The DOI matches its Crossref record; 51 of the 51 references it cites were found in a registry or an index.
A Vibrio cholerae viral satellite maximizes its spread and inhibits phage by remodeling hijacked phage coat proteins into small capsids
Open accessPreprint — published as 10.7554/elife.87611.3
Abstract
Abstract Phage satellites commonly remodel capsids they hijack from the phages they parasitize, but only a few mechanisms regulating the change in capsid size have been reported. Here, we investigated how a satellite from Vibrio cholerae, PLE, remodels the capsid it has been predicted to steal from the phage ICP1 (1). We identified that a PLE-encoded protein, TcaP, is both necessary and sufficient to form small capsids during ICP1 infection. Interestingly, we found that PLE is dependent on small capsids for efficient transduction of its genome, making it the first satellite to have this requirement. ICP1 isolates that escaped TcaP-mediated remodeling acquired substitutions in the coat protein, suggesting an interaction between these two proteins. With a procapsid-like-particle (PLP) assembly platform in Escherichia coli, we demonstrated that TcaP is a bona fide scaffold that regulates the assembly of small capsids. Further, we studied the structure of PLE PLPs using cryogenic electron microscopy and found that TcaP is an external scaffold, that is functionally and somewhat structurally similar to the external scaffold, Sid, encoded by the unrelated satellite P4 (2). Finally, we showed that TcaP is largely conserved across PLEs. Together, these data support a model in which TcaP directs the assembly of small capsids comprised of ICP1 coat proteins, which inhibits the complete packaging of the ICP1 genome and permits more efficient packaging of replicated PLE genomes.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
Features and development of Coot
Emsley, P., Lohkamp, B., Scott, W. G., & Cowtan, K. (2010) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444910007493 · Cited by 29,915
cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination
Punjani, A., Rubinstein, J. L., Fleet, D. J., & Brubaker, M. A. (2017) · Nature Methods · doi:10.1038/nmeth.4169 · Cited by 11,626
Liebschner, D., Afonine, P. V., Baker, M. L., Bunkóczi, G., Chen, V. B., Croll, T. I., Hintze, B., Hung, L.-W., Jain, S., McCoy, A. J., et al. (2019) · Acta Crystallographica Section D Structural Biology · doi:10.1107/s2059798319011471 · Cited by 7,953
New tools for automated cryo-EM single-particle analysis in RELION-4.0
Kimanius, D., Dong, L., Sharov, G., Nakane, T., & Scheres, S. H. W. (2021) · Biochemical Journal · doi:10.1042/bcj20210708 · Cited by 1,086
de la Rosa-Trevín, J. M., Quintana, A., del Cano, L., Zaldívar, A., Foche, I., Gutiérrez, J., Gómez-Blanco, J., Burguet-Castell, J., Cuenca-Alba, J., Abrishami, V., et al. (2016) · Journal of Structural Biology · doi:10.1016/j.jsb.2016.04.010 · Cited by 589
A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity
Seed, K. D., Lazinski, D. W., Calderwood, S. B., & Camilli, A. (2013) · Nature · doi:10.1038/nature11927 · Cited by 386
Self-citationAsarnow, D., Palovcak, E., & Cheng, Y. (2019) · Figshare · doi:10.5281/zenodo.3576629 · Cited by 241
Catalytic head assembling protein in virus morphogenesis
King, J. W., & Casjens, S. (1974) · Nature · doi:10.1038/251112a0 · Cited by 193
Mechanisms of DNA Packaging by Large Double-Stranded DNA Viruses
Rao, V. B., & Feiss, M. G. (2015) · Annual Review of Virology · doi:10.1146/annurev-virology-100114-055212 · Cited by 191
Prevelige, P. E., Thomas, D., & King, J. W. (1988) · Journal of Molecular Biology · doi:10.1016/0022-2836(88)90555-4 · Cited by 185
Steven, A. C., Heymann, J. B., Cheng, N., Trus, B. L., & Conway, J. F. (2005) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2005.03.008 · Cited by 178
Structure of a viral procapsid with molecular scaffolding
Dokland, T., McKENNA, R. V., Ilag, L. L., Bowman, B. R., Incardona, N. L., Fane, B. A., & Rossmann, M. G. (1997) · Nature · doi:10.1038/38537 · Cited by 154
Scaffolding proteins and their role in viral assembly
Dokland, T. (1999) · Cellular and Molecular Life Sciences · doi:10.1007/s000180050455 · Cited by 152
Suhanovsky, M. M., & Teschke, C. M. (2015) · Virology · doi:10.1016/j.virol.2015.02.055 · Cited by 125
A highly specific phage defense system is a conserved feature of the Vibrio cholerae mobilome
O’Hara, B. J., Barth, Z. K., McKitterick, A. C., & Seed, K. D. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006838 · Cited by 125
Self-citationDalia, A. B., Lazinski, D. W., & Camilli, A. (2014) · mBio · doi:10.1128/mbio.01028-13 · Cited by 124
Christie, G. E., & Dokland, T. (2012) · Virology · doi:10.1016/j.virol.2012.10.028 · Cited by 119
Genetic basis of bacteriophage HK97 prohead assembly
Duda, R. L., Martincic, K., & Hendrix, R. W. (1995) · Journal of Molecular Biology · doi:10.1016/s0022-2836(05)80144-5 · Cited by 116
Six, E. W. (1975) · Virology · doi:10.1016/0042-6822(75)90422-5 · Cited by 110
Determination of capsid size by satellite bacteriophage P4.
Shore, D., Dehò, G., Ebel-Tsipis, J., & Goldstein, R. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.1.400 · Cited by 86
Identification and characterization of thousands of bacteriophage satellites across bacteria
de Sousa, J. A. M., Fillol-Salom, A., Penadés, J. R., & Rocha, E. P. C. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad123 · Cited by 75
Anti-phage islands force their target phage to directly mediate island excision and spread
McKitterick, A. C., & Seed, K. D. (2018) · Nature Communications · doi:10.1038/s41467-018-04786-5 · Cited by 68
Self-citationThe Capsid Size-determining Protein Sid Forms an External Scaffold on Phage P4 Procapsids
Marvik, O. J., Dokland, T., Nøkling, R. H., Jacobsen, E., Larsen, T., & Lindqvist, B. H. (1995) · Journal of Molecular Biology · doi:10.1006/jmbi.1995.0416 · Cited by 67
Cerritelli, M. E., & Studier, W. F. (1996) · Journal of Molecular Biology · doi:10.1006/jmbi.1996.0250 · Cited by 62
Hays, S. G., & Seed, K. D. (2020) · eLife · doi:10.7554/elife.53200 · Cited by 61
Self-citationDearborn, A. D., Wall, E. A., Kizziah, J. L., Klenow, L., Parker, L. K., Manning, K. A., Spilman, M. S., Spear, J. M., Christie, G. E., & Dokland, T. (2017) · eLife · doi:10.7554/elife.30822 · Cited by 60
Damle, P. K., Wall, E. A., Spilman, M. S., Dearborn, A. D., Ram, G., Novick, R. P., Dokland, T., & Christie, G. E. (2012) · Virology · doi:10.1016/j.virol.2012.05.026 · Cited by 59
Barth, Z. K., Nguyen, M. H. T., & Seed, K. D. (2021) · eLife · doi:10.7554/elife.68339 · Cited by 54
Self-citationAlqurainy, N., Miguel-Romero, L., de Sousa, J. A. M., et al. (2023) · Cell Host & Microbe · doi:10.1016/j.chom.2022.12.001 · Cited by 51
Barth, Z. K., Silvas, T. V., Angermeyer, A., & Seed, K. D. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz1005 · Cited by 48
Self-citationHafenstein, S. L., & Fane, B. A. (2002) · Journal of Virology · doi:10.1128/jvi.76.11.5350-5356.2002 · Cited by 42
McKitterick, A. C., LeGault, K. N., Angermeyer, A., Alam, M., & Seed, K. D. (2019) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2018.0089 · Cited by 42
Self-citationA phage parasite deploys a nicking nuclease effector to inhibit viral host replication
LeGault, K. N., Barth, Z. K., DePaola, P., & Seed, K. D. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac002 · Cited by 39
Self-citationDuda, R. L., Oh, B., & Hendrix, R. W. (2013) · Journal of Molecular Biology · doi:10.1016/j.jmb.2013.05.002 · Cited by 38
Convergent evolution of pathogenicity islands in helper cos phage interference
Carpena, N., Manning, K. A., Dokland, T., Marina, A., & Penadés, J. R. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0505 · Cited by 38
Netter, Z., Boyd, C. M., Silvas, T. V., & Seed, K. D. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab207 · Cited by 38
Self-citationAssembly of bacteriophage P2 and P4 procapsids with internal scaffolding protein
Wang, S., Chang, J. R., & Dokland, T. (2006) · Virology · doi:10.1016/j.virol.2005.12.021 · Cited by 37
Angermeyer, A., Hays, S. G., Nguyen, M. H. T., Johura, F., Sultana, M., Alam, M., & Seed, K. D. (2022) · mBio · doi:10.1128/mbio.03088-21 · Cited by 35
Self-citationMarine viral particles reveal an expansive repertoire of phage-parasitizing mobile elements
Eppley, J. M., Biller, S. J., Luo, E., Burger, A. H., & DeLong, E. F. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2212722119 · Cited by 34
Cherwa, J. E., Organtini, L. J., Ashley, R. E., Hafenstein, S. L., & Fane, B. A. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.07.070 · Cited by 33
Bacteriophage P2 and P4 Assembly: Alternative Scaffolding Proteins Regulate Capsid Size
Marvik, O. J., Sharma, P., Dokland, T., & Lindqvist, B. H. (1994) · Virology · doi:10.1006/viro.1994.1234 · Cited by 32
Lander, G. C., Baudoux, A., Azam, F., Potter, C. S., Carragher, B. O., & Johnson, J. E. (2012) · Structure · doi:10.1016/j.str.2012.01.007 · Cited by 31
Assembly of bacteriophage 80α capsids in a Staphylococcus aureus expression system
Spilman, M. S., Damle, P. K., Dearborn, A. D., Rodenburg, C. M., Chang, J. R., Wall, E. A., Christie, G. E., & Dokland, T. (2012) · Virology · doi:10.1016/j.virol.2012.08.031 · Cited by 25
Incorporation of scaffolding protein gpO in bacteriophages P2 and P4
Chang, J. R., Poliakov, A., Prevelige, P. E., Mobley, J. A., & Dokland, T. (2007) · Virology · doi:10.1016/j.virol.2007.08.039 · Cited by 25
Huet, A., Duda, R. L., Hendrix, R. W., Boulanger, P., & Conway, J. F. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2015.11.019 · Cited by 25
Kim, K., Sunshine, M. G., Lindqvist, B. H., & Six, E. W. (2001) · Virology · doi:10.1006/viro.2001.0853 · Cited by 19
A phage weaponizes a satellite recombinase to subvert viral restriction
Nguyen, M. H. T., Netter, Z., Angermeyer, A., & Seed, K. D. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac845 · Cited by 19
Self-citationStructure of the Capsid Size-Determining Scaffold of “Satellite” Bacteriophage P4
Kizziah, J. L., Rodenburg, C. M., & Dokland, T. (2020) · Viruses · doi:10.3390/v12090953 · Cited by 18
Shape shifter: redirection of prolate phage capsid assembly by staphylococcal pathogenicity islands
Hawkins, N. C., Kizziah, J. L., Penadés, J. R., & Dokland, T. (2021) · Nature Communications · doi:10.1038/s41467-021-26759-x · Cited by 18
Robertson, B., McCann, P. J., Matusick-Kumar, L., Preston, V. G., & Gao, M. (1997) · Journal of Virology · doi:10.1128/jvi.71.2.1683-1687.1997 · Cited by 14
Research works printed but not linked: 5
- 2021, Bacteriophage ICP1: A Persistent Predator of, Annu. Rev. Virol, 12, 1
- 2022, UVC inactivation of pathogenic samples suitable for cryo-EM analysis. Commun, Biol, 5
- 2012, Assembly of bacteriophage 80α capsids in a Staphylococcus aureus expression system, Virology, 434, 242, 10.1016/j.virol.2012.08.031 · DOI
- 2020, Dominant Vibrio cholerae phage exhibits lysis inhibition sensitive to disruption by a defensive phage satellite, eLife, 9, 1
- 2019, Competition between mobile genetic elements drives optimization of a phage-encoded CRISPR-Cas system: Insights from a natural arms race, Philos. Trans. R. Soc. B Biol. Sci, 374, 1
Metadata
- Authors
- Boyd, C. M., Subramanian, S., Dunham, D. T., Parent, K. N., & Seed, K. D.
- Affiliations
- University of California, Berkeley (US)
- Michigan State University (US)
- Corresponding author
- Seed, Kimberley D.
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2023-11-16
- ISSN
- 2050-084X (ISSN-L)
- OpenAlex
- W4388722884
- Cited by
- 1
- References
- 51
- Citations by year
- 2024: 1
- Type
- posted content
- Language
- en
- Open access
- gold
- doi.org
- Locations
- eLife (acceptedVersion, cc-by)
- Funders
- National Institute of Allergy and Infectious Diseases (R01AI127652)
- National Institutes of Health (GM110185, GM140803, GM116789, T32 GM132022)
- National Science Foundation Graduate Research Fellowship Program (2018257700)
- National Science Foundation (1750125)
- Topics
- Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
- Life Sciences › Immunology and Microbiology › Virology › Plant and Fungal Interactions Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- phage satellites, Vibrio cholerae, TCAP, transduction, capsid assembly, phage packaging, phage inhibition, genome packaging
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.
