First description of arginine catabolic mobile element (ACME) type VI harboring the kdp operon only in Staphylococcus epidermidis using short and long read whole genome sequencing: Further evidence of ACME diversity
The arginine catabolic mobile element (ACME) was first described in methicillin-resistant Staphylococcus aureus and is considered to enhance transmission, persistence and survival. Subsequently ACMEs were shown to be more prevalent in the coagulase-negative Staphylococcus epidermidis. Previously, AC...
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description | The arginine catabolic mobile element (ACME) was first described in methicillin-resistant Staphylococcus aureus and is considered to enhance transmission, persistence and survival. Subsequently ACMEs were shown to be more prevalent in the coagulase-negative Staphylococcus epidermidis. Previously, ACME types were distinguished by characteristic combinations of the arc and opp3 operons [I (arc+, opp3+), II (arc+, opp3-) and III (arc-, opp3+)] encoding an arginine deaminase pathway and oligopeptide permease transporter, respectively. Recently two novel ACME types harboring the potassium transporter-encoding operon kdp were described in oral S. epidermidis isolates [IV (arc+, opp3-, kdp+), and V (arc+, opp3+, kdp+)].
This study investigated two independent oral S. epidermidis isolates that yielded amplimers with kdp-directed primers only when subjected to ACME typing PCRs. Hybrid assemblies based on Illumina MiSeq short-read and Oxford Nanopore MinION long-read whole genome sequences revealed that both isolates harbored a sixth, novel ACME type (VI) integrated into orfX. Both ACME VIs lacked the arc and opp3 operons, harbored the kdp operon adjacent to other commonly ACME-associated genes including speG, hsd, sdr, and rep, but the structural organization of the adjacent regions were distinct. These ACMEs were flanked by different direct repeat sequences and the ACME VI-positive isolates belonged to unrelated genetic clusters. Overall these findings are indicative of independent evolution. The identification of ACME type VI further illustrates the diversity of ACME elements in S. epidermidis. The presence of ACMEs harboring kdp may confer a selective advantage on oral S. epidermidis in a potassium-rich environment such as found in dental plaque.
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•First description of novel arginine catabolic mobile element (ACME) type VI•The ACME type VI element harbors the kdp operon but lacks the arc and opp3 operons.•Two phylogenetically distinct oral S. epidermidis isolates harbored ACME VI.•Each ACME VI investigated was flanked by distinct direct repeat sequences.•The kdp operon encodes a potassium transporter system. |
doi_str_mv | 10.1016/j.meegid.2019.03.008 |
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This study investigated two independent oral S. epidermidis isolates that yielded amplimers with kdp-directed primers only when subjected to ACME typing PCRs. Hybrid assemblies based on Illumina MiSeq short-read and Oxford Nanopore MinION long-read whole genome sequences revealed that both isolates harbored a sixth, novel ACME type (VI) integrated into orfX. Both ACME VIs lacked the arc and opp3 operons, harbored the kdp operon adjacent to other commonly ACME-associated genes including speG, hsd, sdr, and rep, but the structural organization of the adjacent regions were distinct. These ACMEs were flanked by different direct repeat sequences and the ACME VI-positive isolates belonged to unrelated genetic clusters. Overall these findings are indicative of independent evolution. The identification of ACME type VI further illustrates the diversity of ACME elements in S. epidermidis. The presence of ACMEs harboring kdp may confer a selective advantage on oral S. epidermidis in a potassium-rich environment such as found in dental plaque.
[Display omitted]
•First description of novel arginine catabolic mobile element (ACME) type VI•The ACME type VI element harbors the kdp operon but lacks the arc and opp3 operons.•Two phylogenetically distinct oral S. epidermidis isolates harbored ACME VI.•Each ACME VI investigated was flanked by distinct direct repeat sequences.•The kdp operon encodes a potassium transporter system.</description><identifier>ISSN: 1567-1348</identifier><identifier>EISSN: 1567-7257</identifier><identifier>DOI: 10.1016/j.meegid.2019.03.008</identifier><identifier>PMID: 30898642</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>ACME ; Adenosine Triphosphatases - genetics ; Arginine - genetics ; Arginine - metabolism ; Cation Transport Proteins - genetics ; DNA Transposable Elements - genetics ; Genetic Variation ; Genomic Islands ; Humans ; kdp operon ; Operon - genetics ; Oral cavity ; Potassium uptake ; Staphylococcal Infections - microbiology ; Staphylococcus epidermidis ; Staphylococcus epidermidis - genetics ; Whole Genome Sequencing</subject><ispartof>Infection, genetics and evolution, 2019-07, Vol.71, p.51-53</ispartof><rights>2019 The Authors</rights><rights>Copyright © 2019 The Authors. Published by Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c408t-c01026d658752919d6ec9d922614683f6522f00d53a0718677415eaee8ec4c643</citedby><cites>FETCH-LOGICAL-c408t-c01026d658752919d6ec9d922614683f6522f00d53a0718677415eaee8ec4c643</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1567134818308165$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30898642$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>McManus, Brenda A.</creatorcontrib><creatorcontrib>O'Connor, Aoife M.</creatorcontrib><creatorcontrib>Egan, Sarah A.</creatorcontrib><creatorcontrib>Flanagan, Peter R.</creatorcontrib><creatorcontrib>Coleman, David C.</creatorcontrib><title>First description of arginine catabolic mobile element (ACME) type VI harboring the kdp operon only in Staphylococcus epidermidis using short and long read whole genome sequencing: Further evidence of ACME diversity</title><title>Infection, genetics and evolution</title><addtitle>Infect Genet Evol</addtitle><description>The arginine catabolic mobile element (ACME) was first described in methicillin-resistant Staphylococcus aureus and is considered to enhance transmission, persistence and survival. Subsequently ACMEs were shown to be more prevalent in the coagulase-negative Staphylococcus epidermidis. Previously, ACME types were distinguished by characteristic combinations of the arc and opp3 operons [I (arc+, opp3+), II (arc+, opp3-) and III (arc-, opp3+)] encoding an arginine deaminase pathway and oligopeptide permease transporter, respectively. Recently two novel ACME types harboring the potassium transporter-encoding operon kdp were described in oral S. epidermidis isolates [IV (arc+, opp3-, kdp+), and V (arc+, opp3+, kdp+)].
This study investigated two independent oral S. epidermidis isolates that yielded amplimers with kdp-directed primers only when subjected to ACME typing PCRs. Hybrid assemblies based on Illumina MiSeq short-read and Oxford Nanopore MinION long-read whole genome sequences revealed that both isolates harbored a sixth, novel ACME type (VI) integrated into orfX. Both ACME VIs lacked the arc and opp3 operons, harbored the kdp operon adjacent to other commonly ACME-associated genes including speG, hsd, sdr, and rep, but the structural organization of the adjacent regions were distinct. These ACMEs were flanked by different direct repeat sequences and the ACME VI-positive isolates belonged to unrelated genetic clusters. Overall these findings are indicative of independent evolution. The identification of ACME type VI further illustrates the diversity of ACME elements in S. epidermidis. The presence of ACMEs harboring kdp may confer a selective advantage on oral S. epidermidis in a potassium-rich environment such as found in dental plaque.
[Display omitted]
•First description of novel arginine catabolic mobile element (ACME) type VI•The ACME type VI element harbors the kdp operon but lacks the arc and opp3 operons.•Two phylogenetically distinct oral S. epidermidis isolates harbored ACME VI.•Each ACME VI investigated was flanked by distinct direct repeat sequences.•The kdp operon encodes a potassium transporter system.</description><subject>ACME</subject><subject>Adenosine Triphosphatases - genetics</subject><subject>Arginine - genetics</subject><subject>Arginine - metabolism</subject><subject>Cation Transport Proteins - genetics</subject><subject>DNA Transposable Elements - genetics</subject><subject>Genetic Variation</subject><subject>Genomic Islands</subject><subject>Humans</subject><subject>kdp operon</subject><subject>Operon - genetics</subject><subject>Oral cavity</subject><subject>Potassium uptake</subject><subject>Staphylococcal Infections - microbiology</subject><subject>Staphylococcus epidermidis</subject><subject>Staphylococcus epidermidis - genetics</subject><subject>Whole Genome Sequencing</subject><issn>1567-1348</issn><issn>1567-7257</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9Uc2O0zAQjhCIXRbeAKE57h5abCdxEg5Iq2oLKy3iwM_Vcu1pO0tiB9sp6pPyOjhq4chpPNL3N_6K4jVnS864fPu4HBB3ZJeC8W7JyiVj7ZPikteyWTSibp6e37ys2oviRYyPjPGGifZ5cVGytmtlJS6L32sKMYHFaAKNibwDvwUdduTIIRid9Mb3ZGDwG-oRsMcBXYLr29WnuxtIxxHh-z3sddj4QG4HaY_ww47gRwyzmOuPQA6-JD3uj7033pgpAo5kMQxkKcIUZ17c-5BAOwu9z2tAbeHX3mfLHTo_IET8OaEzGfsO1lPIPgHwkGWcwTnzHAgsHTBESseXxbOt7iO-Os-r4tv67uvq4-Lh84f71e3DwlSsTQvDOBPSyrptatHxzko0ne2EkLySbbmVtRBbxmxdatbwVjZNxWvUiC2aysiqvCquT7pj8DlfTGqgaLDvtUM_RSV4lzXKmpcZWp2gJvgYA27VGGjQ4ag4U3Ol6lGdKlVzpYqVKleaaW_ODtNmQPuP9LfDDHh_AmC-80AYVDQ0_4qlgCYp6-n_Dn8ALR63Tw</recordid><startdate>201907</startdate><enddate>201907</enddate><creator>McManus, Brenda A.</creator><creator>O'Connor, Aoife M.</creator><creator>Egan, Sarah A.</creator><creator>Flanagan, Peter R.</creator><creator>Coleman, David C.</creator><general>Elsevier B.V</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>201907</creationdate><title>First description of arginine catabolic mobile element (ACME) type VI harboring the kdp operon only in Staphylococcus epidermidis using short and long read whole genome sequencing: Further evidence of ACME diversity</title><author>McManus, Brenda A. ; O'Connor, Aoife M. ; Egan, Sarah A. ; Flanagan, Peter R. ; Coleman, David C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c408t-c01026d658752919d6ec9d922614683f6522f00d53a0718677415eaee8ec4c643</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>ACME</topic><topic>Adenosine Triphosphatases - genetics</topic><topic>Arginine - genetics</topic><topic>Arginine - metabolism</topic><topic>Cation Transport Proteins - genetics</topic><topic>DNA Transposable Elements - genetics</topic><topic>Genetic Variation</topic><topic>Genomic Islands</topic><topic>Humans</topic><topic>kdp operon</topic><topic>Operon - genetics</topic><topic>Oral cavity</topic><topic>Potassium uptake</topic><topic>Staphylococcal Infections - microbiology</topic><topic>Staphylococcus epidermidis</topic><topic>Staphylococcus epidermidis - genetics</topic><topic>Whole Genome Sequencing</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>McManus, Brenda A.</creatorcontrib><creatorcontrib>O'Connor, Aoife M.</creatorcontrib><creatorcontrib>Egan, Sarah A.</creatorcontrib><creatorcontrib>Flanagan, Peter R.</creatorcontrib><creatorcontrib>Coleman, David C.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Infection, genetics and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>McManus, Brenda A.</au><au>O'Connor, Aoife M.</au><au>Egan, Sarah A.</au><au>Flanagan, Peter R.</au><au>Coleman, David C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>First description of arginine catabolic mobile element (ACME) type VI harboring the kdp operon only in Staphylococcus epidermidis using short and long read whole genome sequencing: Further evidence of ACME diversity</atitle><jtitle>Infection, genetics and evolution</jtitle><addtitle>Infect Genet Evol</addtitle><date>2019-07</date><risdate>2019</risdate><volume>71</volume><spage>51</spage><epage>53</epage><pages>51-53</pages><issn>1567-1348</issn><eissn>1567-7257</eissn><abstract>The arginine catabolic mobile element (ACME) was first described in methicillin-resistant Staphylococcus aureus and is considered to enhance transmission, persistence and survival. Subsequently ACMEs were shown to be more prevalent in the coagulase-negative Staphylococcus epidermidis. Previously, ACME types were distinguished by characteristic combinations of the arc and opp3 operons [I (arc+, opp3+), II (arc+, opp3-) and III (arc-, opp3+)] encoding an arginine deaminase pathway and oligopeptide permease transporter, respectively. Recently two novel ACME types harboring the potassium transporter-encoding operon kdp were described in oral S. epidermidis isolates [IV (arc+, opp3-, kdp+), and V (arc+, opp3+, kdp+)].
This study investigated two independent oral S. epidermidis isolates that yielded amplimers with kdp-directed primers only when subjected to ACME typing PCRs. Hybrid assemblies based on Illumina MiSeq short-read and Oxford Nanopore MinION long-read whole genome sequences revealed that both isolates harbored a sixth, novel ACME type (VI) integrated into orfX. Both ACME VIs lacked the arc and opp3 operons, harbored the kdp operon adjacent to other commonly ACME-associated genes including speG, hsd, sdr, and rep, but the structural organization of the adjacent regions were distinct. These ACMEs were flanked by different direct repeat sequences and the ACME VI-positive isolates belonged to unrelated genetic clusters. Overall these findings are indicative of independent evolution. The identification of ACME type VI further illustrates the diversity of ACME elements in S. epidermidis. The presence of ACMEs harboring kdp may confer a selective advantage on oral S. epidermidis in a potassium-rich environment such as found in dental plaque.
[Display omitted]
•First description of novel arginine catabolic mobile element (ACME) type VI•The ACME type VI element harbors the kdp operon but lacks the arc and opp3 operons.•Two phylogenetically distinct oral S. epidermidis isolates harbored ACME VI.•Each ACME VI investigated was flanked by distinct direct repeat sequences.•The kdp operon encodes a potassium transporter system.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>30898642</pmid><doi>10.1016/j.meegid.2019.03.008</doi><tpages>3</tpages><oa>free_for_read</oa></addata></record> |
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subjects | ACME Adenosine Triphosphatases - genetics Arginine - genetics Arginine - metabolism Cation Transport Proteins - genetics DNA Transposable Elements - genetics Genetic Variation Genomic Islands Humans kdp operon Operon - genetics Oral cavity Potassium uptake Staphylococcal Infections - microbiology Staphylococcus epidermidis Staphylococcus epidermidis - genetics Whole Genome Sequencing |
title | First description of arginine catabolic mobile element (ACME) type VI harboring the kdp operon only in Staphylococcus epidermidis using short and long read whole genome sequencing: Further evidence of ACME diversity |
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