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Geochemical constraints on bacteriophage infectivity in terrestrial environments

Lytic phages can be potent and selective inhibitors of microbial growth and can have profound impacts on microbiome composition and function. However, there is uncertainty about the biogeochemical conditions under which phage predation modulates microbial ecosystem function, particularly in terrestr...

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Autores principales: Carlson, Hans K., Piya, Denish, Moore, Madeline L., Magar, Roniya T., Elisabeth, Nathalie H., Deutschbauer, Adam M., Arkin, Adam P., Mutalik, Vivek K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10439110/
https://www.ncbi.nlm.nih.gov/pubmed/37596312
http://dx.doi.org/10.1038/s43705-023-00297-7
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author Carlson, Hans K.
Piya, Denish
Moore, Madeline L.
Magar, Roniya T.
Elisabeth, Nathalie H.
Deutschbauer, Adam M.
Arkin, Adam P.
Mutalik, Vivek K.
author_facet Carlson, Hans K.
Piya, Denish
Moore, Madeline L.
Magar, Roniya T.
Elisabeth, Nathalie H.
Deutschbauer, Adam M.
Arkin, Adam P.
Mutalik, Vivek K.
author_sort Carlson, Hans K.
collection PubMed
description Lytic phages can be potent and selective inhibitors of microbial growth and can have profound impacts on microbiome composition and function. However, there is uncertainty about the biogeochemical conditions under which phage predation modulates microbial ecosystem function, particularly in terrestrial systems. Ionic strength is critical for infection of bacteria by many phages, but quantitative data is limited on the ion thresholds for phage infection that can be compared with environmental ion concentrations. Similarly, while carbon composition varies in the environment, we do not know how this variability influences the impact of phage predation on microbiome function. Here, we measured the half-maximal effective concentrations (EC(50)) of 80 different inorganic ions for the infection of E. coli with two canonical dsDNA and ssRNA phages, T4 and MS2, respectively. Many alkaline earth metals and alkali metals enabled lytic infection but the ionic strength thresholds varied for different ions between phages. Additionally, using a freshwater nitrate-reducing microbiome, we found that the ability of lytic phages to influence nitrate reduction end-products depended upon the carbon source as well as ionic strength. For all phage:host pairs, the ion EC(50)s for phage infection exceeded the ion concentrations found in many terrestrial freshwater systems. Thus, our findings support a model where phages most influence terrestrial microbial functional ecology in hot spots and hot moments such as metazoan guts, drought influenced soils, or biofilms where ion concentration is locally or transiently elevated and nutrients are available to support the growth of specific phage hosts.
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spelling pubmed-104391102023-08-20 Geochemical constraints on bacteriophage infectivity in terrestrial environments Carlson, Hans K. Piya, Denish Moore, Madeline L. Magar, Roniya T. Elisabeth, Nathalie H. Deutschbauer, Adam M. Arkin, Adam P. Mutalik, Vivek K. ISME Commun Article Lytic phages can be potent and selective inhibitors of microbial growth and can have profound impacts on microbiome composition and function. However, there is uncertainty about the biogeochemical conditions under which phage predation modulates microbial ecosystem function, particularly in terrestrial systems. Ionic strength is critical for infection of bacteria by many phages, but quantitative data is limited on the ion thresholds for phage infection that can be compared with environmental ion concentrations. Similarly, while carbon composition varies in the environment, we do not know how this variability influences the impact of phage predation on microbiome function. Here, we measured the half-maximal effective concentrations (EC(50)) of 80 different inorganic ions for the infection of E. coli with two canonical dsDNA and ssRNA phages, T4 and MS2, respectively. Many alkaline earth metals and alkali metals enabled lytic infection but the ionic strength thresholds varied for different ions between phages. Additionally, using a freshwater nitrate-reducing microbiome, we found that the ability of lytic phages to influence nitrate reduction end-products depended upon the carbon source as well as ionic strength. For all phage:host pairs, the ion EC(50)s for phage infection exceeded the ion concentrations found in many terrestrial freshwater systems. Thus, our findings support a model where phages most influence terrestrial microbial functional ecology in hot spots and hot moments such as metazoan guts, drought influenced soils, or biofilms where ion concentration is locally or transiently elevated and nutrients are available to support the growth of specific phage hosts. Nature Publishing Group UK 2023-08-18 /pmc/articles/PMC10439110/ /pubmed/37596312 http://dx.doi.org/10.1038/s43705-023-00297-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Carlson, Hans K.
Piya, Denish
Moore, Madeline L.
Magar, Roniya T.
Elisabeth, Nathalie H.
Deutschbauer, Adam M.
Arkin, Adam P.
Mutalik, Vivek K.
Geochemical constraints on bacteriophage infectivity in terrestrial environments
title Geochemical constraints on bacteriophage infectivity in terrestrial environments
title_full Geochemical constraints on bacteriophage infectivity in terrestrial environments
title_fullStr Geochemical constraints on bacteriophage infectivity in terrestrial environments
title_full_unstemmed Geochemical constraints on bacteriophage infectivity in terrestrial environments
title_short Geochemical constraints on bacteriophage infectivity in terrestrial environments
title_sort geochemical constraints on bacteriophage infectivity in terrestrial environments
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10439110/
https://www.ncbi.nlm.nih.gov/pubmed/37596312
http://dx.doi.org/10.1038/s43705-023-00297-7
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