Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail

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

doi:10.1038/s41467-023-44630-z

Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail

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

Cell Biology

Rowan University

Research output: Contribution to journal › Article › peer-review

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.

Original language	American English
Article number	317
Journal	Nature communications
Volume	15
Issue number	1
DOIs	https://doi.org/10.1038/s41467-023-44630-z
State	Published - Dec 2024

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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Chaban, A., Minakhin, L., Goldobina, E., Bae, B., Hao, Y., Borukhov, S., Putzeys, L., Boon, M., Kabinger, F., Lavigne, R., Makarova, K. S., Koonin, E. V., Nair, S. K., Tagami, S., Severinov, K., & Sokolova, M. L. (2024). Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail. Nature communications, 15(1), Article 317. https://doi.org/10.1038/s41467-023-44630-z

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title = "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-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.",

author = "Anastasiia Chaban and Leonid Minakhin and Ekaterina Goldobina and Brain Bae and Yue Hao and Sergei Borukhov and Leena Putzeys and Maarten Boon and Florian Kabinger and Rob Lavigne and Makarova, {Kira S.} and Koonin, {Eugene V.} and Nair, {Satish K.} and Shunsuke Tagami and Konstantin Severinov and Sokolova, {Maria L.}",

note = "Publisher Copyright: {\textcopyright} 2024, The Author(s).",

year = "2024",

month = dec,

doi = "10.1038/s41467-023-44630-z",

language = "American English",

volume = "15",

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Chaban, A, Minakhin, L, Goldobina, E, Bae, B, Hao, Y, Borukhov, S, Putzeys, L, Boon, M, Kabinger, F, Lavigne, R, Makarova, KS, Koonin, EV, Nair, SK, Tagami, S, Severinov, K & Sokolova, ML 2024, 'Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail', Nature communications, vol. 15, no. 1, 317. https://doi.org/10.1038/s41467-023-44630-z

TY - JOUR

T1 - Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail

AU - Chaban, Anastasiia

AU - Minakhin, Leonid

AU - Goldobina, Ekaterina

AU - Bae, Brain

AU - Hao, Yue

AU - Borukhov, Sergei

AU - Putzeys, Leena

AU - Boon, Maarten

AU - Kabinger, Florian

AU - Lavigne, Rob

AU - Makarova, Kira S.

AU - Koonin, Eugene V.

AU - Nair, Satish K.

AU - Tagami, Shunsuke

AU - Severinov, Konstantin

AU - Sokolova, Maria L.

PY - 2024/12

Y1 - 2024/12

N2 - 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.

AB - 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.

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SN - 2041-1723

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JO - Nature communications

JF - Nature communications

IS - 1

M1 - 317

ER -

Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail

Abstract

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