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Phage tail-like nanostructures affect microbial interactions between Streptomyces and fungi

Extracellular contractile injection systems (eCISs) are structurally similar to headless phages and are versatile nanomachines conserved among diverse classes of bacteria. Herein, Streptomyces species, which comprise filamentous Gram-positive bacteria and are ubiquitous in soil, were shown to produc...

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Autores principales: Nagakubo, Toshiki, Yamamoto, Tatsuya, Asamizu, Shumpei, Toyofuku, Masanori, Nomura, Nobuhiko, Onaka, Hiroyasu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8505568/
https://www.ncbi.nlm.nih.gov/pubmed/34635733
http://dx.doi.org/10.1038/s41598-021-99490-8
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author Nagakubo, Toshiki
Yamamoto, Tatsuya
Asamizu, Shumpei
Toyofuku, Masanori
Nomura, Nobuhiko
Onaka, Hiroyasu
author_facet Nagakubo, Toshiki
Yamamoto, Tatsuya
Asamizu, Shumpei
Toyofuku, Masanori
Nomura, Nobuhiko
Onaka, Hiroyasu
author_sort Nagakubo, Toshiki
collection PubMed
description Extracellular contractile injection systems (eCISs) are structurally similar to headless phages and are versatile nanomachines conserved among diverse classes of bacteria. Herein, Streptomyces species, which comprise filamentous Gram-positive bacteria and are ubiquitous in soil, were shown to produce Streptomyces phage tail-like particles (SLPs) from eCIS-related genes that are widely conserved among Streptomyces species. In some Streptomyces species, these eCIS-related genes are regulated by a key regulatory gene, which is essential for Streptomyces life cycle and is involved in morphological differentiation and antibiotic production. Deletion mutants of S. lividans of the eCIS-related genes appeared phenotypically normal in terms of morphological differentiation and antibiotic production, suggesting that SLPs are involved in other aspects of Streptomyces life cycle. Using co-culture method, we found that colonies of SLP-deficient mutants of S. lividans were more severely invaded by fungi, including Saccharomyces cerevisiae and Schizosaccharomyces pombe. In addition, microscopic and transcriptional analyses demonstrated that SLP expression was elevated upon co-culture with the fungi. In contrast, co-culture with Bacillus subtilis markedly decreased SLP expression and increased antibiotic production. Our findings demonstrate that in Streptomyces, eCIS-related genes affect microbial competition, and the patterns of SLP expression can differ depending on the competitor species.
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spelling pubmed-85055682021-10-13 Phage tail-like nanostructures affect microbial interactions between Streptomyces and fungi Nagakubo, Toshiki Yamamoto, Tatsuya Asamizu, Shumpei Toyofuku, Masanori Nomura, Nobuhiko Onaka, Hiroyasu Sci Rep Article Extracellular contractile injection systems (eCISs) are structurally similar to headless phages and are versatile nanomachines conserved among diverse classes of bacteria. Herein, Streptomyces species, which comprise filamentous Gram-positive bacteria and are ubiquitous in soil, were shown to produce Streptomyces phage tail-like particles (SLPs) from eCIS-related genes that are widely conserved among Streptomyces species. In some Streptomyces species, these eCIS-related genes are regulated by a key regulatory gene, which is essential for Streptomyces life cycle and is involved in morphological differentiation and antibiotic production. Deletion mutants of S. lividans of the eCIS-related genes appeared phenotypically normal in terms of morphological differentiation and antibiotic production, suggesting that SLPs are involved in other aspects of Streptomyces life cycle. Using co-culture method, we found that colonies of SLP-deficient mutants of S. lividans were more severely invaded by fungi, including Saccharomyces cerevisiae and Schizosaccharomyces pombe. In addition, microscopic and transcriptional analyses demonstrated that SLP expression was elevated upon co-culture with the fungi. In contrast, co-culture with Bacillus subtilis markedly decreased SLP expression and increased antibiotic production. Our findings demonstrate that in Streptomyces, eCIS-related genes affect microbial competition, and the patterns of SLP expression can differ depending on the competitor species. Nature Publishing Group UK 2021-10-11 /pmc/articles/PMC8505568/ /pubmed/34635733 http://dx.doi.org/10.1038/s41598-021-99490-8 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Nagakubo, Toshiki
Yamamoto, Tatsuya
Asamizu, Shumpei
Toyofuku, Masanori
Nomura, Nobuhiko
Onaka, Hiroyasu
Phage tail-like nanostructures affect microbial interactions between Streptomyces and fungi
title Phage tail-like nanostructures affect microbial interactions between Streptomyces and fungi
title_full Phage tail-like nanostructures affect microbial interactions between Streptomyces and fungi
title_fullStr Phage tail-like nanostructures affect microbial interactions between Streptomyces and fungi
title_full_unstemmed Phage tail-like nanostructures affect microbial interactions between Streptomyces and fungi
title_short Phage tail-like nanostructures affect microbial interactions between Streptomyces and fungi
title_sort phage tail-like nanostructures affect microbial interactions between streptomyces and fungi
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8505568/
https://www.ncbi.nlm.nih.gov/pubmed/34635733
http://dx.doi.org/10.1038/s41598-021-99490-8
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