Cargando…

Mobility of extracellular DNA within gonococcal colonies

Transformation enables bacteria to acquire genetic information from extracellular DNA (eDNA). Close proximity between bacteria in colonies and biofilms may inhibit escape of eDNA from the colony but it also hinders its diffusion between donor and recipient. In this study, we investigate the mobility...

Descripción completa

Detalles Bibliográficos
Autores principales: Bender, Niklas, Hennes, Marc, Maier, Berenike
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9136125/
https://www.ncbi.nlm.nih.gov/pubmed/35647521
http://dx.doi.org/10.1016/j.bioflm.2022.100078
_version_ 1784714108311961600
author Bender, Niklas
Hennes, Marc
Maier, Berenike
author_facet Bender, Niklas
Hennes, Marc
Maier, Berenike
author_sort Bender, Niklas
collection PubMed
description Transformation enables bacteria to acquire genetic information from extracellular DNA (eDNA). Close proximity between bacteria in colonies and biofilms may inhibit escape of eDNA from the colony but it also hinders its diffusion between donor and recipient. In this study, we investigate the mobility of DNA within colonies formed by Neisseria gonorrhoeae, and relate it to transformation efficiency. We characterize the penetration dynamics of fluorescent DNA into the colony at a time scale of hours and find that 300 bp fragments diffuse through the colony without hindrance. For DNA length exceeding 3 kbp, a concentration gradient between the edge and the center of the colony develops, indicating hindered diffusion. Accumulation of DNA within the colony increases with increasing DNA length. The presence of the gonococcal DNA uptake sequence (DUS), which mediates specific binding to type 4 pili (T4P) and uptake into the cell, steepens the radial concentration gradient within the colony, suggesting that the DUS reduces DNA mobility. In particular, DNA of N. gonorrhoeae containing multiple DUS is trapped at the periphery. Under conditions, where DUS containing DNA fragments readily enter the colony center, we investigate the efficiency of transformation. We show that despite rapid diffusion of DNA, the transformation is limited to the edge of young colonies. We conclude that DNA mobility depends on DNA length and specific binding mediated by the DUS, resulting in restricted mobility of gonococcal DNA. Yet gonococcal colonies accumulate DNA, and may therefore act as a reservoir for eDNA.
format Online
Article
Text
id pubmed-9136125
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Elsevier
record_format MEDLINE/PubMed
spelling pubmed-91361252022-05-28 Mobility of extracellular DNA within gonococcal colonies Bender, Niklas Hennes, Marc Maier, Berenike Biofilm Article Transformation enables bacteria to acquire genetic information from extracellular DNA (eDNA). Close proximity between bacteria in colonies and biofilms may inhibit escape of eDNA from the colony but it also hinders its diffusion between donor and recipient. In this study, we investigate the mobility of DNA within colonies formed by Neisseria gonorrhoeae, and relate it to transformation efficiency. We characterize the penetration dynamics of fluorescent DNA into the colony at a time scale of hours and find that 300 bp fragments diffuse through the colony without hindrance. For DNA length exceeding 3 kbp, a concentration gradient between the edge and the center of the colony develops, indicating hindered diffusion. Accumulation of DNA within the colony increases with increasing DNA length. The presence of the gonococcal DNA uptake sequence (DUS), which mediates specific binding to type 4 pili (T4P) and uptake into the cell, steepens the radial concentration gradient within the colony, suggesting that the DUS reduces DNA mobility. In particular, DNA of N. gonorrhoeae containing multiple DUS is trapped at the periphery. Under conditions, where DUS containing DNA fragments readily enter the colony center, we investigate the efficiency of transformation. We show that despite rapid diffusion of DNA, the transformation is limited to the edge of young colonies. We conclude that DNA mobility depends on DNA length and specific binding mediated by the DUS, resulting in restricted mobility of gonococcal DNA. Yet gonococcal colonies accumulate DNA, and may therefore act as a reservoir for eDNA. Elsevier 2022-05-20 /pmc/articles/PMC9136125/ /pubmed/35647521 http://dx.doi.org/10.1016/j.bioflm.2022.100078 Text en © 2022 The Authors https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Bender, Niklas
Hennes, Marc
Maier, Berenike
Mobility of extracellular DNA within gonococcal colonies
title Mobility of extracellular DNA within gonococcal colonies
title_full Mobility of extracellular DNA within gonococcal colonies
title_fullStr Mobility of extracellular DNA within gonococcal colonies
title_full_unstemmed Mobility of extracellular DNA within gonococcal colonies
title_short Mobility of extracellular DNA within gonococcal colonies
title_sort mobility of extracellular dna within gonococcal colonies
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9136125/
https://www.ncbi.nlm.nih.gov/pubmed/35647521
http://dx.doi.org/10.1016/j.bioflm.2022.100078
work_keys_str_mv AT benderniklas mobilityofextracellulardnawithingonococcalcolonies
AT hennesmarc mobilityofextracellulardnawithingonococcalcolonies
AT maierberenike mobilityofextracellulardnawithingonococcalcolonies