Cargando…
Isolation and Characterization of Shewanella Phage Thanatos Infecting and Lysing Shewanella oneidensis and Promoting Nascent Biofilm Formation
Species of the genus Shewanella are widespread in nature in various habitats, however, little is known about phages affecting Shewanella sp. Here, we report the isolation of phages from diverse freshwater environments that infect and lyse strains of Shewanella oneidensis and other Shewanella sp. Seq...
Autores principales: | , , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2020
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7530303/ https://www.ncbi.nlm.nih.gov/pubmed/33072035 http://dx.doi.org/10.3389/fmicb.2020.573260 |
_version_ | 1783589543904018432 |
---|---|
author | Kreienbaum, Maximilian Dörrich, Anja K. Brandt, David Schmid, Nicole E. Leonhard, Tabea Hager, Fabian Brenzinger, Susanne Hahn, Julia Glatter, Timo Ruwe, Matthias Briegel, Ariane Kalinowski, Jörn Thormann, Kai M. |
author_facet | Kreienbaum, Maximilian Dörrich, Anja K. Brandt, David Schmid, Nicole E. Leonhard, Tabea Hager, Fabian Brenzinger, Susanne Hahn, Julia Glatter, Timo Ruwe, Matthias Briegel, Ariane Kalinowski, Jörn Thormann, Kai M. |
author_sort | Kreienbaum, Maximilian |
collection | PubMed |
description | Species of the genus Shewanella are widespread in nature in various habitats, however, little is known about phages affecting Shewanella sp. Here, we report the isolation of phages from diverse freshwater environments that infect and lyse strains of Shewanella oneidensis and other Shewanella sp. Sequence analysis and microscopic imaging strongly indicate that these phages form a so far unclassified genus, now named Shewanella phage Thanatos, which can be positioned within the subfamily of Tevenvirinae (Duplodnaviria; Heunggongvirae; Uroviricota; Caudoviricetes; Caudovirales; Myoviridae; Tevenvirinae). We characterized one member of this group in more detail using S. oneidensis MR-1 as a host. Shewanella phage Thanatos-1 possesses a prolate icosahedral capsule of about 110 nm in height and 70 nm in width and a tail of about 95 nm in length. The dsDNA genome exhibits a GC content of about 34.5%, has a size of 160.6 kbp and encodes about 206 proteins (92 with an annotated putative function) and two tRNAs. Out of those 206, MS analyses identified about 155 phage proteins in PEG-precipitated samples of infected cells. Phage attachment likely requires the outer lipopolysaccharide of S. oneidensis, narrowing the phage’s host range. Under the applied conditions, about 20 novel phage particles per cell were produced after a latent period of approximately 40 min, which are stable at a pH range from 4 to 12 and resist temperatures up to 55°C for at least 24 h. Addition of Thanatos to S. oneidensis results in partial dissolution of established biofilms, however, early exposure of planktonic cells to Thanatos significantly enhances biofilm formation. Taken together, we identified a novel genus of Myophages affecting S. oneidensis communities in different ways. |
format | Online Article Text |
id | pubmed-7530303 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-75303032020-10-17 Isolation and Characterization of Shewanella Phage Thanatos Infecting and Lysing Shewanella oneidensis and Promoting Nascent Biofilm Formation Kreienbaum, Maximilian Dörrich, Anja K. Brandt, David Schmid, Nicole E. Leonhard, Tabea Hager, Fabian Brenzinger, Susanne Hahn, Julia Glatter, Timo Ruwe, Matthias Briegel, Ariane Kalinowski, Jörn Thormann, Kai M. Front Microbiol Microbiology Species of the genus Shewanella are widespread in nature in various habitats, however, little is known about phages affecting Shewanella sp. Here, we report the isolation of phages from diverse freshwater environments that infect and lyse strains of Shewanella oneidensis and other Shewanella sp. Sequence analysis and microscopic imaging strongly indicate that these phages form a so far unclassified genus, now named Shewanella phage Thanatos, which can be positioned within the subfamily of Tevenvirinae (Duplodnaviria; Heunggongvirae; Uroviricota; Caudoviricetes; Caudovirales; Myoviridae; Tevenvirinae). We characterized one member of this group in more detail using S. oneidensis MR-1 as a host. Shewanella phage Thanatos-1 possesses a prolate icosahedral capsule of about 110 nm in height and 70 nm in width and a tail of about 95 nm in length. The dsDNA genome exhibits a GC content of about 34.5%, has a size of 160.6 kbp and encodes about 206 proteins (92 with an annotated putative function) and two tRNAs. Out of those 206, MS analyses identified about 155 phage proteins in PEG-precipitated samples of infected cells. Phage attachment likely requires the outer lipopolysaccharide of S. oneidensis, narrowing the phage’s host range. Under the applied conditions, about 20 novel phage particles per cell were produced after a latent period of approximately 40 min, which are stable at a pH range from 4 to 12 and resist temperatures up to 55°C for at least 24 h. Addition of Thanatos to S. oneidensis results in partial dissolution of established biofilms, however, early exposure of planktonic cells to Thanatos significantly enhances biofilm formation. Taken together, we identified a novel genus of Myophages affecting S. oneidensis communities in different ways. Frontiers Media S.A. 2020-09-18 /pmc/articles/PMC7530303/ /pubmed/33072035 http://dx.doi.org/10.3389/fmicb.2020.573260 Text en Copyright © 2020 Kreienbaum, Dörrich, Brandt, Schmid, Leonhard, Hager, Brenzinger, Hahn, Glatter, Ruwe, Briegel, Kalinowski and Thormann. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Microbiology Kreienbaum, Maximilian Dörrich, Anja K. Brandt, David Schmid, Nicole E. Leonhard, Tabea Hager, Fabian Brenzinger, Susanne Hahn, Julia Glatter, Timo Ruwe, Matthias Briegel, Ariane Kalinowski, Jörn Thormann, Kai M. Isolation and Characterization of Shewanella Phage Thanatos Infecting and Lysing Shewanella oneidensis and Promoting Nascent Biofilm Formation |
title | Isolation and Characterization of Shewanella Phage Thanatos Infecting and Lysing Shewanella oneidensis and Promoting Nascent Biofilm Formation |
title_full | Isolation and Characterization of Shewanella Phage Thanatos Infecting and Lysing Shewanella oneidensis and Promoting Nascent Biofilm Formation |
title_fullStr | Isolation and Characterization of Shewanella Phage Thanatos Infecting and Lysing Shewanella oneidensis and Promoting Nascent Biofilm Formation |
title_full_unstemmed | Isolation and Characterization of Shewanella Phage Thanatos Infecting and Lysing Shewanella oneidensis and Promoting Nascent Biofilm Formation |
title_short | Isolation and Characterization of Shewanella Phage Thanatos Infecting and Lysing Shewanella oneidensis and Promoting Nascent Biofilm Formation |
title_sort | isolation and characterization of shewanella phage thanatos infecting and lysing shewanella oneidensis and promoting nascent biofilm formation |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7530303/ https://www.ncbi.nlm.nih.gov/pubmed/33072035 http://dx.doi.org/10.3389/fmicb.2020.573260 |
work_keys_str_mv | AT kreienbaummaximilian isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation AT dorrichanjak isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation AT brandtdavid isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation AT schmidnicolee isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation AT leonhardtabea isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation AT hagerfabian isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation AT brenzingersusanne isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation AT hahnjulia isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation AT glattertimo isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation AT ruwematthias isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation AT briegelariane isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation AT kalinowskijorn isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation AT thormannkaim isolationandcharacterizationofshewanellaphagethanatosinfectingandlysingshewanellaoneidensisandpromotingnascentbiofilmformation |