ComM is a hexameric helicase that promotes branch migration during natural transformation in diverse Gram-negative species
Abstract Acquisition of foreign DNA by natural transformation is an important mechanism of adaptation and evolution in diverse microbial species. Here, we characterize the mechanism of ComM, a broadly conserved AAA+ protein previously implicated in homologous recombination of transforming DNA (tDNA)...
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| Veröffentlicht in: | Nucleic acids research 2018-07, Vol.46 (12), p.6099-6111 |
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| creator | Nero, Thomas M Dalia, Triana N Wang, Joseph Che-Yen Kysela, David T Bochman, Matthew L Dalia, Ankur B |
| description | Abstract
Acquisition of foreign DNA by natural transformation is an important mechanism of adaptation and evolution in diverse microbial species. Here, we characterize the mechanism of ComM, a broadly conserved AAA+ protein previously implicated in homologous recombination of transforming DNA (tDNA) in naturally competent Gram-negative bacterial species. In vivo, we found that ComM was required for efficient comigration of linked genetic markers in Vibrio cholerae and Acinetobacter baylyi, which is consistent with a role in branch migration. Also, ComM was particularly important for integration of tDNA with increased sequence heterology, suggesting that its activity promotes the acquisition of novel DNA sequences. In vitro, we showed that purified ComM binds ssDNA, oligomerizes into a hexameric ring, and has bidirectional helicase and branch migration activity. Based on these data, we propose a model for tDNA integration during natural transformation. This study provides mechanistic insight into the enigmatic steps involved in tDNA integration and uncovers the function of a protein required for this conserved mechanism of horizontal gene transfer. |
| doi_str_mv | 10.1093/nar/gky343 |
| format | Article |
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Acquisition of foreign DNA by natural transformation is an important mechanism of adaptation and evolution in diverse microbial species. Here, we characterize the mechanism of ComM, a broadly conserved AAA+ protein previously implicated in homologous recombination of transforming DNA (tDNA) in naturally competent Gram-negative bacterial species. In vivo, we found that ComM was required for efficient comigration of linked genetic markers in Vibrio cholerae and Acinetobacter baylyi, which is consistent with a role in branch migration. Also, ComM was particularly important for integration of tDNA with increased sequence heterology, suggesting that its activity promotes the acquisition of novel DNA sequences. In vitro, we showed that purified ComM binds ssDNA, oligomerizes into a hexameric ring, and has bidirectional helicase and branch migration activity. Based on these data, we propose a model for tDNA integration during natural transformation. This study provides mechanistic insight into the enigmatic steps involved in tDNA integration and uncovers the function of a protein required for this conserved mechanism of horizontal gene transfer.</description><identifier>ISSN: 0305-1048</identifier><identifier>ISSN: 1362-4962</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gky343</identifier><identifier>PMID: 29722872</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Acinetobacter - enzymology ; Acinetobacter - genetics ; Adenosine Triphosphate - metabolism ; Bacterial Proteins - physiology ; DNA - metabolism ; DNA Helicases - metabolism ; DNA Helicases - physiology ; DNA Repair ; DNA, Bacterial - metabolism ; DNA, Single-Stranded - metabolism ; DNA-Binding Proteins - physiology ; Gene Transfer, Horizontal ; Genome Integrity, Repair and ; Gram-Negative Bacteria - enzymology ; Gram-Negative Bacteria - genetics ; Protein Multimerization ; Transformation, Genetic ; Vibrio cholerae - enzymology ; Vibrio cholerae - genetics</subject><ispartof>Nucleic acids research, 2018-07, Vol.46 (12), p.6099-6111</ispartof><rights>The Author(s) 2018. Published by Oxford University Press on behalf of Nucleic Acids Research. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c408t-aac4c9d20b92b48fac89427a1ac58fd1289de242b6d8daa6facc486cbf055f683</citedby><cites>FETCH-LOGICAL-c408t-aac4c9d20b92b48fac89427a1ac58fd1289de242b6d8daa6facc486cbf055f683</cites><orcidid>0000-0002-2807-0452</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6158740/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6158740/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1598,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29722872$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nero, Thomas M</creatorcontrib><creatorcontrib>Dalia, Triana N</creatorcontrib><creatorcontrib>Wang, Joseph Che-Yen</creatorcontrib><creatorcontrib>Kysela, David T</creatorcontrib><creatorcontrib>Bochman, Matthew L</creatorcontrib><creatorcontrib>Dalia, Ankur B</creatorcontrib><title>ComM is a hexameric helicase that promotes branch migration during natural transformation in diverse Gram-negative species</title><title>Nucleic acids research</title><addtitle>Nucleic Acids Res</addtitle><description>Abstract
Acquisition of foreign DNA by natural transformation is an important mechanism of adaptation and evolution in diverse microbial species. Here, we characterize the mechanism of ComM, a broadly conserved AAA+ protein previously implicated in homologous recombination of transforming DNA (tDNA) in naturally competent Gram-negative bacterial species. In vivo, we found that ComM was required for efficient comigration of linked genetic markers in Vibrio cholerae and Acinetobacter baylyi, which is consistent with a role in branch migration. Also, ComM was particularly important for integration of tDNA with increased sequence heterology, suggesting that its activity promotes the acquisition of novel DNA sequences. In vitro, we showed that purified ComM binds ssDNA, oligomerizes into a hexameric ring, and has bidirectional helicase and branch migration activity. Based on these data, we propose a model for tDNA integration during natural transformation. This study provides mechanistic insight into the enigmatic steps involved in tDNA integration and uncovers the function of a protein required for this conserved mechanism of horizontal gene transfer.</description><subject>Acinetobacter - enzymology</subject><subject>Acinetobacter - genetics</subject><subject>Adenosine Triphosphate - metabolism</subject><subject>Bacterial Proteins - physiology</subject><subject>DNA - metabolism</subject><subject>DNA Helicases - metabolism</subject><subject>DNA Helicases - physiology</subject><subject>DNA Repair</subject><subject>DNA, Bacterial - metabolism</subject><subject>DNA, Single-Stranded - metabolism</subject><subject>DNA-Binding Proteins - physiology</subject><subject>Gene Transfer, Horizontal</subject><subject>Genome Integrity, Repair and</subject><subject>Gram-Negative Bacteria - enzymology</subject><subject>Gram-Negative Bacteria - genetics</subject><subject>Protein Multimerization</subject><subject>Transformation, Genetic</subject><subject>Vibrio cholerae - enzymology</subject><subject>Vibrio cholerae - genetics</subject><issn>0305-1048</issn><issn>1362-4962</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNp9kVFr1TAYhoM43NnmjT9g5EYYQl2Spj3pjSCHOYUNb9x1-Jp-7Yk2SU3ag_PXm9E55o1X-eB9ePLCS8gbzt5z1pSXHuLl8OO-lOULsuFlLQrZ1OIl2bCSVQVnUh2Tk5S-M8Ylr-QrciyarRBqKzbk9y64W2oTBbrHX-AwWpOv0RpISOc9zHSKwYUZE20jeLOnzg4RZhs87ZZo_UA9zEuEkc45T32Ibk1tBuwBY_ZcR3CFxyEHB6RpQmMxnZGjHsaErx_fU3L36erb7nNx8_X6y-7jTWEkU3MBYKRpOsHaRrRS9WBUI8UWOJhK9R0XqulQSNHWneoA6gwYqWrT9qyq-lqVp-TD6p2W1mFn0Oeio56idRDvdQCr_0283eshHHTNK7WVLAsuHgUx_FwwzdrZZHAcwWNYkhaslLmFYHVG362oiSGliP3TN5zph7F0HkuvY2X4_HmxJ_TvOhl4uwJhmf4n-gM4PaJz</recordid><startdate>20180706</startdate><enddate>20180706</enddate><creator>Nero, Thomas M</creator><creator>Dalia, Triana N</creator><creator>Wang, Joseph Che-Yen</creator><creator>Kysela, David T</creator><creator>Bochman, Matthew L</creator><creator>Dalia, Ankur B</creator><general>Oxford University Press</general><scope>TOX</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><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2807-0452</orcidid></search><sort><creationdate>20180706</creationdate><title>ComM is a hexameric helicase that promotes branch migration during natural transformation in diverse Gram-negative species</title><author>Nero, Thomas M ; Dalia, Triana N ; Wang, Joseph Che-Yen ; Kysela, David T ; Bochman, Matthew L ; Dalia, Ankur B</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c408t-aac4c9d20b92b48fac89427a1ac58fd1289de242b6d8daa6facc486cbf055f683</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Acinetobacter - enzymology</topic><topic>Acinetobacter - genetics</topic><topic>Adenosine Triphosphate - metabolism</topic><topic>Bacterial Proteins - physiology</topic><topic>DNA - metabolism</topic><topic>DNA Helicases - metabolism</topic><topic>DNA Helicases - physiology</topic><topic>DNA Repair</topic><topic>DNA, Bacterial - metabolism</topic><topic>DNA, Single-Stranded - metabolism</topic><topic>DNA-Binding Proteins - physiology</topic><topic>Gene Transfer, Horizontal</topic><topic>Genome Integrity, Repair and</topic><topic>Gram-Negative Bacteria - enzymology</topic><topic>Gram-Negative Bacteria - genetics</topic><topic>Protein Multimerization</topic><topic>Transformation, Genetic</topic><topic>Vibrio cholerae - enzymology</topic><topic>Vibrio cholerae - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nero, Thomas M</creatorcontrib><creatorcontrib>Dalia, Triana N</creatorcontrib><creatorcontrib>Wang, Joseph Che-Yen</creatorcontrib><creatorcontrib>Kysela, David T</creatorcontrib><creatorcontrib>Bochman, Matthew L</creatorcontrib><creatorcontrib>Dalia, Ankur B</creatorcontrib><collection>Oxford Open</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><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nucleic acids research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nero, Thomas M</au><au>Dalia, Triana N</au><au>Wang, Joseph Che-Yen</au><au>Kysela, David T</au><au>Bochman, Matthew L</au><au>Dalia, Ankur B</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>ComM is a hexameric helicase that promotes branch migration during natural transformation in diverse Gram-negative species</atitle><jtitle>Nucleic acids research</jtitle><addtitle>Nucleic Acids Res</addtitle><date>2018-07-06</date><risdate>2018</risdate><volume>46</volume><issue>12</issue><spage>6099</spage><epage>6111</epage><pages>6099-6111</pages><issn>0305-1048</issn><issn>1362-4962</issn><eissn>1362-4962</eissn><abstract>Abstract
Acquisition of foreign DNA by natural transformation is an important mechanism of adaptation and evolution in diverse microbial species. Here, we characterize the mechanism of ComM, a broadly conserved AAA+ protein previously implicated in homologous recombination of transforming DNA (tDNA) in naturally competent Gram-negative bacterial species. In vivo, we found that ComM was required for efficient comigration of linked genetic markers in Vibrio cholerae and Acinetobacter baylyi, which is consistent with a role in branch migration. Also, ComM was particularly important for integration of tDNA with increased sequence heterology, suggesting that its activity promotes the acquisition of novel DNA sequences. In vitro, we showed that purified ComM binds ssDNA, oligomerizes into a hexameric ring, and has bidirectional helicase and branch migration activity. Based on these data, we propose a model for tDNA integration during natural transformation. This study provides mechanistic insight into the enigmatic steps involved in tDNA integration and uncovers the function of a protein required for this conserved mechanism of horizontal gene transfer.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>29722872</pmid><doi>10.1093/nar/gky343</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-2807-0452</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Acinetobacter - enzymology Acinetobacter - genetics Adenosine Triphosphate - metabolism Bacterial Proteins - physiology DNA - metabolism DNA Helicases - metabolism DNA Helicases - physiology DNA Repair DNA, Bacterial - metabolism DNA, Single-Stranded - metabolism DNA-Binding Proteins - physiology Gene Transfer, Horizontal Genome Integrity, Repair and Gram-Negative Bacteria - enzymology Gram-Negative Bacteria - genetics Protein Multimerization Transformation, Genetic Vibrio cholerae - enzymology Vibrio cholerae - genetics |
| title | ComM is a hexameric helicase that promotes branch migration during natural transformation in diverse Gram-negative species |
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