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Aggregation/dispersion transitions of T4 phage triggered by environmental ion availability

BACKGROUND: Bacteriophage survives in at least two extremes of ionic environments: bacterial host (high ionic-cytosol) and that of soil (low ionic-environmental water). The impact of ionic composition in the micro- and macro-environments has not so far been addressed in phage biology. RESULTS: Here,...

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Autores principales: Szermer-Olearnik, Bożena, Drab, Marek, Mąkosa, Mateusz, Zembala, Maria, Barbasz, Jakub, Dąbrowska, Krystyna, Boratyński, Janusz
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5404661/
https://www.ncbi.nlm.nih.gov/pubmed/28438164
http://dx.doi.org/10.1186/s12951-017-0266-5
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author Szermer-Olearnik, Bożena
Drab, Marek
Mąkosa, Mateusz
Zembala, Maria
Barbasz, Jakub
Dąbrowska, Krystyna
Boratyński, Janusz
author_facet Szermer-Olearnik, Bożena
Drab, Marek
Mąkosa, Mateusz
Zembala, Maria
Barbasz, Jakub
Dąbrowska, Krystyna
Boratyński, Janusz
author_sort Szermer-Olearnik, Bożena
collection PubMed
description BACKGROUND: Bacteriophage survives in at least two extremes of ionic environments: bacterial host (high ionic-cytosol) and that of soil (low ionic-environmental water). The impact of ionic composition in the micro- and macro-environments has not so far been addressed in phage biology. RESULTS: Here, we discovered a novel mechanism of aggregation/disaggregation transitions by phage virions. When normal sodium levels in phage media (150 mM) were lowered to 10 mM, advanced imaging by scanning electron microscopy, atomic force microscopy and dynamic light scattering all revealed formation of viral packages, each containing 20–100 virions. When ionic strength was returned from low to high, the aggregated state of phage reversed to a dispersed state, and the change in ionic strength did not substantially affect infectivity of the phage. By providing the direct evidence, that lowering of the sodium ion below the threshold of 20 mM causes rapid aggregation of phage while returning Na(+) concentration to the values above this threshold causes dispersion of phage, we identified a biophysical mechanism of phage aggregation. CONCLUSIONS: Our results implicate operation of group behavior in phage and suggest a new kind of quorum sensing among its virions that is mediated by ions. Loss of ionic strength may act as a trigger in an evolutionary mechanism to improve the survival of bacteriophage by stimulating aggregation of phage when outside a bacterial host. Reversal of phage aggregation is also a promising breakthrough in biotechnological applications, since we demonstrated here the ability to retain viable virion aggregates on standard micro-filters.
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spelling pubmed-54046612017-04-27 Aggregation/dispersion transitions of T4 phage triggered by environmental ion availability Szermer-Olearnik, Bożena Drab, Marek Mąkosa, Mateusz Zembala, Maria Barbasz, Jakub Dąbrowska, Krystyna Boratyński, Janusz J Nanobiotechnology Research BACKGROUND: Bacteriophage survives in at least two extremes of ionic environments: bacterial host (high ionic-cytosol) and that of soil (low ionic-environmental water). The impact of ionic composition in the micro- and macro-environments has not so far been addressed in phage biology. RESULTS: Here, we discovered a novel mechanism of aggregation/disaggregation transitions by phage virions. When normal sodium levels in phage media (150 mM) were lowered to 10 mM, advanced imaging by scanning electron microscopy, atomic force microscopy and dynamic light scattering all revealed formation of viral packages, each containing 20–100 virions. When ionic strength was returned from low to high, the aggregated state of phage reversed to a dispersed state, and the change in ionic strength did not substantially affect infectivity of the phage. By providing the direct evidence, that lowering of the sodium ion below the threshold of 20 mM causes rapid aggregation of phage while returning Na(+) concentration to the values above this threshold causes dispersion of phage, we identified a biophysical mechanism of phage aggregation. CONCLUSIONS: Our results implicate operation of group behavior in phage and suggest a new kind of quorum sensing among its virions that is mediated by ions. Loss of ionic strength may act as a trigger in an evolutionary mechanism to improve the survival of bacteriophage by stimulating aggregation of phage when outside a bacterial host. Reversal of phage aggregation is also a promising breakthrough in biotechnological applications, since we demonstrated here the ability to retain viable virion aggregates on standard micro-filters. BioMed Central 2017-04-24 /pmc/articles/PMC5404661/ /pubmed/28438164 http://dx.doi.org/10.1186/s12951-017-0266-5 Text en © The Author(s) 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Szermer-Olearnik, Bożena
Drab, Marek
Mąkosa, Mateusz
Zembala, Maria
Barbasz, Jakub
Dąbrowska, Krystyna
Boratyński, Janusz
Aggregation/dispersion transitions of T4 phage triggered by environmental ion availability
title Aggregation/dispersion transitions of T4 phage triggered by environmental ion availability
title_full Aggregation/dispersion transitions of T4 phage triggered by environmental ion availability
title_fullStr Aggregation/dispersion transitions of T4 phage triggered by environmental ion availability
title_full_unstemmed Aggregation/dispersion transitions of T4 phage triggered by environmental ion availability
title_short Aggregation/dispersion transitions of T4 phage triggered by environmental ion availability
title_sort aggregation/dispersion transitions of t4 phage triggered by environmental ion availability
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5404661/
https://www.ncbi.nlm.nih.gov/pubmed/28438164
http://dx.doi.org/10.1186/s12951-017-0266-5
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