmpB and characteristics expected of a porin including predominant β-sheet structure, a carboxy terminus porin anchoring motif, and a porin-specific amino acid composition. We highly enriched a toga fraction of cells for OmpB by sucrose gradient centrifugation and hydroxyapatite chromatography and analyzed it by LC/MS/MS. We found that the only porin candidate that it contained was the TM0476 product. This cell fraction also had β-sheet character as determined by circular dichroism, consistent with its enrichment for OmpB. We conclude that TM0476 encodes OmpB. A phylogenetic analysis of OmpB found orthologs encoded in syntenic locations in the genomes of all but two Thermotogales species. Those without orthologs have putative isofunctional genes in their place. Phylogenetic analyses of OmpA1 revealed that each species of the Thermotogales has one or two OmpA homologs. T. maritima has two OmpA homologs, encoded by ompA1 (TM0477) and ompA2 (TM1729), both of which were found in the toga protein-enriched cell extracts. These annotations of the genes encoding toga structural proteins will guide future examinations of the structure and function of this unusual lineage-defining cell sheath.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22768259</pmid><doi>10.1371/journal.pone.0040236</doi><tpages>e40236</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PLoS One, 7(6):e40236, 2012-06, Vol.7 (6), p.e40236-e40236 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1325045101 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Algorithms Amino acid composition Amino Acid Sequence Amino acids Anchoring Annotations Bacteria Bacterial Outer Membrane Proteins - genetics Bacterial Outer Membrane Proteins - isolation & purification Base Sequence Biological evolution Biology Cell Membrane - genetics Centrifugation Centrifugation, Density Gradient Chromatography Circular Dichroism Cladistic analysis Dichroism Durapatite E coli Enrichment Environmental Molecular Sciences Laboratory Evolution Evolution, Molecular Genes Genes, Bacterial - genetics Genomes Genomics Homology Hydroxyapatite Hydroxyapatites Laboratories Likelihood Functions Molecular Sequence Data Nucleotide sequence Phylogenetics Phylogeny Porins Porins - chemistry Porins - genetics Protein Multimerization Proteins Proteomics - methods Sequence Homology, Nucleic Acid Species Species Specificity Structural proteins Structure-function relationships Sucrose Sugar Synteny Synteny - genetics Thermotoga maritima - cytology Thermotoga maritima - genetics User interface |
| title | Genes for the major structural components of Thermotogales species' togas revealed by proteomic and evolutionary analyses of OmpA and OmpB homologs |
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