Extracellular Vesicles From Xylella fastidiosa Carry sRNAs and Genomic Islands, Suggesting Roles in Recipient Cells
ABSTRACT Xylella fastidiosa (Xf) is a Gram‐negative bacterial plant pathogen responsible for severe diseases in a variety of economically important crops. A critical aspect of its virulence is the production of extracellular vesicles (EVs). In this study, we discovered that DNA‐binding proteins and...
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| Format: | Article |
| Language: | English |
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Wiley
2025-06-01
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| Series: | Journal of Extracellular Vesicles |
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| Online Access: | https://doi.org/10.1002/jev2.70102 |
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| author | Alessa Ruf Patrick Blumenkamp Christina Ludwig Anne Lippegaus Andreas Brachmann Andreas Klingl Alexander Goesmann Karina Brinkrolf Kai Papenfort Silke Robatzek |
| author_facet | Alessa Ruf Patrick Blumenkamp Christina Ludwig Anne Lippegaus Andreas Brachmann Andreas Klingl Alexander Goesmann Karina Brinkrolf Kai Papenfort Silke Robatzek |
| author_sort | Alessa Ruf |
| collection | DOAJ |
| description | ABSTRACT Xylella fastidiosa (Xf) is a Gram‐negative bacterial plant pathogen responsible for severe diseases in a variety of economically important crops. A critical aspect of its virulence is the production of extracellular vesicles (EVs). In this study, we discovered that DNA‐binding proteins and nonribosomal RNA‐binding proteins are abundant in the corona of Xf‐EVs. DNA‐seq revealed enrichment of three genomic islands (GIs) in EVs, which carry molecular signatures indicative of horizontal gene transfer (HGT). The most abundant GI encodes five homologous small RNAs designated sXFs. RNA sequencing revealed a distinct pattern of noncoding RNAs enriched in EVs, including four island‐encoded sXFs. One of the sXF’s stem‐loops contains motifs for binding the RNA chaperone Hfq, which is also abundant in EVs. Predicted target analysis suggests that sXFs play a role in regulation of natural competence in bacteria. Additionally, sXF plant target prediction identifies a coiled‐coil nucleotide‐binding domain leucine‐rich repeat receptor (CNL) immune gene that is downregulated following Xf infection and Xf‐EV treatment. We propose a model where Xf releases nucleic acid carrying EVs with two functions: one to deliver RNA‐related cargo that regulates gene expression in both bacterial and plant cells, and another to deliver DNA‐related cargo for the genetic transfer of genomic islands. We highlight island‐encoded sXFs as potential virulence factors and vesiduction as a mechanism of HGT of sXFs in Xf. Taken together, our data on Xf‐EV cargoes provide a molecular framework for understanding the virulence of Xf. |
| format | Article |
| id | doaj-art-6fcb43bc55d147389ff6d86f3eeddfaf |
| institution | DOAJ |
| issn | 2001-3078 |
| language | English |
| publishDate | 2025-06-01 |
| publisher | Wiley |
| record_format | Article |
| series | Journal of Extracellular Vesicles |
| spelling | doaj-art-6fcb43bc55d147389ff6d86f3eeddfaf2025-08-20T02:48:54ZengWileyJournal of Extracellular Vesicles2001-30782025-06-01146n/an/a10.1002/jev2.70102Extracellular Vesicles From Xylella fastidiosa Carry sRNAs and Genomic Islands, Suggesting Roles in Recipient CellsAlessa Ruf0Patrick Blumenkamp1Christina Ludwig2Anne Lippegaus3Andreas Brachmann4Andreas Klingl5Alexander Goesmann6Karina Brinkrolf7Kai Papenfort8Silke Robatzek9LMU Munich Biocenter Ludwig‐Maximilian‐University of Munich Martinsried GermanyBioinformatics and Systems Biology Justus Liebig University Giessen Giessen GermanyBavarian Center for Biomolecular Mass Spectrometry (BayBioMS) TUM School of Life Sciences Freising GermanyBioinstrumentezentrum Friedrich‐ Schiller University Institute of Microbiology Jena GermanyLMU Munich Biocenter Ludwig‐Maximilian‐University of Munich Martinsried GermanyLMU Munich Biocenter Ludwig‐Maximilian‐University of Munich Martinsried GermanyBioinformatics and Systems Biology Justus Liebig University Giessen Giessen GermanyBioinformatics and Systems Biology Justus Liebig University Giessen Giessen GermanyBioinstrumentezentrum Friedrich‐ Schiller University Institute of Microbiology Jena GermanyLMU Munich Biocenter Ludwig‐Maximilian‐University of Munich Martinsried GermanyABSTRACT Xylella fastidiosa (Xf) is a Gram‐negative bacterial plant pathogen responsible for severe diseases in a variety of economically important crops. A critical aspect of its virulence is the production of extracellular vesicles (EVs). In this study, we discovered that DNA‐binding proteins and nonribosomal RNA‐binding proteins are abundant in the corona of Xf‐EVs. DNA‐seq revealed enrichment of three genomic islands (GIs) in EVs, which carry molecular signatures indicative of horizontal gene transfer (HGT). The most abundant GI encodes five homologous small RNAs designated sXFs. RNA sequencing revealed a distinct pattern of noncoding RNAs enriched in EVs, including four island‐encoded sXFs. One of the sXF’s stem‐loops contains motifs for binding the RNA chaperone Hfq, which is also abundant in EVs. Predicted target analysis suggests that sXFs play a role in regulation of natural competence in bacteria. Additionally, sXF plant target prediction identifies a coiled‐coil nucleotide‐binding domain leucine‐rich repeat receptor (CNL) immune gene that is downregulated following Xf infection and Xf‐EV treatment. We propose a model where Xf releases nucleic acid carrying EVs with two functions: one to deliver RNA‐related cargo that regulates gene expression in both bacterial and plant cells, and another to deliver DNA‐related cargo for the genetic transfer of genomic islands. We highlight island‐encoded sXFs as potential virulence factors and vesiduction as a mechanism of HGT of sXFs in Xf. Taken together, our data on Xf‐EV cargoes provide a molecular framework for understanding the virulence of Xf.https://doi.org/10.1002/jev2.70102EVsgenomic islandsHfqhorizontal gene transfersmall noncoding RNAs |
| spellingShingle | Alessa Ruf Patrick Blumenkamp Christina Ludwig Anne Lippegaus Andreas Brachmann Andreas Klingl Alexander Goesmann Karina Brinkrolf Kai Papenfort Silke Robatzek Extracellular Vesicles From Xylella fastidiosa Carry sRNAs and Genomic Islands, Suggesting Roles in Recipient Cells Journal of Extracellular Vesicles EVs genomic islands Hfq horizontal gene transfer small noncoding RNAs |
| title | Extracellular Vesicles From Xylella fastidiosa Carry sRNAs and Genomic Islands, Suggesting Roles in Recipient Cells |
| title_full | Extracellular Vesicles From Xylella fastidiosa Carry sRNAs and Genomic Islands, Suggesting Roles in Recipient Cells |
| title_fullStr | Extracellular Vesicles From Xylella fastidiosa Carry sRNAs and Genomic Islands, Suggesting Roles in Recipient Cells |
| title_full_unstemmed | Extracellular Vesicles From Xylella fastidiosa Carry sRNAs and Genomic Islands, Suggesting Roles in Recipient Cells |
| title_short | Extracellular Vesicles From Xylella fastidiosa Carry sRNAs and Genomic Islands, Suggesting Roles in Recipient Cells |
| title_sort | extracellular vesicles from xylella fastidiosa carry srnas and genomic islands suggesting roles in recipient cells |
| topic | EVs genomic islands Hfq horizontal gene transfer small noncoding RNAs |
| url | https://doi.org/10.1002/jev2.70102 |
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