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DNA uptake from a laboratory environment drives unexpected adaptation of a thermophile to a minor medium component

DNA uptake is widespread among microorganisms and considered a strategy for rapid adaptation to new conditions. While both DNA uptake and adaptation are referred to in the context of natural environments, they are often studied in laboratories under defined conditions. For example, a strain of the t...

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Autores principales: Zeldes, Benjamin, Poehlein, Anja, Jain, Surbhi, Baum, Christoph, Daniel, Rolf, Müller, Volker, Basen, Mirko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9834392/
https://www.ncbi.nlm.nih.gov/pubmed/37938748
http://dx.doi.org/10.1038/s43705-022-00211-7
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author Zeldes, Benjamin
Poehlein, Anja
Jain, Surbhi
Baum, Christoph
Daniel, Rolf
Müller, Volker
Basen, Mirko
author_facet Zeldes, Benjamin
Poehlein, Anja
Jain, Surbhi
Baum, Christoph
Daniel, Rolf
Müller, Volker
Basen, Mirko
author_sort Zeldes, Benjamin
collection PubMed
description DNA uptake is widespread among microorganisms and considered a strategy for rapid adaptation to new conditions. While both DNA uptake and adaptation are referred to in the context of natural environments, they are often studied in laboratories under defined conditions. For example, a strain of the thermophile Thermoanaerobacter kivui had been adapted to growth on high concentrations of carbon monoxide (CO). Unusual phenotypes of the CO-adapted strain prompted us to examine it more closely, revealing a horizontal gene transfer (HGT) event from another thermophile, Thermoanaerobacter sp. strain X514, being cultured in the same laboratory. The transferred genes conferred on T. kivui the ability to utilize trehalose, a trace component of the yeast-extract added to the media during CO-adaptation. This same HGT event simultaneously deleted a native operon for thiamine biosynthesis, which likely explains why the CO-adapted strain grows poorly without added vitamins. Attempts to replicate this HGT by providing T. kivui with genomic DNA from Thermoanaerobacter sp. strain X514 revealed that it is easily reproducible in the lab. This subtle form of “genome contamination” is difficult to detect, since the genome remains predominantly T. kivui, and no living cells from the original contamination remain. Unexpected HGT between two microorganisms as well as simultaneous adaptation to several conditions may occur often and unrecognized in laboratory environments, requiring caution and careful monitoring of phenotype and genotype of microorganisms that are naturally-competent for DNA uptake.
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spelling pubmed-98343922023-01-13 DNA uptake from a laboratory environment drives unexpected adaptation of a thermophile to a minor medium component Zeldes, Benjamin Poehlein, Anja Jain, Surbhi Baum, Christoph Daniel, Rolf Müller, Volker Basen, Mirko ISME Commun Article DNA uptake is widespread among microorganisms and considered a strategy for rapid adaptation to new conditions. While both DNA uptake and adaptation are referred to in the context of natural environments, they are often studied in laboratories under defined conditions. For example, a strain of the thermophile Thermoanaerobacter kivui had been adapted to growth on high concentrations of carbon monoxide (CO). Unusual phenotypes of the CO-adapted strain prompted us to examine it more closely, revealing a horizontal gene transfer (HGT) event from another thermophile, Thermoanaerobacter sp. strain X514, being cultured in the same laboratory. The transferred genes conferred on T. kivui the ability to utilize trehalose, a trace component of the yeast-extract added to the media during CO-adaptation. This same HGT event simultaneously deleted a native operon for thiamine biosynthesis, which likely explains why the CO-adapted strain grows poorly without added vitamins. Attempts to replicate this HGT by providing T. kivui with genomic DNA from Thermoanaerobacter sp. strain X514 revealed that it is easily reproducible in the lab. This subtle form of “genome contamination” is difficult to detect, since the genome remains predominantly T. kivui, and no living cells from the original contamination remain. Unexpected HGT between two microorganisms as well as simultaneous adaptation to several conditions may occur often and unrecognized in laboratory environments, requiring caution and careful monitoring of phenotype and genotype of microorganisms that are naturally-competent for DNA uptake. Nature Publishing Group UK 2023-01-11 /pmc/articles/PMC9834392/ /pubmed/37938748 http://dx.doi.org/10.1038/s43705-022-00211-7 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
Zeldes, Benjamin
Poehlein, Anja
Jain, Surbhi
Baum, Christoph
Daniel, Rolf
Müller, Volker
Basen, Mirko
DNA uptake from a laboratory environment drives unexpected adaptation of a thermophile to a minor medium component
title DNA uptake from a laboratory environment drives unexpected adaptation of a thermophile to a minor medium component
title_full DNA uptake from a laboratory environment drives unexpected adaptation of a thermophile to a minor medium component
title_fullStr DNA uptake from a laboratory environment drives unexpected adaptation of a thermophile to a minor medium component
title_full_unstemmed DNA uptake from a laboratory environment drives unexpected adaptation of a thermophile to a minor medium component
title_short DNA uptake from a laboratory environment drives unexpected adaptation of a thermophile to a minor medium component
title_sort dna uptake from a laboratory environment drives unexpected adaptation of a thermophile to a minor medium component
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9834392/
https://www.ncbi.nlm.nih.gov/pubmed/37938748
http://dx.doi.org/10.1038/s43705-022-00211-7
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