Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail
Abstract Thermus thermophilus bacteriophage P23-45 encodes a giant 5,002-residue tail tape measure protein (TMP) that defines the length of its extraordinarily long tail. Here, we show that the N-terminal portion of P23-45 TMP is an unusual RNA polymerase (RNAP) homologous to cellular RNAPs. The TMP...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-44630-z |
| _version_ | 1827388366511931392 |
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| author | Anastasiia Chaban Leonid Minakhin Ekaterina Goldobina Brain Bae Yue Hao Sergei Borukhov Leena Putzeys Maarten Boon Florian Kabinger Rob Lavigne Kira S. Makarova Eugene V. Koonin Satish K. Nair Shunsuke Tagami Konstantin Severinov Maria L. Sokolova |
| author_facet | Anastasiia Chaban Leonid Minakhin Ekaterina Goldobina Brain Bae Yue Hao Sergei Borukhov Leena Putzeys Maarten Boon Florian Kabinger Rob Lavigne Kira S. Makarova Eugene V. Koonin Satish K. Nair Shunsuke Tagami Konstantin Severinov Maria L. Sokolova |
| author_sort | Anastasiia Chaban |
| collection | DOAJ |
| description | Abstract Thermus thermophilus bacteriophage P23-45 encodes a giant 5,002-residue tail tape measure protein (TMP) that defines the length of its extraordinarily long tail. Here, we show that the N-terminal portion of P23-45 TMP is an unusual RNA polymerase (RNAP) homologous to cellular RNAPs. The TMP-fused virion RNAP transcribes pre-early phage genes, including a gene that encodes another, non-virion RNAP, that transcribes early and some middle phage genes. We report the crystal structures of both P23-45 RNAPs. The non-virion RNAP has a crab-claw-like architecture. By contrast, the virion RNAP adopts a unique flat structure without a clamp. Structure and sequence comparisons of the P23-45 RNAPs with other RNAPs suggest that, despite the extensive functional differences, the two P23-45 RNAPs originate from an ancient gene duplication in an ancestral phage. Our findings demonstrate striking adaptability of RNAPs that can be attained within a single virus species. |
| first_indexed | 2024-03-08T16:16:49Z |
| format | Article |
| id | doaj.art-df2a07d49e874c7f8abbaf09ef7dc600 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-08T16:16:49Z |
| publishDate | 2024-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-df2a07d49e874c7f8abbaf09ef7dc6002024-01-07T12:34:26ZengNature PortfolioNature Communications2041-17232024-01-0115111210.1038/s41467-023-44630-zTail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tailAnastasiia Chaban0Leonid Minakhin1Ekaterina Goldobina2Brain Bae3Yue Hao4Sergei Borukhov5Leena Putzeys6Maarten Boon7Florian Kabinger8Rob Lavigne9Kira S. Makarova10Eugene V. Koonin11Satish K. Nair12Shunsuke Tagami13Konstantin Severinov14Maria L. Sokolova15Center of Life Sciences, Skolkovo Institute of Science and TechnologyWaksman Institute for Microbiology, Rutgers, The State University of New JerseyCenter of Life Sciences, Skolkovo Institute of Science and TechnologyDepartment of Biochemistry, University of Illinois at Urbana−ChampaignDepartment of Biochemistry, University of Illinois at Urbana−ChampaignDepartment of Cell Biology and Neuroscience, Rowan University School of Osteopathic Medicine at StratfordDepartment of Biosystems, Laboratory of Gene Technology, KU LeuvenDepartment of Biosystems, Laboratory of Gene Technology, KU LeuvenDepartment of Molecular Biology, Max Planck Institute for Multidisciplinary SciencesDepartment of Biosystems, Laboratory of Gene Technology, KU LeuvenNational Center for Biotechnology Information, National Library of Medicine, National Institutes of HealthNational Center for Biotechnology Information, National Library of Medicine, National Institutes of HealthDepartment of Biochemistry, University of Illinois at Urbana−ChampaignRIKEN Center for Biosystems Dynamics ResearchWaksman Institute for Microbiology, Rutgers, The State University of New JerseyCenter of Life Sciences, Skolkovo Institute of Science and TechnologyAbstract Thermus thermophilus bacteriophage P23-45 encodes a giant 5,002-residue tail tape measure protein (TMP) that defines the length of its extraordinarily long tail. Here, we show that the N-terminal portion of P23-45 TMP is an unusual RNA polymerase (RNAP) homologous to cellular RNAPs. The TMP-fused virion RNAP transcribes pre-early phage genes, including a gene that encodes another, non-virion RNAP, that transcribes early and some middle phage genes. We report the crystal structures of both P23-45 RNAPs. The non-virion RNAP has a crab-claw-like architecture. By contrast, the virion RNAP adopts a unique flat structure without a clamp. Structure and sequence comparisons of the P23-45 RNAPs with other RNAPs suggest that, despite the extensive functional differences, the two P23-45 RNAPs originate from an ancient gene duplication in an ancestral phage. Our findings demonstrate striking adaptability of RNAPs that can be attained within a single virus species.https://doi.org/10.1038/s41467-023-44630-z |
| spellingShingle | Anastasiia Chaban Leonid Minakhin Ekaterina Goldobina Brain Bae Yue Hao Sergei Borukhov Leena Putzeys Maarten Boon Florian Kabinger Rob Lavigne Kira S. Makarova Eugene V. Koonin Satish K. Nair Shunsuke Tagami Konstantin Severinov Maria L. Sokolova Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail Nature Communications |
| title | Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail |
| title_full | Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail |
| title_fullStr | Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail |
| title_full_unstemmed | Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail |
| title_short | Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail |
| title_sort | tail tape fused virion and non virion rna polymerases of a thermophilic virus with an extremely long tail |
| url | https://doi.org/10.1038/s41467-023-44630-z |
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