Structure and function of virion RNA polymerase of a crAss-like phage

  • 1.

    Dutilh, B. E. et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat. Commun. 5, 4498 (2014).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 2.

    Yutin, N. et al. Discovery of an expansive bacteriophage family that includes the most abundant viruses from the human gut. Nat. Microbiol. 3, 38–46 (2018).

    CAS  PubMed  Article  Google Scholar 

  • 3.

    Koonin, E. V. & Yutin, N. The crAss-like phage group: how metagenomics reshaped the human virome. Trends Microbiol. 28, 349–359 (2020).

    CAS  PubMed  Article  Google Scholar 

  • 4.

    Holmfeldt, K. et al. Twelve previously unknown phage genera are ubiquitous in global oceans. Proc. Natl Acad. Sci. USA 110, 12798–12803 (2013).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 5.

    Werner, F. & Grohmann, D. Evolution of multisubunit RNA polymerases in the three domains of life. Nat. Rev. Microbiol. 9, 85–98 (2011).

    CAS  PubMed  Article  Google Scholar 

  • 6.

    Cogoni, C. & Macino, G. Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399, 166–169 (1999).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 7.

    Salgado, P. S. et al. The structure of an RNAi polymerase links RNA silencing and transcription. PLoS Biol. 4, e434 (2006).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 8.

    Shutt, T. E. & Gray, M. W. Bacteriophage origins of mitochondrial replication and transcription proteins. Trends Genet. 22, 90–95 (2006).

    CAS  PubMed  Article  Google Scholar 

  • 9.

    Zhang, G. et al. Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 Å resolution. Cell 98, 811–824 (1999).

    CAS  PubMed  Article  Google Scholar 

  • 10.

    Sidorenkov, I., Komissarova, N. & Kashlev, M. Crucial role of the RNA:DNA hybrid in the processivity of transcription. Mol. Cell 2, 55–64 (1998).

    CAS  PubMed  Article  Google Scholar 

  • 11.

    Campbell, E. A. et al. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104, 901–912 (2001).

    CAS  PubMed  Article  Google Scholar 

  • 12.

    Shkoporov, A. N. et al. ΦCrAss001 represents the most abundant bacteriophage family in the human gut and infects Bacteroides intestinalis. Nat. Commun. 9, 4781 (2018).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 13.

    Guerin, E. et al. Biology and taxonomy of crAss-like bacteriophages, the most abundant virus in the human gut. Cell Host Microbe 24, 653–664.e6 (2018).

    CAS  PubMed  Article  Google Scholar 

  • 14.

    Paget, M. S. Bacterial sigma factors and anti-sigma factors: structure, function and distribution. Biomolecules 5, 1245–1265 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 15.

    Vassylyev, D. G. et al. Structural basis for substrate loading in bacterial RNA polymerase. Nature 448, 163–168 (2007).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 16.

    Wang, D., Bushnell, D. A., Westover, K. D., Kaplan, C. D. & Kornberg, R. D. Structural basis of transcription: role of the trigger loop in substrate specificity and catalysis. Cell 127, 941–954 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 17.

    Cramer, P., Bushnell, D. A. & Kornberg, R. D. Structural basis of transcription: RNA polymerase II at 2.8 ångstrom resolution. Science 292, 1863–1876 (2001).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 18.

    Lane, W. J. & Darst, S. A. Molecular evolution of multisubunit RNA polymerases: structural analysis. J. Mol. Biol. 395, 686–704 (2010).

    CAS  PubMed  Article  Google Scholar 

  • 19.

    Krissinel, E. & Henrick, K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D 60, 2256–2268 (2004).

    CAS  PubMed  Article  Google Scholar 

  • 20.

    Holm, L. Benchmarking fold detection by DaliLite v.5. Bioinformatics 35, 5326–5327 (2019).

    CAS  PubMed  Article  Google Scholar 

  • 21.

    Berman, H. M. et al. The Protein Data Bank. Nucleic Acids Res. 28, 235–242 (2000).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 22.

    Engel, C., Sainsbury, S., Cheung, A. C., Kostrewa, D. & Cramer, P. RNA polymerase I structure and transcription regulation. Nature 502, 650–655 (2013).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 23.

    Fernández-Tornero, C. et al. Crystal structure of the 14-subunit RNA polymerase I. Nature 502, 644–649 (2013).

    ADS  PubMed  Article  CAS  Google Scholar 

  • 24.

    Murakami, K. S., Davydova, E. K. & Rothman-Denes, L. B. X-ray crystal structure of the polymerase domain of the bacteriophage N4 virion RNA polymerase. Proc. Natl Acad. Sci. USA 105, 5046–5051 (2008).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 25.

    Gleghorn, M. L., Davydova, E. K., Rothman-Denes, L. B. & Murakami, K. S. Structural basis for DNA-hairpin promoter recognition by the bacteriophage N4 virion RNA polymerase. Mol. Cell 32, 707–717 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 26.

    Iyer, L. M., Koonin, E. V. & Aravind, L. Evolutionary connection between the catalytic subunits of DNA-dependent RNA polymerases and eukaryotic RNA-dependent RNA polymerases and the origin of RNA polymerases. BMC Struct. Biol. 3, 1 (2003).

    PubMed  PubMed Central  Article  Google Scholar 

  • 27.

    Shabalina, S. A. & Koonin, E. V. Origins and evolution of eukaryotic RNA interference. Trends Ecol. Evol. 23, 578–587 (2008).

    PubMed  PubMed Central  Article  Google Scholar 

  • 28.

    Aalto, A. P., Poranen, M. M., Grimes, J. M., Stuart, D. I. & Bamford, D. H. In vitro activities of the multifunctional RNA silencing polymerase QDE-1 of Neurospora crassa. J. Biol. Chem. 285, 29367–29374 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 29.

    Lee, H. C. et al. The DNA/RNA-dependent RNA polymerase QDE-1 generates aberrant RNA and dsRNA for RNAi in a process requiring replication protein A and a DNA helicase. PLoS Biol. 8, e1000496 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 30.

    Holmfeldt, K., Middelboe, M., Nybroe, O. & Riemann, L. Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts. Appl. Environ. Microbiol. 73, 6730–6739 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 31.

    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 32.

    Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).

    MathSciNet  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 33.

    Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 34.

    Liao, Y., Smyth, G. K. & Shi, W. The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. Nucleic Acids Res. 47, e47 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 35.

    Sokolova, M. et al. A non-canonical multisubunit RNA polymerase encoded by the AR9 phage recognizes the template strand of its uracil-containing promoters. Nucleic Acids Res. 45, 5958–5967 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 36.

    Kabsch, W. Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr. D 66, 133–144 (2010).

    CAS  PubMed  Article  Google Scholar 

  • 37.

    Pape, T. & Schneider, T. R. HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs. J. Appl. Crystallogr. 37, 843–844 (2004).

    CAS  Article  Google Scholar 

  • 38.

    Sheldrick, G. M. Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D 66, 479–485 (2010).

    CAS  PubMed  Article  Google Scholar 

  • 39.

    Cowtan, K. Recent developments in classical density modification. Acta Crystallogr. D 66, 470–478 (2010).

    CAS  PubMed  Article  Google Scholar 

  • 40.

    Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235–242 (2011).

    CAS  PubMed  Article  Google Scholar 

  • 41.

    Read, R. J. & McCoy, A. J. Using SAD data in Phaser. Acta Crystallogr. D 67, 338–344 (2011).

    CAS  PubMed  Article  Google Scholar 

  • 42.

    Cowtan, K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D 62, 1002–1011 (2006).

    PubMed  Article  CAS  Google Scholar 

  • 43.

    Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).

    CAS  Article  Google Scholar 

  • 44.

    Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).

    CAS  Article  Google Scholar 

  • 45.

    Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12–21 (2010).

    CAS  PubMed  Article  Google Scholar 

  • 46.

    Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).

    CAS  Article  Google Scholar 

  • 47.

    Kettenberger, H., Armache, K. J. & Cramer, P. Complete RNA polymerase II elongation complex structure and its interactions with NTP and TFIIS. Mol. Cell 16, 955–965 (2004).

    CAS  PubMed  PubMed Central  Article  Google Scholar