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Rapid dissemination of host metabolism-manipulating genes via integrative and conjugative elements.

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Τίτλος: Rapid dissemination of host metabolism-manipulating genes via integrative and conjugative elements.
Συγγραφείς: Colombi E; School of Agriculture, Food and Ecosystem Sciences, Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia., Bertels F; Department of Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Plön 24306, Germany., Doulcier G; Laboratoire Biophysique et Évolution, Institut Chemie Biologie Innovation, École Supérieure de Physique et de Chemie Industrielles de la Ville de Paris, Université Paris Science et Lettres, Centre National de al Reserche Scientifique, Paris 75005, France., McConnell E; Department of Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Plön 24306, Germany., Pichugina T; Department of Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Plön 24306, Germany., Sohn KH; Plant Immunity Research Center, Seoul National University, Seoul 08826, Republic of Korea.; Department of Agricultural Biotechnology, Seoul National University, Seoul 08826, Republic of Korea.; Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Republic of Korea.; Plant Genomics and Breeding Institute, Seoul National University, Seoul 08826, Republic of Korea., Straub C; Health and Environment, Institute of Environmental Science and Research, Auckland 1025, New Zealand.; Division of Microbial Ecology, Center for Microbiology and Environmental Systems Science, University of Vienna, Vienna 1030, Austria., McCann HC; Plant Pathogen Evolution Research Group, Max Planck Institute for Biology, Tübingen 72076, Germany., Rainey PB; Department of Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Plön 24306, Germany.; Laboratoire Biophysique et Évolution, Institut Chemie Biologie Innovation, École Supérieure de Physique et de Chemie Industrielles de la Ville de Paris, Université Paris Science et Lettres, Centre National de al Reserche Scientifique, Paris 75005, France.
Πηγή: Proceedings of the National Academy of Sciences of the United States of America [Proc Natl Acad Sci U S A] 2024 Mar 12; Vol. 121 (11), pp. e2309263121. Date of Electronic Publication: 2024 Mar 08.
Τύπος έκδοσης: Journal Article; Research Support, Non-U.S. Gov't
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: National Academy of Sciences Country of Publication: United States NLM ID: 7505876 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1091-6490 (Electronic) Linking ISSN: 00278424 NLM ISO Abbreviation: Proc Natl Acad Sci U S A Subsets: MEDLINE
Imprint Name(s): Original Publication: Washington, DC : National Academy of Sciences
Ιατρικοί όροι (MeSH): Gene Transfer, Horizontal*/genetics , Conjugation, Genetic*, DNA Transposable Elements/genetics ; Phylogeny ; Biological Evolution
Περίληψη: Integrative and conjugative elements (ICEs) are self-transmissible mobile elements that transfer functional genetic units across broad phylogenetic distances. Accessory genes shuttled by ICEs can make significant contributions to bacterial fitness. Most ICEs characterized to date encode readily observable phenotypes contributing to symbiosis, pathogenicity, and antimicrobial resistance, yet the majority of ICEs carry genes of unknown function. Recent observations of rapid acquisition of ICEs in a pandemic lineage of Pseudomonas syringae pv. actinidae led to investigation of the structural and functional diversity of these elements. Fifty-three unique ICE types were identified across the P. syringae species complex. Together they form a distinct family of ICEs (PsICEs) that share a distant relationship to ICEs found in Pseudomonas aeruginosa. PsICEs are defined by conserved backbone genes punctuated by an array of accessory cargo genes, are highly recombinogenic, and display distinct evolutionary histories compared to their bacterial hosts. The most common cargo is a recently disseminated 16-kb mobile genetic element designated Tn6212. Deletion of Tn6212 did not alter pathogen growth in planta, but mutants displayed fitness defects when grown on tricarboxylic acid (TCA) cycle intermediates. RNA-seq analysis of a set of nested deletion mutants showed that a Tn6212-encoded LysR regulator has global effects on chromosomal gene expression. We show that Tn6212 responds to preferred carbon sources and manipulates bacterial metabolism to maximize growth.
Competing Interests: Competing interests statement:The authors declare no competing interest.
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J Bacteriol. 2007 Mar;189(6):2443-59. (PMID: 17194795)
Nat Commun. 2018 Nov 30;9(1):5114. (PMID: 30504855)
Mol Biol Evol. 2013 Apr;30(4):772-80. (PMID: 23329690)
Nat Rev Microbiol. 2010 Aug;8(8):552-63. (PMID: 20601965)
PLoS Genet. 2011 Aug;7(8):e1002222. (PMID: 21876676)
Front Plant Sci. 2019 Apr 05;10:418. (PMID: 31024592)
Bioinformatics. 2015 Nov 15;31(22):3691-3. (PMID: 26198102)
Mol Plant Pathol. 2017 Jan;18(1):152-168. (PMID: 27798954)
Genome Biol. 2014;15(12):550. (PMID: 25516281)
ISME J. 2008 Mar;2(3):321-34. (PMID: 18185595)
PLoS Pathog. 2013;9(7):e1003503. (PMID: 23935484)
Mol Biol Evol. 2006 Feb;23(2):254-67. (PMID: 16221896)
Annu Rev Genet. 2015;49:577-601. (PMID: 26473380)
J Bacteriol. 2004 Dec;186(23):8114-22. (PMID: 15547285)
Mol Biol Evol. 2014 May;31(5):1077-88. (PMID: 24600054)
Environ Microbiol. 2014 Aug;16(8):2374-88. (PMID: 24286439)
Mol Biol Evol. 1987 Jul;4(4):406-25. (PMID: 3447015)
Cell Mol Life Sci. 2020 Feb;77(3):395-413. (PMID: 31768608)
FEMS Microbiol Rev. 2017 Jul 1;41(4):512-537. (PMID: 28369623)
Plant Commun. 2021 Dec 28;3(2):100272. (PMID: 35529946)
Microb Genom. 2021 Oct;7(10):. (PMID: 34605762)
Sci Rep. 2017 Jun 15;7(1):3557. (PMID: 28620210)
Mol Biol Evol. 2019 May 1;36(5):1071-1085. (PMID: 30835268)
Nature. 1996 May 9;381(6578):169-72. (PMID: 8610017)
Curr Biol. 2005 Dec 20;15(24):2230-5. (PMID: 16360685)
mBio. 2010 Jun 29;1(3):. (PMID: 20802828)
Theor Popul Biol. 2002 Jun;61(4):449-60. (PMID: 12167364)
Mol Microbiol. 2000 Oct;38(2):186-97. (PMID: 11069647)
Environ Microbiol. 2017 Feb;19(2):819-832. (PMID: 28063194)
Mol Biol Evol. 2004 Feb;21(2):255-65. (PMID: 14660700)
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J Mol Biol. 1990 Oct 5;215(3):403-10. (PMID: 2231712)
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Grant Information: MAU1709 Royal Society of New Zealand | Marsden Fund (Royal Society of New Zealand Marsden Fund); SFB1182 Project C4 Deutsche Forschungsgemeinschaft (DFG)
Contributed Indexing: Keywords: horizontal gene transfer; microbial evolution; mobile elements; plant–microbe interactions
Substance Nomenclature: 0 (DNA Transposable Elements)
Entry Date(s): Date Created: 20240308 Date Completed: 20240311 Latest Revision: 20260917
Update Code: 20260917
PubMed Central ID: PMC10945833
DOI: 10.1073/pnas.2309263121
PMID: 38457521
Βάση Δεδομένων: MEDLINE
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  Data: Rapid dissemination of host metabolism-manipulating genes via integrative and conjugative elements.
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  Data: <searchLink fieldCode="AU" term="%22Colombi+E%22">Colombi E</searchLink>; School of Agriculture, Food and Ecosystem Sciences, Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia.<br /><searchLink fieldCode="AU" term="%22Bertels+F%22">Bertels F</searchLink>; Department of Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Plön 24306, Germany.<br /><searchLink fieldCode="AU" term="%22Doulcier+G%22">Doulcier G</searchLink>; Laboratoire Biophysique et Évolution, Institut Chemie Biologie Innovation, École Supérieure de Physique et de Chemie Industrielles de la Ville de Paris, Université Paris Science et Lettres, Centre National de al Reserche Scientifique, Paris 75005, France.<br /><searchLink fieldCode="AU" term="%22McConnell+E%22">McConnell E</searchLink>; Department of Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Plön 24306, Germany.<br /><searchLink fieldCode="AU" term="%22Pichugina+T%22">Pichugina T</searchLink>; Department of Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Plön 24306, Germany.<br /><searchLink fieldCode="AU" term="%22Sohn+KH%22">Sohn KH</searchLink>; Plant Immunity Research Center, Seoul National University, Seoul 08826, Republic of Korea.; Department of Agricultural Biotechnology, Seoul National University, Seoul 08826, Republic of Korea.; Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Republic of Korea.; Plant Genomics and Breeding Institute, Seoul National University, Seoul 08826, Republic of Korea.<br /><searchLink fieldCode="AU" term="%22Straub+C%22">Straub C</searchLink>; Health and Environment, Institute of Environmental Science and Research, Auckland 1025, New Zealand.; Division of Microbial Ecology, Center for Microbiology and Environmental Systems Science, University of Vienna, Vienna 1030, Austria.<br /><searchLink fieldCode="AU" term="%22McCann+HC%22">McCann HC</searchLink>; Plant Pathogen Evolution Research Group, Max Planck Institute for Biology, Tübingen 72076, Germany.<br /><searchLink fieldCode="AU" term="%22Rainey+PB%22">Rainey PB</searchLink>; Department of Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Plön 24306, Germany.; Laboratoire Biophysique et Évolution, Institut Chemie Biologie Innovation, École Supérieure de Physique et de Chemie Industrielles de la Ville de Paris, Université Paris Science et Lettres, Centre National de al Reserche Scientifique, Paris 75005, France.
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  Data: <searchLink fieldCode="JN" term="%227505876%22">Proceedings of the National Academy of Sciences of the United States of America</searchLink> [Proc Natl Acad Sci U S A] 2024 Mar 12; Vol. 121 (11), pp. e2309263121. <i>Date of Electronic Publication: </i>2024 Mar 08.
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  Data: <i>Original Publication</i>: Washington, DC : National Academy of Sciences
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  Data: <searchLink fieldCode="MM" term="%22Gene+Transfer%2C+Horizontal%22">Gene Transfer, Horizontal*</searchLink>/<searchLink fieldCode="MM" term="%22Gene+Transfer%2C+Horizontal+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Conjugation%2C+Genetic%22">Conjugation, Genetic*</searchLink><br /><searchLink fieldCode="MH" term="%22DNA+Transposable+Elements%22">DNA Transposable Elements</searchLink>/<searchLink fieldCode="MH" term="%22DNA+Transposable+Elements+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Phylogeny%22">Phylogeny</searchLink> ; <searchLink fieldCode="MH" term="%22Biological+Evolution%22">Biological Evolution</searchLink>
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  Data: Integrative and conjugative elements (ICEs) are self-transmissible mobile elements that transfer functional genetic units across broad phylogenetic distances. Accessory genes shuttled by ICEs can make significant contributions to bacterial fitness. Most ICEs characterized to date encode readily observable phenotypes contributing to symbiosis, pathogenicity, and antimicrobial resistance, yet the majority of ICEs carry genes of unknown function. Recent observations of rapid acquisition of ICEs in a pandemic lineage of Pseudomonas syringae pv. actinidae led to investigation of the structural and functional diversity of these elements. Fifty-three unique ICE types were identified across the P. syringae species complex. Together they form a distinct family of ICEs (PsICEs) that share a distant relationship to ICEs found in Pseudomonas aeruginosa. PsICEs are defined by conserved backbone genes punctuated by an array of accessory cargo genes, are highly recombinogenic, and display distinct evolutionary histories compared to their bacterial hosts. The most common cargo is a recently disseminated 16-kb mobile genetic element designated Tn6212. Deletion of Tn6212 did not alter pathogen growth in planta, but mutants displayed fitness defects when grown on tricarboxylic acid (TCA) cycle intermediates. RNA-seq analysis of a set of nested deletion mutants showed that a Tn6212-encoded LysR regulator has global effects on chromosomal gene expression. We show that Tn6212 responds to preferred carbon sources and manipulates bacterial metabolism to maximize growth.
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: Competing interests statement:The authors declare no competing interest.
– Name: Ref
  Label: References
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(PMID: <searchLink fieldCode="PM" term="%2228373865%22">28373865)</searchLink><br />BMC Genomics. 2017 Jan 5;18(1):36. (PMID: <searchLink fieldCode="PM" term="%2228056800%22">28056800)</searchLink><br />J Bacteriol. 2007 Mar;189(6):2443-59. (PMID: <searchLink fieldCode="PM" term="%2217194795%22">17194795)</searchLink><br />Nat Commun. 2018 Nov 30;9(1):5114. (PMID: <searchLink fieldCode="PM" term="%2230504855%22">30504855)</searchLink><br />Mol Biol Evol. 2013 Apr;30(4):772-80. (PMID: <searchLink fieldCode="PM" term="%2223329690%22">23329690)</searchLink><br />Nat Rev Microbiol. 2010 Aug;8(8):552-63. (PMID: <searchLink fieldCode="PM" term="%2220601965%22">20601965)</searchLink><br />PLoS Genet. 2011 Aug;7(8):e1002222. (PMID: <searchLink fieldCode="PM" term="%2221876676%22">21876676)</searchLink><br />Front Plant Sci. 2019 Apr 05;10:418. (PMID: <searchLink fieldCode="PM" term="%2231024592%22">31024592)</searchLink><br />Bioinformatics. 2015 Nov 15;31(22):3691-3. (PMID: <searchLink fieldCode="PM" term="%2226198102%22">26198102)</searchLink><br />Mol Plant Pathol. 2017 Jan;18(1):152-168. (PMID: <searchLink fieldCode="PM" term="%2227798954%22">27798954)</searchLink><br />Genome Biol. 2014;15(12):550. (PMID: <searchLink fieldCode="PM" term="%2225516281%22">25516281)</searchLink><br />ISME J. 2008 Mar;2(3):321-34. (PMID: <searchLink fieldCode="PM" term="%2218185595%22">18185595)</searchLink><br />PLoS Pathog. 2013;9(7):e1003503. (PMID: <searchLink fieldCode="PM" term="%2223935484%22">23935484)</searchLink><br />Mol Biol Evol. 2006 Feb;23(2):254-67. (PMID: <searchLink fieldCode="PM" term="%2216221896%22">16221896)</searchLink><br />Annu Rev Genet. 2015;49:577-601. (PMID: <searchLink fieldCode="PM" term="%2226473380%22">26473380)</searchLink><br />J Bacteriol. 2004 Dec;186(23):8114-22. (PMID: <searchLink fieldCode="PM" term="%2215547285%22">15547285)</searchLink><br />Mol Biol Evol. 2014 May;31(5):1077-88. (PMID: <searchLink fieldCode="PM" term="%2224600054%22">24600054)</searchLink><br />Environ Microbiol. 2014 Aug;16(8):2374-88. (PMID: <searchLink fieldCode="PM" term="%2224286439%22">24286439)</searchLink><br />Mol Biol Evol. 1987 Jul;4(4):406-25. (PMID: <searchLink fieldCode="PM" term="%223447015%22">3447015)</searchLink><br />Cell Mol Life Sci. 2020 Feb;77(3):395-413. (PMID: <searchLink fieldCode="PM" term="%2231768608%22">31768608)</searchLink><br />FEMS Microbiol Rev. 2017 Jul 1;41(4):512-537. (PMID: <searchLink fieldCode="PM" term="%2228369623%22">28369623)</searchLink><br />Plant Commun. 2021 Dec 28;3(2):100272. (PMID: <searchLink fieldCode="PM" term="%2235529946%22">35529946)</searchLink><br />Microb Genom. 2021 Oct;7(10):. (PMID: <searchLink fieldCode="PM" term="%2234605762%22">34605762)</searchLink><br />Sci Rep. 2017 Jun 15;7(1):3557. (PMID: <searchLink fieldCode="PM" term="%2228620210%22">28620210)</searchLink><br />Mol Biol Evol. 2019 May 1;36(5):1071-1085. (PMID: <searchLink fieldCode="PM" term="%2230835268%22">30835268)</searchLink><br />Nature. 1996 May 9;381(6578):169-72. (PMID: <searchLink fieldCode="PM" term="%228610017%22">8610017)</searchLink><br />Curr Biol. 2005 Dec 20;15(24):2230-5. (PMID: <searchLink fieldCode="PM" term="%2216360685%22">16360685)</searchLink><br />mBio. 2010 Jun 29;1(3):. (PMID: <searchLink fieldCode="PM" term="%2220802828%22">20802828)</searchLink><br />Theor Popul Biol. 2002 Jun;61(4):449-60. (PMID: <searchLink fieldCode="PM" term="%2212167364%22">12167364)</searchLink><br />Mol Microbiol. 2000 Oct;38(2):186-97. (PMID: <searchLink fieldCode="PM" term="%2211069647%22">11069647)</searchLink><br />Environ Microbiol. 2017 Feb;19(2):819-832. (PMID: <searchLink fieldCode="PM" term="%2228063194%22">28063194)</searchLink><br />Mol Biol Evol. 2004 Feb;21(2):255-65. (PMID: <searchLink fieldCode="PM" term="%2214660700%22">14660700)</searchLink><br />PLoS One. 2018 Apr 3;13(4):e0195332. (PMID: <searchLink fieldCode="PM" term="%2229614096%22">29614096)</searchLink><br />Nat Rev Microbiol. 2005 Sep;3(9):722-32. (PMID: <searchLink fieldCode="PM" term="%2216138100%22">16138100)</searchLink><br />PLoS One. 2008;3(11):e3647. (PMID: <searchLink fieldCode="PM" term="%2218985154%22">18985154)</searchLink><br />New Phytol. 2020 Feb;225(3):1327-1342. (PMID: <searchLink fieldCode="PM" term="%2231550400%22">31550400)</searchLink><br />Infect Genet Evol. 2007 Jan;7(1):84-92. (PMID: <searchLink fieldCode="PM" term="%2216807133%22">16807133)</searchLink><br />Mol Microbiol. 2018 Nov;110(3):444-454. (PMID: <searchLink fieldCode="PM" term="%2230152900%22">30152900)</searchLink><br />Appl Environ Microbiol. 2018 Jun 18;84(13):. (PMID: <searchLink fieldCode="PM" term="%2229654185%22">29654185)</searchLink><br />PLoS One. 2014 Sep 03;9(9):e105547. (PMID: <searchLink fieldCode="PM" term="%2225184292%22">25184292)</searchLink><br />PLoS Comput Biol. 2015 Feb 12;11(2):e1004041. (PMID: <searchLink fieldCode="PM" term="%2225675341%22">25675341)</searchLink><br />mBio. 2022 Nov 15;13(6):e0254122. (PMID: <searchLink fieldCode="PM" term="%2236377867%22">36377867)</searchLink><br />Bioinformatics. 2011 Feb 15;27(4):592-3. (PMID: <searchLink fieldCode="PM" term="%2221169378%22">21169378)</searchLink><br />PLoS One. 2013;8(2):e57464. (PMID: <searchLink fieldCode="PM" term="%2223555547%22">23555547)</searchLink><br />Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):11064-9. (PMID: <searchLink fieldCode="PM" term="%2216043691%22">16043691)</searchLink><br />Planta. 2019 Feb;249(2):305-318. (PMID: <searchLink fieldCode="PM" term="%2230267150%22">30267150)</searchLink><br />Plant Cell. 1991 Jan;3(1):49-59. (PMID: <searchLink fieldCode="PM" term="%221824334%22">1824334)</searchLink><br />Bioinformatics. 2011 Jun 1;27(11):1466-72. (PMID: <searchLink fieldCode="PM" term="%2221471011%22">21471011)</searchLink><br />J Mol Biol. 1990 Oct 5;215(3):403-10. (PMID: <searchLink fieldCode="PM" term="%222231712%22">2231712)</searchLink><br />Syst Biol. 2010 May;59(3):307-21. (PMID: <searchLink fieldCode="PM" term="%2220525638%22">20525638)</searchLink>
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  Data: MAU1709 Royal Society of New Zealand | Marsden Fund (Royal Society of New Zealand Marsden Fund); SFB1182 Project C4 Deutsche Forschungsgemeinschaft (DFG)
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  Data: <i>Keywords: </i>horizontal gene transfer; microbial evolution; mobile elements; plant–microbe interactions
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        Text: English
    PhysicalDescription:
      Pagination:
        StartPage: e2309263121
    Subjects:
      – SubjectFull: DNA Transposable Elements genetics
        Type: general
      – SubjectFull: Phylogeny
        Type: general
      – SubjectFull: Biological Evolution
        Type: general
      – SubjectFull: Gene Transfer, Horizontal genetics
        Type: general
      – SubjectFull: Conjugation, Genetic
        Type: general
    Titles:
      – TitleFull: Rapid dissemination of host metabolism-manipulating genes via integrative and conjugative elements.
        Type: main
  BibRelationships:
    HasContributorRelationships:
      – PersonEntity:
          Name:
            NameFull: Colombi E
      – PersonEntity:
          Name:
            NameFull: Bertels F
      – PersonEntity:
          Name:
            NameFull: Doulcier G
      – PersonEntity:
          Name:
            NameFull: McConnell E
      – PersonEntity:
          Name:
            NameFull: Pichugina T
      – PersonEntity:
          Name:
            NameFull: Sohn KH
      – PersonEntity:
          Name:
            NameFull: Straub C
      – PersonEntity:
          Name:
            NameFull: McCann HC
      – PersonEntity:
          Name:
            NameFull: Rainey PB
    IsPartOfRelationships:
      – BibEntity:
          Dates:
            – D: 12
              M: 03
              Text: 2024 Mar 12
              Type: published
              Y: 2024
          Identifiers:
            – Type: issn-electronic
              Value: 1091-6490
          Numbering:
            – Type: volume
              Value: 121
            – Type: issue
              Value: 11
          Titles:
            – TitleFull: Proceedings of the National Academy of Sciences of the United States of America
              Type: main
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