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Chimeric systems composed of swapped Tra subunits between distantly-related F plasmids reveal striking plasticity among type IV secretion machines
Bacterial type IV secretion systems (T4SSs) are a versatile family of macromolecular translocators, collectively able to recruit diverse DNA and protein substrates and deliver them to a wide range of cell types. Presently, there is little understanding of how T4SSs recognize substrate repertoires an...
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| Published in: | PLoS genetics 2024-03, Vol.20 (3), p.e1011088-e1011088 |
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| creator | Kishida, Kouhei Li, Yang Grace Ogawa-Kishida, Natsumi Khara, Pratick Al Mamun, Abu Amar M Bosserman, Rachel E Christie, Peter J |
| description | Bacterial type IV secretion systems (T4SSs) are a versatile family of macromolecular translocators, collectively able to recruit diverse DNA and protein substrates and deliver them to a wide range of cell types. Presently, there is little understanding of how T4SSs recognize substrate repertoires and form productive contacts with specific target cells. Although T4SSs are composed of a number of conserved subunits and adopt certain conserved structural features, they also display considerable compositional and structural diversity. Here, we explored the structural bases underlying the functional versatility of T4SSs through systematic deletion and subunit swapping between two conjugation systems encoded by the distantly-related IncF plasmids, pED208 and F. We identified several regions of intrinsic flexibility among the encoded T4SSs, as evidenced by partial or complete functionality of chimeric machines. Swapping of VirD4-like TraD type IV coupling proteins (T4CPs) yielded functional chimeras, indicative of relaxed specificity at the substrate-TraD and TraD-T4SS interfaces. Through mutational analyses, we further delineated domains of the TraD T4CPs contributing to recruitment of cognate vs heterologous DNA substrates. Remarkably, swaps of components comprising the outer membrane core complexes, a few F-specific subunits, or the TraA pilins supported DNA transfer in the absence of detectable pilus production. Among sequenced enterobacterial species in the NCBI database, we identified many strains that harbor two or more F-like plasmids and many F plasmids lacking one or more T4SS components required for self-transfer. We confirmed that host cells carrying co-resident, non-selftransmissible variants of pED208 and F elaborate chimeric T4SSs, as evidenced by transmission of both plasmids. We propose that T4SS plasticity enables the facile assembly of functional chimeras, and this intrinsic flexibility at the structural level can account for functional diversification of this superfamily over evolutionary time and, on a more immediate time-scale, to proliferation of transfer-defective MGEs in nature. |
| doi_str_mv | 10.1371/journal.pgen.1011088 |
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Presently, there is little understanding of how T4SSs recognize substrate repertoires and form productive contacts with specific target cells. Although T4SSs are composed of a number of conserved subunits and adopt certain conserved structural features, they also display considerable compositional and structural diversity. Here, we explored the structural bases underlying the functional versatility of T4SSs through systematic deletion and subunit swapping between two conjugation systems encoded by the distantly-related IncF plasmids, pED208 and F. We identified several regions of intrinsic flexibility among the encoded T4SSs, as evidenced by partial or complete functionality of chimeric machines. Swapping of VirD4-like TraD type IV coupling proteins (T4CPs) yielded functional chimeras, indicative of relaxed specificity at the substrate-TraD and TraD-T4SS interfaces. Through mutational analyses, we further delineated domains of the TraD T4CPs contributing to recruitment of cognate vs heterologous DNA substrates. Remarkably, swaps of components comprising the outer membrane core complexes, a few F-specific subunits, or the TraA pilins supported DNA transfer in the absence of detectable pilus production. Among sequenced enterobacterial species in the NCBI database, we identified many strains that harbor two or more F-like plasmids and many F plasmids lacking one or more T4SS components required for self-transfer. We confirmed that host cells carrying co-resident, non-selftransmissible variants of pED208 and F elaborate chimeric T4SSs, as evidenced by transmission of both plasmids. 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This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><rights>2024 Kishida et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://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>2024 Kishida et al 2024 Kishida et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c637t-e4f5a168a3e25bd228391882769122120a3fff8d1a1f5d84dfdcbbe54b95c4f73</citedby><cites>FETCH-LOGICAL-c637t-e4f5a168a3e25bd228391882769122120a3fff8d1a1f5d84dfdcbbe54b95c4f73</cites><orcidid>0000-0002-4844-4212 ; 0009-0003-0093-345X ; 0000-0003-4870-5838 ; 0009-0007-4895-9535</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/3069179553/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/3069179553?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,315,733,786,790,891,25783,27957,27958,37047,37048,44625,53827,53829,75483</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38437248$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Dalia, Ankur B.</contributor><creatorcontrib>Kishida, Kouhei</creatorcontrib><creatorcontrib>Li, Yang Grace</creatorcontrib><creatorcontrib>Ogawa-Kishida, Natsumi</creatorcontrib><creatorcontrib>Khara, Pratick</creatorcontrib><creatorcontrib>Al Mamun, Abu Amar M</creatorcontrib><creatorcontrib>Bosserman, Rachel E</creatorcontrib><creatorcontrib>Christie, Peter J</creatorcontrib><title>Chimeric systems composed of swapped Tra subunits between distantly-related F plasmids reveal striking plasticity among type IV secretion machines</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Bacterial type IV secretion systems (T4SSs) are a versatile family of macromolecular translocators, collectively able to recruit diverse DNA and protein substrates and deliver them to a wide range of cell types. 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Through mutational analyses, we further delineated domains of the TraD T4CPs contributing to recruitment of cognate vs heterologous DNA substrates. Remarkably, swaps of components comprising the outer membrane core complexes, a few F-specific subunits, or the TraA pilins supported DNA transfer in the absence of detectable pilus production. Among sequenced enterobacterial species in the NCBI database, we identified many strains that harbor two or more F-like plasmids and many F plasmids lacking one or more T4SS components required for self-transfer. We confirmed that host cells carrying co-resident, non-selftransmissible variants of pED208 and F elaborate chimeric T4SSs, as evidenced by transmission of both plasmids. 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kishida, Kouhei</au><au>Li, Yang Grace</au><au>Ogawa-Kishida, Natsumi</au><au>Khara, Pratick</au><au>Al Mamun, Abu Amar M</au><au>Bosserman, Rachel E</au><au>Christie, Peter J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Chimeric systems composed of swapped Tra subunits between distantly-related F plasmids reveal striking plasticity among type IV secretion machines</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2024-03-04</date><risdate>2024</risdate><volume>20</volume><issue>3</issue><spage>e1011088</spage><epage>e1011088</epage><pages>e1011088-e1011088</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><notes>new_version</notes><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Current address: Natsumi Ogawa-Kishida, Graduate School of Life Sciences, Tohoku University, Katahira, Aobaku, Sendai, Japan</notes><notes>Current address: Kouhei Kishida, Graduate School of Life Sciences, Tohoku University, Katahira, Aobaku, Sendai, Japan</notes><notes>Current address: Rachel Bosserman. Department of Pathology and Immunology, Division of Laboratory and Genomic Medicine, Washington School of Medicine, St. Louis, Missouri, United States of America</notes><notes>The authors have declared that no competing interests exist.</notes><abstract>Bacterial type IV secretion systems (T4SSs) are a versatile family of macromolecular translocators, collectively able to recruit diverse DNA and protein substrates and deliver them to a wide range of cell types. Presently, there is little understanding of how T4SSs recognize substrate repertoires and form productive contacts with specific target cells. Although T4SSs are composed of a number of conserved subunits and adopt certain conserved structural features, they also display considerable compositional and structural diversity. Here, we explored the structural bases underlying the functional versatility of T4SSs through systematic deletion and subunit swapping between two conjugation systems encoded by the distantly-related IncF plasmids, pED208 and F. We identified several regions of intrinsic flexibility among the encoded T4SSs, as evidenced by partial or complete functionality of chimeric machines. Swapping of VirD4-like TraD type IV coupling proteins (T4CPs) yielded functional chimeras, indicative of relaxed specificity at the substrate-TraD and TraD-T4SS interfaces. Through mutational analyses, we further delineated domains of the TraD T4CPs contributing to recruitment of cognate vs heterologous DNA substrates. Remarkably, swaps of components comprising the outer membrane core complexes, a few F-specific subunits, or the TraA pilins supported DNA transfer in the absence of detectable pilus production. Among sequenced enterobacterial species in the NCBI database, we identified many strains that harbor two or more F-like plasmids and many F plasmids lacking one or more T4SS components required for self-transfer. We confirmed that host cells carrying co-resident, non-selftransmissible variants of pED208 and F elaborate chimeric T4SSs, as evidenced by transmission of both plasmids. We propose that T4SS plasticity enables the facile assembly of functional chimeras, and this intrinsic flexibility at the structural level can account for functional diversification of this superfamily over evolutionary time and, on a more immediate time-scale, to proliferation of transfer-defective MGEs in nature.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>38437248</pmid><doi>10.1371/journal.pgen.1011088</doi><tpages>e1011088</tpages><orcidid>https://orcid.org/0000-0002-4844-4212</orcidid><orcidid>https://orcid.org/0009-0003-0093-345X</orcidid><orcidid>https://orcid.org/0000-0003-4870-5838</orcidid><orcidid>https://orcid.org/0009-0007-4895-9535</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1553-7404 |
| ispartof | PLoS genetics, 2024-03, Vol.20 (3), p.e1011088-e1011088 |
| issn | 1553-7404 1553-7390 1553-7404 |
| language | eng |
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| source | PubMed Central (Open access); Publicly Available Content Database |
| subjects | Bacterial Proteins - metabolism Biology and Life Sciences Chimeras Conjugation Deoxyribonucleic acid DNA DNA, Bacterial F Factor Fimbriae Proteins - genetics Gene deletion Genetic aspects Gram-negative bacteria Medicine and Health Sciences Mutation Nucleotide sequence Plasmids Plasmids - genetics Proteins Research and Analysis Methods Secretion Translocation (Genetics) Type IV Secretion Systems - chemistry Type IV Secretion Systems - genetics Type IV Secretion Systems - metabolism |
| title | Chimeric systems composed of swapped Tra subunits between distantly-related F plasmids reveal striking plasticity among type IV secretion machines |
| url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-09-21T13%3A46%3A57IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Chimeric%20systems%20composed%20of%20swapped%20Tra%20subunits%20between%20distantly-related%20F%20plasmids%20reveal%20striking%20plasticity%20among%20type%20IV%20secretion%20machines&rft.jtitle=PLoS%20genetics&rft.au=Kishida,%20Kouhei&rft.date=2024-03-04&rft.volume=20&rft.issue=3&rft.spage=e1011088&rft.epage=e1011088&rft.pages=e1011088-e1011088&rft.issn=1553-7404&rft.eissn=1553-7404&rft_id=info:doi/10.1371/journal.pgen.1011088&rft_dat=%3Cgale_pubme%3EA790637791%3C/gale_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c637t-e4f5a168a3e25bd228391882769122120a3fff8d1a1f5d84dfdcbbe54b95c4f73%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=3069179553&rft_id=info:pmid/38437248&rft_galeid=A790637791&rfr_iscdi=true |