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Prophage Activation Triggers Extracellular Synthesis of DNA in Bacterial Biofilms via Rolling Circle Replication.

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Τίτλος: Prophage Activation Triggers Extracellular Synthesis of DNA in Bacterial Biofilms via Rolling Circle Replication.
Συγγραφείς: Minero GAS; Interdisciplinary Nanoscience Center (iNANO), Aarhus University, Aarhus, Denmark.; Department of Biology, Aarhus University, Aarhus, Denmark., Mørkholt Lund L; Interdisciplinary Nanoscience Center (iNANO), Aarhus University, Aarhus, Denmark.; Department of Chemistry, Aarhus University, Aarhus, Denmark., Hyldgaard Klausen L; Interdisciplinary Nanoscience Center (iNANO), Aarhus University, Aarhus, Denmark.; Department of Chemistry, Aarhus University, Aarhus, Denmark.; Center of Electromicrobiology (CEM), Department of Biology, Aarhus University, Aarhus, Denmark., Ajunwa OM; Interdisciplinary Nanoscience Center (iNANO), Aarhus University, Aarhus, Denmark.; Center of Electromicrobiology (CEM), Department of Biology, Aarhus University, Aarhus, Denmark., Dong M; Interdisciplinary Nanoscience Center (iNANO), Aarhus University, Aarhus, Denmark.; Department of Chemistry, Aarhus University, Aarhus, Denmark.; Center of Electromicrobiology (CEM), Department of Biology, Aarhus University, Aarhus, Denmark., Meyer RL; Interdisciplinary Nanoscience Center (iNANO), Aarhus University, Aarhus, Denmark.; Department of Biology, Aarhus University, Aarhus, Denmark., Birkedal V; Interdisciplinary Nanoscience Center (iNANO), Aarhus University, Aarhus, Denmark.; Department of Chemistry, Aarhus University, Aarhus, Denmark., Thormann K; Institut für Mikrobiologie und Molekularbiologie, Justus-Liebig-Universität Gießen, Gießen, Germany.
Πηγή: Angewandte Chemie (International ed. in English) [Angew Chem Int Ed Engl] 2026 Oct 05; Vol. 65 (41), pp. e3695434. Date of Electronic Publication: 2026 Aug 24.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Wiley-VCH Country of Publication: Germany NLM ID: 0370543 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1521-3773 (Electronic) Linking ISSN: 14337851 NLM ISO Abbreviation: Angew Chem Int Ed Engl Subsets: MEDLINE
Imprint Name(s): Publication: <2004-> : Weinheim : Wiley-VCH
Original Publication: Weinheim/Bergstr. : New York, : Verlag Chemie ; Academic Press, c1962-
Ιατρικοί όροι (MeSH): Bacillus subtilis*/virology , Bacillus subtilis*/genetics , Bacillus subtilis*/physiology , Bacillus subtilis*/metabolism , Shewanella*/virology , Shewanella*/genetics , Shewanella*/physiology , Prophages*/physiology , DNA, Bacterial*/biosynthesis , Biofilms*, DNA Replication ; Extrachromosomal DNA ; G-Quadruplexes
Περίληψη: Extracellular DNA (eDNA) plays crucial roles in biofilm formation and function, yet the role of bacteriophages, which can exist in a dormant state as prophages, in controlling eDNA synthesis, structure, and activity remains obscure. Here, we demonstrate that prophages harbored by environmental bacteria can be exploited for synthesis of programmable eDNA superstructures with a distinct function. We designed a custom circular template and used it to direct rolling circle replication of G-quadruplex (GQ) motifs in Shewanella oneidensis and Bacillus subtilis. Under nutrient-limiting conditions, prophage activation and proliferation triggered cell lysis and subsequent eDNA synthesis, producing multimeric GQ concatemers that self-assembled into spherical (≤10 µm) and wire-like (>50 µm) superstructures in S. oneidensis and B. subtilis, respectively. Real-time monitoring using fluorescent reporter strains revealed that DNA synthesis occurred predominantly after bacterial lysis, coinciding with prophage replication. The resulting eDNA superstructures enhanced the electrochemical properties of S. oneidensis and exhibited peroxidase activity through GQ-hemin DNAzyme formation in S. oneidensis and B. subtilis cocultured biofilm. This work unveils a previously unknown mechanism by which prophages contribute to biofilm architecture and establishes a novel biotechnological platform for engineering functional DNA materials in living bacterial communities with potential applications in synthetic biology.
(© 2026 The Author(s). Angewandte Chemie International Edition published by Wiley‐VCH GmbH.)
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Grant Information: 00050284 Villum Foundation; 00069632 Villum Foundation; 2032-00294B Danish council for independent research; NNF20OC0061417 Novo Nordisk Foundation; CF20-0364 Carlsberg Foundation; 101086226-ENSIGN Horizon Europe Marie Skłodowska-Curie Actions; Center for Integrated Materials Research (Aarhus University)
Contributed Indexing: Keywords: Bacillus subtilis; DNA replication; G‐quadruplex deoxyribozyme; Shewanella oneidensis; bacterial lysis control; biofilm engineering; extracellular DNA synthesis; molecular machines; prophage; rolling circle replication
Substance Nomenclature: 0 (Extrachromosomal DNA)
0 (DNA, Bacterial)
SCR Organism: Shewanella oneidensis
Entry Date(s): Date Created: 20260825 Date Completed: 20261005 Latest Revision: 20261007
Update Code: 20261007
PubMed Central ID: PMC13638115
DOI: 10.1002/anie.3695434
PMID: 42638202
Βάση Δεδομένων: MEDLINE
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PubTypeId: academicJournal
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  Data: Prophage Activation Triggers Extracellular Synthesis of DNA in Bacterial Biofilms via Rolling Circle Replication.
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  Data: Extracellular DNA (eDNA) plays crucial roles in biofilm formation and function, yet the role of bacteriophages, which can exist in a dormant state as prophages, in controlling eDNA synthesis, structure, and activity remains obscure. Here, we demonstrate that prophages harbored by environmental bacteria can be exploited for synthesis of programmable eDNA superstructures with a distinct function. We designed a custom circular template and used it to direct rolling circle replication of G-quadruplex (GQ) motifs in Shewanella oneidensis and Bacillus subtilis. Under nutrient-limiting conditions, prophage activation and proliferation triggered cell lysis and subsequent eDNA synthesis, producing multimeric GQ concatemers that self-assembled into spherical (≤10&#160;&#181;m) and wire-like (&amp;gt;50&#160;&#181;m) superstructures in S. oneidensis and B. subtilis, respectively. Real-time monitoring using fluorescent reporter strains revealed that DNA synthesis occurred predominantly after bacterial lysis, coinciding with prophage replication. The resulting eDNA superstructures enhanced the electrochemical properties of S. oneidensis and exhibited peroxidase activity through GQ-hemin DNAzyme formation in S. oneidensis and B. subtilis cocultured biofilm. This work unveils a previously unknown mechanism by which prophages contribute to biofilm architecture and establishes a novel biotechnological platform for engineering functional DNA materials in living bacterial communities with potential applications in synthetic biology.&lt;br /&gt; (&#169; 2026 The Author(s). Angewandte Chemie International Edition published by Wiley‐VCH GmbH.)
– Name: Ref
  Label: References
  Group: RefInfo
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– Name: GrantInfo
  Label: Grant Information
  Group: Grant
  Data: 00050284 Villum Foundation; 00069632 Villum Foundation; 2032-00294B Danish council for independent research; NNF20OC0061417 Novo Nordisk Foundation; CF20-0364 Carlsberg Foundation; 101086226-ENSIGN Horizon Europe Marie Skłodowska-Curie Actions; Center for Integrated Materials Research (Aarhus University)
– Name: SubjectMinor
  Label: Contributed Indexing
  Group:
  Data: &lt;i&gt;Keywords: &lt;/i&gt;Bacillus subtilis; DNA replication; G‐quadruplex deoxyribozyme; Shewanella oneidensis; bacterial lysis control; biofilm engineering; extracellular DNA synthesis; molecular machines; prophage; rolling circle replication
– Name: NumberCAS
  Label: Substance Nomenclature
  Group: ID
  Data: 0 (Extrachromosomal DNA)&lt;br /&gt;0 (DNA, Bacterial)
– Name: SubjectOther
  Label: SCR Organism
  Group: Su
  Data: Shewanella oneidensis
– Name: DateEntry
  Label: Entry Date(s)
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  Data: &lt;i&gt;Date Created: &lt;/i&gt;20260825 &lt;i&gt;Date Completed: &lt;/i&gt;20261005 &lt;i&gt;Latest Revision: &lt;/i&gt;20261007
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  Label: Update Code
  Group: Date
  Data: 20261007
– Name: PubmedCentralID
  Label: PubMed Central ID
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  Data: PMC13638115
– Name: DOI
  Label: DOI
  Group: ID
  Data: 10.1002/anie.3695434
– Name: AN
  Label: PMID
  Group: ID
  Data: 42638202
PLink https://search.ebscohost.com/login.aspx?direct=true&site=eds-live&db=cmedm&AN=42638202
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  BibEntity:
    Identifiers:
      – Type: doi
        Value: 10.1002/anie.3695434
    Languages:
      – Code: eng
        Text: English
    PhysicalDescription:
      Pagination:
        StartPage: e3695434
    Subjects:
      – SubjectFull: DNA Replication
        Type: general
      – SubjectFull: Extrachromosomal DNA
        Type: general
      – SubjectFull: G-Quadruplexes
        Type: general
      – SubjectFull: Bacillus subtilis virology
        Type: general
      – SubjectFull: Bacillus subtilis genetics
        Type: general
      – SubjectFull: Bacillus subtilis physiology
        Type: general
      – SubjectFull: Bacillus subtilis metabolism
        Type: general
      – SubjectFull: Shewanella virology
        Type: general
      – SubjectFull: Shewanella genetics
        Type: general
      – SubjectFull: Shewanella physiology
        Type: general
      – SubjectFull: Prophages physiology
        Type: general
      – SubjectFull: DNA, Bacterial biosynthesis
        Type: general
      – SubjectFull: Biofilms
        Type: general
    Titles:
      – TitleFull: Prophage Activation Triggers Extracellular Synthesis of DNA in Bacterial Biofilms via Rolling Circle Replication.
        Type: main
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            NameFull: Minero GAS
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            NameFull: Mørkholt Lund L
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            NameFull: Hyldgaard Klausen L
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            NameFull: Thormann K
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          Dates:
            – D: 05
              M: 10
              Text: 2026 Oct 05
              Type: published
              Y: 2026
          Identifiers:
            – Type: issn-electronic
              Value: 1521-3773
          Numbering:
            – Type: volume
              Value: 65
            – Type: issue
              Value: 41
          Titles:
            – TitleFull: Angewandte Chemie (International ed. in English)
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