Phage tail-like nanostructures affect microbial interactions between Streptomyces and fungi
Abstract 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...
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| Format: | Article |
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Nature Portfolio
2021-10-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-021-99490-8 |
| _version_ | 1819148418867527680 |
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| author | Toshiki Nagakubo Tatsuya Yamamoto Shumpei Asamizu Masanori Toyofuku Nobuhiko Nomura Hiroyasu Onaka |
| author_facet | Toshiki Nagakubo Tatsuya Yamamoto Shumpei Asamizu Masanori Toyofuku Nobuhiko Nomura Hiroyasu Onaka |
| author_sort | Toshiki Nagakubo |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-22T13:45:24Z |
| format | Article |
| id | doaj.art-e8d43e3ee0a247a99bd375242f22559f |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-12-22T13:45:24Z |
| publishDate | 2021-10-01 |
| publisher | Nature Portfolio |
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| series | Scientific Reports |
| spelling | doaj.art-e8d43e3ee0a247a99bd375242f22559f2022-12-21T18:23:48ZengNature PortfolioScientific Reports2045-23222021-10-0111111110.1038/s41598-021-99490-8Phage tail-like nanostructures affect microbial interactions between Streptomyces and fungiToshiki Nagakubo0Tatsuya Yamamoto1Shumpei Asamizu2Masanori Toyofuku3Nobuhiko Nomura4Hiroyasu Onaka5Graduate School of Agricultural and Life Sciences, Department of Biotechnology, The University of TokyoDepartment of Life and Environmental Sciences, University of TsukubaGraduate School of Agricultural and Life Sciences, Department of Biotechnology, The University of TokyoDepartment of Life and Environmental Sciences, University of TsukubaDepartment of Life and Environmental Sciences, University of TsukubaGraduate School of Agricultural and Life Sciences, Department of Biotechnology, The University of TokyoAbstract 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.https://doi.org/10.1038/s41598-021-99490-8 |
| spellingShingle | Toshiki Nagakubo Tatsuya Yamamoto Shumpei Asamizu Masanori Toyofuku Nobuhiko Nomura Hiroyasu Onaka Phage tail-like nanostructures affect microbial interactions between Streptomyces and fungi Scientific Reports |
| 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 |
| url | https://doi.org/10.1038/s41598-021-99490-8 |
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