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Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system

Nonmotile microorganisms often enter new habitats by co-transport with motile microorganisms. Here, we report that also lytic phages can co-transport with hyphal-riding bacteria and facilitate bacterial colonization of a new habitat. This is comparable to the concept of biological invasions in macro...

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Autores principales: You, Xin, Kallies, René, Kühn, Ingolf, Schmidt, Matthias, Harms, Hauke, Chatzinotas, Antonis, Wick, Lukas Y.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9039081/
https://www.ncbi.nlm.nih.gov/pubmed/34903848
http://dx.doi.org/10.1038/s41396-021-01155-x
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author You, Xin
Kallies, René
Kühn, Ingolf
Schmidt, Matthias
Harms, Hauke
Chatzinotas, Antonis
Wick, Lukas Y.
author_facet You, Xin
Kallies, René
Kühn, Ingolf
Schmidt, Matthias
Harms, Hauke
Chatzinotas, Antonis
Wick, Lukas Y.
author_sort You, Xin
collection PubMed
description Nonmotile microorganisms often enter new habitats by co-transport with motile microorganisms. Here, we report that also lytic phages can co-transport with hyphal-riding bacteria and facilitate bacterial colonization of a new habitat. This is comparable to the concept of biological invasions in macroecology. In analogy to invasion frameworks in plant and animal ecology, we tailored spatially organized, water-unsaturated model microcosms using hyphae of Pythium ultimum as invasion paths and flagellated soil-bacterium Pseudomonas putida KT2440 as carrier for co-transport of Escherichia virus T4. P. putida KT2440 efficiently dispersed along P. ultimum to new habitats and dispatched T4 phages across air gaps transporting ≈0.6 phages bacteria(−1). No T4 displacement along hyphae was observed in the absence of carrier bacteria. If E. coli occupied the new habitat, T4 co-transport fueled the fitness of invading P. putida KT2440, while the absence of phage co-transport led to poor colonization followed by extinction. Our data emphasize the importance of hyphal transport of bacteria and associated phages in regulating fitness and composition of microbial populations in water-unsaturated systems. As such co-transport seems analogous to macroecological invasion processes, hyphosphere systems with motile bacteria and co-transported phages could be useful models for testing hypotheses in invasion ecology.
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spelling pubmed-90390812022-04-28 Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system You, Xin Kallies, René Kühn, Ingolf Schmidt, Matthias Harms, Hauke Chatzinotas, Antonis Wick, Lukas Y. ISME J Article Nonmotile microorganisms often enter new habitats by co-transport with motile microorganisms. Here, we report that also lytic phages can co-transport with hyphal-riding bacteria and facilitate bacterial colonization of a new habitat. This is comparable to the concept of biological invasions in macroecology. In analogy to invasion frameworks in plant and animal ecology, we tailored spatially organized, water-unsaturated model microcosms using hyphae of Pythium ultimum as invasion paths and flagellated soil-bacterium Pseudomonas putida KT2440 as carrier for co-transport of Escherichia virus T4. P. putida KT2440 efficiently dispersed along P. ultimum to new habitats and dispatched T4 phages across air gaps transporting ≈0.6 phages bacteria(−1). No T4 displacement along hyphae was observed in the absence of carrier bacteria. If E. coli occupied the new habitat, T4 co-transport fueled the fitness of invading P. putida KT2440, while the absence of phage co-transport led to poor colonization followed by extinction. Our data emphasize the importance of hyphal transport of bacteria and associated phages in regulating fitness and composition of microbial populations in water-unsaturated systems. As such co-transport seems analogous to macroecological invasion processes, hyphosphere systems with motile bacteria and co-transported phages could be useful models for testing hypotheses in invasion ecology. Nature Publishing Group UK 2021-12-13 2022-05 /pmc/articles/PMC9039081/ /pubmed/34903848 http://dx.doi.org/10.1038/s41396-021-01155-x Text en © The Author(s) 2021 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
You, Xin
Kallies, René
Kühn, Ingolf
Schmidt, Matthias
Harms, Hauke
Chatzinotas, Antonis
Wick, Lukas Y.
Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system
title Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system
title_full Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system
title_fullStr Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system
title_full_unstemmed Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system
title_short Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system
title_sort phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9039081/
https://www.ncbi.nlm.nih.gov/pubmed/34903848
http://dx.doi.org/10.1038/s41396-021-01155-x
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