The Type IV Pilus of Plasmid TP114 Displays Adhesins Conferring Conjugation Specificity and Is Important for DNA Transfer in the Mouse Gut Microbiota
ABSTRACT Type IV pili (T4P) are common bacterial surface appendages involved in different biological processes such as adherence, motility, competence, pathogenesis, and conjugation. In this work, we describe the T4P of TP114, an IncI2 enterobacterial conjugative plasmid recently shown to disseminat...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2022-04-01
|
| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02303-21 |
| _version_ | 1817979246644035584 |
|---|---|
| author | Nancy Allard Kevin Neil Frédéric Grenier Sébastien Rodrigue |
| author_facet | Nancy Allard Kevin Neil Frédéric Grenier Sébastien Rodrigue |
| author_sort | Nancy Allard |
| collection | DOAJ |
| description | ABSTRACT Type IV pili (T4P) are common bacterial surface appendages involved in different biological processes such as adherence, motility, competence, pathogenesis, and conjugation. In this work, we describe the T4P of TP114, an IncI2 enterobacterial conjugative plasmid recently shown to disseminate at high rates in the mouse intestinal tract. This pilus is composed of the major PilS and minor PilV pilins that are both important for conjugation in broth and in the gut microbiota but not on a solid support. The PilV-coding sequence is part of a shufflon and can bear different C-terminal domains. The shufflon is a multiple DNA inversion system containing many DNA cassettes flanked by recombination sites that are recognized by a shufflon-specific tyrosine recombinase (shufflase) promoting the recombination between DNA segments. The different PilV variants act as adhesins that can modify the affinity for different recipient bacteria. Eight PilV variants were identified in TP114, including one that has not been described in other shufflons. All PilV variants allowed conjugative transfer with different recipient Escherichia coli strains. We conclude that the T4P carried by TP114 plays a major role in mating pair stabilization in broth as well as in the gut microbiota and that the shufflon acts as a biological switch modifying the conjugative host range specificity. IMPORTANCE Conjugative plasmids are involved in horizontal gene transfer in the gut microbiota, which constitutes an important antibiotic resistance gene reservoir. However, the molecular mechanisms used by conjugative plasmids to select recipient bacteria and transfer at high rates in the mouse gut microbiota remain poorly characterized. We studied the type IV pilus carried by TP114 and demonstrated that the minor pilin PilV acts as an adhesin that can efficiently select target cells for conjugative transfer. Moreover, the pilV gene can be rapidly modified by a shufflon, hence modulating the nature of the recipient bacteria during conjugation. Our study highlights the role of mating pair stabilization for conjugation in broth as well as in the gut microbiome and explains how the host spectrum of a plasmid can be expanded simply by remodeling the PilV adhesin. |
| first_indexed | 2024-04-13T22:40:27Z |
| format | Article |
| id | doaj.art-db90ddd4291f42ada6057ec619510554 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-13T22:40:27Z |
| publishDate | 2022-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-db90ddd4291f42ada6057ec6195105542022-12-22T02:26:38ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-04-0110210.1128/spectrum.02303-21The Type IV Pilus of Plasmid TP114 Displays Adhesins Conferring Conjugation Specificity and Is Important for DNA Transfer in the Mouse Gut MicrobiotaNancy Allard0Kevin Neil1Frédéric Grenier2Sébastien Rodrigue3Département de biologie, Faculté des sciences, Université de Sherbrooke, Sherbrooke, Quebec, CanadaDépartement de biologie, Faculté des sciences, Université de Sherbrooke, Sherbrooke, Quebec, CanadaDépartement de biologie, Faculté des sciences, Université de Sherbrooke, Sherbrooke, Quebec, CanadaDépartement de biologie, Faculté des sciences, Université de Sherbrooke, Sherbrooke, Quebec, CanadaABSTRACT Type IV pili (T4P) are common bacterial surface appendages involved in different biological processes such as adherence, motility, competence, pathogenesis, and conjugation. In this work, we describe the T4P of TP114, an IncI2 enterobacterial conjugative plasmid recently shown to disseminate at high rates in the mouse intestinal tract. This pilus is composed of the major PilS and minor PilV pilins that are both important for conjugation in broth and in the gut microbiota but not on a solid support. The PilV-coding sequence is part of a shufflon and can bear different C-terminal domains. The shufflon is a multiple DNA inversion system containing many DNA cassettes flanked by recombination sites that are recognized by a shufflon-specific tyrosine recombinase (shufflase) promoting the recombination between DNA segments. The different PilV variants act as adhesins that can modify the affinity for different recipient bacteria. Eight PilV variants were identified in TP114, including one that has not been described in other shufflons. All PilV variants allowed conjugative transfer with different recipient Escherichia coli strains. We conclude that the T4P carried by TP114 plays a major role in mating pair stabilization in broth as well as in the gut microbiota and that the shufflon acts as a biological switch modifying the conjugative host range specificity. IMPORTANCE Conjugative plasmids are involved in horizontal gene transfer in the gut microbiota, which constitutes an important antibiotic resistance gene reservoir. However, the molecular mechanisms used by conjugative plasmids to select recipient bacteria and transfer at high rates in the mouse gut microbiota remain poorly characterized. We studied the type IV pilus carried by TP114 and demonstrated that the minor pilin PilV acts as an adhesin that can efficiently select target cells for conjugative transfer. Moreover, the pilV gene can be rapidly modified by a shufflon, hence modulating the nature of the recipient bacteria during conjugation. Our study highlights the role of mating pair stabilization for conjugation in broth as well as in the gut microbiome and explains how the host spectrum of a plasmid can be expanded simply by remodeling the PilV adhesin.https://journals.asm.org/doi/10.1128/spectrum.02303-21conjugative plasmidtype IV pilusshufflonmicrobiota |
| spellingShingle | Nancy Allard Kevin Neil Frédéric Grenier Sébastien Rodrigue The Type IV Pilus of Plasmid TP114 Displays Adhesins Conferring Conjugation Specificity and Is Important for DNA Transfer in the Mouse Gut Microbiota Microbiology Spectrum conjugative plasmid type IV pilus shufflon microbiota |
| title | The Type IV Pilus of Plasmid TP114 Displays Adhesins Conferring Conjugation Specificity and Is Important for DNA Transfer in the Mouse Gut Microbiota |
| title_full | The Type IV Pilus of Plasmid TP114 Displays Adhesins Conferring Conjugation Specificity and Is Important for DNA Transfer in the Mouse Gut Microbiota |
| title_fullStr | The Type IV Pilus of Plasmid TP114 Displays Adhesins Conferring Conjugation Specificity and Is Important for DNA Transfer in the Mouse Gut Microbiota |
| title_full_unstemmed | The Type IV Pilus of Plasmid TP114 Displays Adhesins Conferring Conjugation Specificity and Is Important for DNA Transfer in the Mouse Gut Microbiota |
| title_short | The Type IV Pilus of Plasmid TP114 Displays Adhesins Conferring Conjugation Specificity and Is Important for DNA Transfer in the Mouse Gut Microbiota |
| title_sort | type iv pilus of plasmid tp114 displays adhesins conferring conjugation specificity and is important for dna transfer in the mouse gut microbiota |
| topic | conjugative plasmid type IV pilus shufflon microbiota |
| url | https://journals.asm.org/doi/10.1128/spectrum.02303-21 |
| work_keys_str_mv | AT nancyallard thetypeivpilusofplasmidtp114displaysadhesinsconferringconjugationspecificityandisimportantfordnatransferinthemousegutmicrobiota AT kevinneil thetypeivpilusofplasmidtp114displaysadhesinsconferringconjugationspecificityandisimportantfordnatransferinthemousegutmicrobiota AT fredericgrenier thetypeivpilusofplasmidtp114displaysadhesinsconferringconjugationspecificityandisimportantfordnatransferinthemousegutmicrobiota AT sebastienrodrigue thetypeivpilusofplasmidtp114displaysadhesinsconferringconjugationspecificityandisimportantfordnatransferinthemousegutmicrobiota AT nancyallard typeivpilusofplasmidtp114displaysadhesinsconferringconjugationspecificityandisimportantfordnatransferinthemousegutmicrobiota AT kevinneil typeivpilusofplasmidtp114displaysadhesinsconferringconjugationspecificityandisimportantfordnatransferinthemousegutmicrobiota AT fredericgrenier typeivpilusofplasmidtp114displaysadhesinsconferringconjugationspecificityandisimportantfordnatransferinthemousegutmicrobiota AT sebastienrodrigue typeivpilusofplasmidtp114displaysadhesinsconferringconjugationspecificityandisimportantfordnatransferinthemousegutmicrobiota |