DNA Transport across the Outer and Inner Membranes of Naturally Transformable <named-content content-type="genus-species">Vibrio cholerae</named-content> Is Spatially but Not Temporally Coupled
ABSTRACT The physiological state of natural competence for transformation allows certain bacteria to take up free DNA from the environment and to recombine such newly acquired DNA into their chromosomes. However, even though conserved components that are required to undergo natural transformation ha...
| Main Authors: | , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2014-08-01
|
| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.01409-14 |
| _version_ | 1818434532096868352 |
|---|---|
| author | Patrick Seitz Melanie Blokesch |
| author_facet | Patrick Seitz Melanie Blokesch |
| author_sort | Patrick Seitz |
| collection | DOAJ |
| description | ABSTRACT The physiological state of natural competence for transformation allows certain bacteria to take up free DNA from the environment and to recombine such newly acquired DNA into their chromosomes. However, even though conserved components that are required to undergo natural transformation have been identified in several naturally competent bacteria, our knowledge of the underlying mechanisms of the DNA uptake process remains very limited. To better understand these mechanisms, we investigated the competence-mediated DNA transport in the naturally transformable pathogen Vibrio cholerae. Previously, we used a cell biology-based approach to experimentally address an existing hypothesis, which suggested the competence protein ComEA plays a role in the DNA uptake process across the outer membrane of Gram-negative bacteria. Here, we extended this knowledge by investigating the dynamics of DNA translocation across both membranes. More precisely, we indirectly visualized the transfer of the external DNA from outside the cell into the periplasm followed by the shuttling of the DNA into the cytoplasm. Based on these data, we conclude that for V. cholerae, the DNA translocation across the outer and inner membranes is spatially but not temporally coupled. IMPORTANCE As a mode of horizontal gene transfer, natural competence for transformation has contributed substantially to the plasticity of genomes and to bacterial evolution. Natural competence is often a tightly regulated process and is induced by diverse environmental cues. This is in contrast to the mechanistic aspects of the DNA translocation event, which are most likely conserved among naturally transformable bacteria. However, the DNA uptake process is still not well understood. We therefore investigated how external DNA reaches the cytosol of the naturally transformable bacterium V. cholerae. More specifically, we provide evidence that the DNA translocation across the membranes is spatially but not temporally coupled. We hypothesize that this model also applies to other competent Gram-negative bacteria and that our study contributes to the general understanding of this important biological process. |
| first_indexed | 2024-12-14T16:38:29Z |
| format | Article |
| id | doaj.art-1111b3ee8de64085a8784528d865d7e6 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-14T16:38:29Z |
| publishDate | 2014-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-1111b3ee8de64085a8784528d865d7e62022-12-21T22:54:22ZengAmerican Society for MicrobiologymBio2150-75112014-08-015410.1128/mBio.01409-14DNA Transport across the Outer and Inner Membranes of Naturally Transformable <named-content content-type="genus-species">Vibrio cholerae</named-content> Is Spatially but Not Temporally CoupledPatrick Seitz0Melanie Blokesch1Laboratory of Molecular Microbiology, Global Health Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, SwitzerlandLaboratory of Molecular Microbiology, Global Health Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, SwitzerlandABSTRACT The physiological state of natural competence for transformation allows certain bacteria to take up free DNA from the environment and to recombine such newly acquired DNA into their chromosomes. However, even though conserved components that are required to undergo natural transformation have been identified in several naturally competent bacteria, our knowledge of the underlying mechanisms of the DNA uptake process remains very limited. To better understand these mechanisms, we investigated the competence-mediated DNA transport in the naturally transformable pathogen Vibrio cholerae. Previously, we used a cell biology-based approach to experimentally address an existing hypothesis, which suggested the competence protein ComEA plays a role in the DNA uptake process across the outer membrane of Gram-negative bacteria. Here, we extended this knowledge by investigating the dynamics of DNA translocation across both membranes. More precisely, we indirectly visualized the transfer of the external DNA from outside the cell into the periplasm followed by the shuttling of the DNA into the cytoplasm. Based on these data, we conclude that for V. cholerae, the DNA translocation across the outer and inner membranes is spatially but not temporally coupled. IMPORTANCE As a mode of horizontal gene transfer, natural competence for transformation has contributed substantially to the plasticity of genomes and to bacterial evolution. Natural competence is often a tightly regulated process and is induced by diverse environmental cues. This is in contrast to the mechanistic aspects of the DNA translocation event, which are most likely conserved among naturally transformable bacteria. However, the DNA uptake process is still not well understood. We therefore investigated how external DNA reaches the cytosol of the naturally transformable bacterium V. cholerae. More specifically, we provide evidence that the DNA translocation across the membranes is spatially but not temporally coupled. We hypothesize that this model also applies to other competent Gram-negative bacteria and that our study contributes to the general understanding of this important biological process.https://journals.asm.org/doi/10.1128/mBio.01409-14 |
| spellingShingle | Patrick Seitz Melanie Blokesch DNA Transport across the Outer and Inner Membranes of Naturally Transformable <named-content content-type="genus-species">Vibrio cholerae</named-content> Is Spatially but Not Temporally Coupled mBio |
| title | DNA Transport across the Outer and Inner Membranes of Naturally Transformable <named-content content-type="genus-species">Vibrio cholerae</named-content> Is Spatially but Not Temporally Coupled |
| title_full | DNA Transport across the Outer and Inner Membranes of Naturally Transformable <named-content content-type="genus-species">Vibrio cholerae</named-content> Is Spatially but Not Temporally Coupled |
| title_fullStr | DNA Transport across the Outer and Inner Membranes of Naturally Transformable <named-content content-type="genus-species">Vibrio cholerae</named-content> Is Spatially but Not Temporally Coupled |
| title_full_unstemmed | DNA Transport across the Outer and Inner Membranes of Naturally Transformable <named-content content-type="genus-species">Vibrio cholerae</named-content> Is Spatially but Not Temporally Coupled |
| title_short | DNA Transport across the Outer and Inner Membranes of Naturally Transformable <named-content content-type="genus-species">Vibrio cholerae</named-content> Is Spatially but Not Temporally Coupled |
| title_sort | dna transport across the outer and inner membranes of naturally transformable named content content type genus species vibrio cholerae named content is spatially but not temporally coupled |
| url | https://journals.asm.org/doi/10.1128/mBio.01409-14 |
| work_keys_str_mv | AT patrickseitz dnatransportacrosstheouterandinnermembranesofnaturallytransformablenamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentisspatiallybutnottemporallycoupled AT melanieblokesch dnatransportacrosstheouterandinnermembranesofnaturallytransformablenamedcontentcontenttypegenusspeciesvibriocholeraenamedcontentisspatiallybutnottemporallycoupled |