Novel genomic island modifies DNA with 7-deazaguanine derivatives
The discovery of ∼20-kb gene clusters containing a family of paralogs of tRNA guanosine transglycosylase genes, called tgtA5, alongside 7-cyano-7-deazaguanine (preQ[subscript 0]) synthesis and DNA metabolism genes, led to the hypothesis that 7-deazaguanine derivatives are inserted in DNA. This was e...
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National Academy of Sciences (U.S.)
2017
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| Online Access: | http://hdl.handle.net/1721.1/107419 https://orcid.org/0000-0003-3224-7502 https://orcid.org/0000-0002-1976-8103 https://orcid.org/0000-0001-9357-0077 https://orcid.org/0000-0003-0011-3067 |
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| author | Thiaville, Jennifer J. Yuan, Yifeng Hutinet, Geoffrey Thiaville, Patrick C. Brochier-Armanet, Celine Letarov, Andrey V. Malik, Chanchal K. Rizzo, Carmelo J. de Crécy-Lagard, Valérie Kellner, Stefanie M Jumpathong, Watthanachai Mohapatra, Susovan Hillebrand, Roman Dedon, Peter C |
| author2 | Massachusetts Institute of Technology. Center for Environmental Health Sciences |
| author_facet | Massachusetts Institute of Technology. Center for Environmental Health Sciences Thiaville, Jennifer J. Yuan, Yifeng Hutinet, Geoffrey Thiaville, Patrick C. Brochier-Armanet, Celine Letarov, Andrey V. Malik, Chanchal K. Rizzo, Carmelo J. de Crécy-Lagard, Valérie Kellner, Stefanie M Jumpathong, Watthanachai Mohapatra, Susovan Hillebrand, Roman Dedon, Peter C |
| author_sort | Thiaville, Jennifer J. |
| collection | MIT |
| description | The discovery of ∼20-kb gene clusters containing a family of paralogs of tRNA guanosine transglycosylase genes, called tgtA5, alongside 7-cyano-7-deazaguanine (preQ[subscript 0]) synthesis and DNA metabolism genes, led to the hypothesis that 7-deazaguanine derivatives are inserted in DNA. This was established by detecting 2’-deoxy-preQ[subscript 0] and 2’-deoxy-7-amido-7-deazaguanosine in enzymatic hydrolysates of DNA extracted from the pathogenic, Gram-negative bacteria Salmonella enterica serovar Montevideo. These modifications were absent in the closely related S. enterica serovar Typhimurium LT2 and from a mutant of S. Montevideo, each lacking the gene cluster. This led us to rename the genes of the S. Montevideo cluster as dpdA-K for 7-deazapurine in DNA. Similar gene clusters were analyzed in ∼150 phylogenetically diverse bacteria, and the modifications were detected in DNA from other organisms containing these clusters, including Kineococcus radiotolerans, Comamonas testosteroni, and Sphingopyxis alaskensis. Comparative genomic analysis shows that, in Enterobacteriaceae, the cluster is a genomic island integrated at the leuX locus, and the phylogenetic analysis of the TgtA5 family is consistent with widespread horizontal gene transfer. Comparison of transformation efficiencies of modified or unmodified plasmids into isogenic S. Montevideo strains containing or lacking the cluster strongly suggests a restriction–modification role for the cluster in Enterobacteriaceae. Another preQ[subscript 0] derivative, 2’-deoxy-7-formamidino-7-deazaguanosine, was found in the Escherichia coli bacteriophage 9g, as predicted from the presence of homologs of genes involved in the synthesis of the archaeosine tRNA modification. These results illustrate a deep and unexpected evolutionary connection between DNA and tRNA metabolism. |
| first_indexed | 2024-09-23T11:55:03Z |
| format | Article |
| id | mit-1721.1/107419 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T11:55:03Z |
| publishDate | 2017 |
| publisher | National Academy of Sciences (U.S.) |
| record_format | dspace |
| spelling | mit-1721.1/1074192022-09-27T22:49:51Z Novel genomic island modifies DNA with 7-deazaguanine derivatives Thiaville, Jennifer J. Yuan, Yifeng Hutinet, Geoffrey Thiaville, Patrick C. Brochier-Armanet, Celine Letarov, Andrey V. Malik, Chanchal K. Rizzo, Carmelo J. de Crécy-Lagard, Valérie Kellner, Stefanie M Jumpathong, Watthanachai Mohapatra, Susovan Hillebrand, Roman Dedon, Peter C Massachusetts Institute of Technology. Center for Environmental Health Sciences Massachusetts Institute of Technology. Department of Biological Engineering Kellner, Stefanie M Jumpathong, Watthanachai Mohapatra, Susovan Hillebrand, Roman Dedon, Peter C The discovery of ∼20-kb gene clusters containing a family of paralogs of tRNA guanosine transglycosylase genes, called tgtA5, alongside 7-cyano-7-deazaguanine (preQ[subscript 0]) synthesis and DNA metabolism genes, led to the hypothesis that 7-deazaguanine derivatives are inserted in DNA. This was established by detecting 2’-deoxy-preQ[subscript 0] and 2’-deoxy-7-amido-7-deazaguanosine in enzymatic hydrolysates of DNA extracted from the pathogenic, Gram-negative bacteria Salmonella enterica serovar Montevideo. These modifications were absent in the closely related S. enterica serovar Typhimurium LT2 and from a mutant of S. Montevideo, each lacking the gene cluster. This led us to rename the genes of the S. Montevideo cluster as dpdA-K for 7-deazapurine in DNA. Similar gene clusters were analyzed in ∼150 phylogenetically diverse bacteria, and the modifications were detected in DNA from other organisms containing these clusters, including Kineococcus radiotolerans, Comamonas testosteroni, and Sphingopyxis alaskensis. Comparative genomic analysis shows that, in Enterobacteriaceae, the cluster is a genomic island integrated at the leuX locus, and the phylogenetic analysis of the TgtA5 family is consistent with widespread horizontal gene transfer. Comparison of transformation efficiencies of modified or unmodified plasmids into isogenic S. Montevideo strains containing or lacking the cluster strongly suggests a restriction–modification role for the cluster in Enterobacteriaceae. Another preQ[subscript 0] derivative, 2’-deoxy-7-formamidino-7-deazaguanosine, was found in the Escherichia coli bacteriophage 9g, as predicted from the presence of homologs of genes involved in the synthesis of the archaeosine tRNA modification. These results illustrate a deep and unexpected evolutionary connection between DNA and tRNA metabolism. Deutsche Forschungsgemeinschaft Singapore-MIT Alliance in Research and Technology (SMART) 2017-03-15T16:56:27Z 2017-03-15T16:56:27Z 2016-03 2015-09 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/107419 Thiaville, Jennifer J. et al. “Novel Genomic Island Modifies DNA with 7-Deazaguanine Derivatives.” Proceedings of the National Academy of Sciences 113.11 (2016): E1452–E1459. © 2016 National Academy of Sciences https://orcid.org/0000-0003-3224-7502 https://orcid.org/0000-0002-1976-8103 https://orcid.org/0000-0001-9357-0077 https://orcid.org/0000-0003-0011-3067 en_US http://dx.doi.org/10.1073/pnas.1518570113 Proceedings of the National Academy of Sciences Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) PNAS |
| spellingShingle | Thiaville, Jennifer J. Yuan, Yifeng Hutinet, Geoffrey Thiaville, Patrick C. Brochier-Armanet, Celine Letarov, Andrey V. Malik, Chanchal K. Rizzo, Carmelo J. de Crécy-Lagard, Valérie Kellner, Stefanie M Jumpathong, Watthanachai Mohapatra, Susovan Hillebrand, Roman Dedon, Peter C Novel genomic island modifies DNA with 7-deazaguanine derivatives |
| title | Novel genomic island modifies DNA with 7-deazaguanine derivatives |
| title_full | Novel genomic island modifies DNA with 7-deazaguanine derivatives |
| title_fullStr | Novel genomic island modifies DNA with 7-deazaguanine derivatives |
| title_full_unstemmed | Novel genomic island modifies DNA with 7-deazaguanine derivatives |
| title_short | Novel genomic island modifies DNA with 7-deazaguanine derivatives |
| title_sort | novel genomic island modifies dna with 7 deazaguanine derivatives |
| url | http://hdl.handle.net/1721.1/107419 https://orcid.org/0000-0003-3224-7502 https://orcid.org/0000-0002-1976-8103 https://orcid.org/0000-0001-9357-0077 https://orcid.org/0000-0003-0011-3067 |
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