CoChat
Sign Up
Cited by 3Bacteriophages and microbial interactionsBiochemical and Structural CharacterizationBacterial Genetics and Biotechnology

The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.

The Evolutionary History of a DNA Methylase Reveals Frequent Horizontal Transfer and Within-Gene Recombination

Open access
Gosselin, Sophia, Arsenault, Danielle, Jennings, Catherine, Gogarten, Johann·2023·Genes
DOI 10.3390/genes14020288PMC PMC9957025

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

Inteins, often referred to as protein introns, are highly mobile genetic elements that invade conserved genes throughout the tree of life. Inteins have been found to invade a wide variety of key genes within actinophages. While in the process of conducting a survey of these inteins in actinophages, we discovered that one protein family of methylases contained a putative intein, and two other unique insertion elements. These methylases are known to occur commonly in phages as orphan methylases (possibly as a form of resistance to restriction–modification systems). We found that the methylase family is not conserved within phage clusters and has a disparate distribution across divergent phage groups. We determined that two of the three insertion elements have a patchy distribution within the methylase protein family. Additionally, we found that the third insertion element is likely a second homing endonuclease, and that all three elements (the intein, the homing endonuclease, and what we refer to as the ShiLan domain) have different insertion sites that are conserved in the methylase gene family. Furthermore, we find strong evidence that both the intein and ShiLan domain are partaking in long-distance horizontal gene transfer events between divergent methylases in disparate phage hosts within the already dispersed methylase distribution. The reticulate evolutionary history of methylases and their insertion elements reveals high rates of gene transfer and within-gene recombination in actinophages.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/genes14020288

Cites

2 of 2 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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

Flagged first, then by citations

Research works printed but not linked: 38

  1. Liu, 2000, Protein-Splicing Intein: Genetic Mobility, Origin, and Evolution, Annu. Rev. Genet., 34, 61, 10.1146/annurev.genet.34.1.61 · DOI
  2. Pietrokovski, 2001, Intein Spread and Extinction in Evolution, Trends Genet., 17, 465, 10.1016/S0168-9525(01)02365-4 · DOI
  3. Perler, 1997, Compilation and Analysis of Intein Sequences, Nucleic Acids Res., 25, 1087, 10.1093/nar/25.6.1087 · DOI
  4. Gogarten, 2002, Inteins: Structure, Function, and Evolution, Annu. Rev. Microbiol., 56, 263, 10.1146/annurev.micro.56.012302.160741 · DOI
  5. Perler, 1998, Protein Splicing of Inteins and Hedgehog Autoproteolysis: Structure, Function, and Evolution, Cell, 92, 1, 10.1016/S0092-8674(00)80892-2 · DOI
  6. Gimble, 1992, Homing of a DNA Endonuclease Gene by Meiotic Gene Conversion in Saccharomyces Cerevisiae, Nature, 357, 301, 10.1038/357301a0 · DOI
  7. Naor, 2016, Impact of a Homing Intein on Recombination Frequency and Organismal Fitness, Proc. Natl. Acad. Sci. USA, 113, E4654, 10.1073/pnas.1606416113 · DOI
  8. Swithers, K.S., Senejani, A.G., Fournier, G.P., and Gogarten, J.P. (2009). Conservation of Intron and Intein Insertion Sites: Implications for Life Histories of Parasitic Genetic Elements. BMC Evol. Biol., 9. · DOI
  9. Kelley, 2016, Mycobacteriophages as Incubators for Intein Dissemination and Evolution, Mbio, 7, e01537-16, 10.1128/mBio.01537-16 · DOI
  10. Barka, 2015, Taxonomy, Physiology, and Natural Products of Actinobacteria, Microbiol. Mol. Biol. Rev., 80, 1, 10.1128/MMBR.00019-15 · DOI
  11. Dedrick, 2021, Toward a Phage Cocktail for Tuberculosis: Susceptibility and Tuberculocidal Action of Mycobacteriophages against Diverse Mycobacterium Tuberculosis Strains, Mbio, 12, e00973-21, 10.1128/mBio.00973-21 · DOI
  12. Hatfull, 2022, Phage Therapy for Antibiotic-Resistant Bacterial Infections, Annu. Rev. Med., 73, 197, 10.1146/annurev-med-080219-122208 · DOI
  13. Fruciano, 2007, Phage as an Antimicrobial Agent: D’Herelle’s Heretical Theories and Their Role in the Decline of Phage Prophylaxis in the West, Can. J. Infect. Dis. Med. Microbiol., 18, 19, 10.1155/2007/976850 · DOI
  14. Russell, 2017, PhagesDB: The Actinobacteriophage Database, Bioinformatics, 33, 784, 10.1093/bioinformatics/btw711 · DOI
  15. Pope, 2015, Whole Genome Comparison of a Large Collection of Mycobacteriophages Reveals a Continuum of Phage Genetic Diversity, Elife, 4, e06416, 10.7554/eLife.06416 · DOI
  16. Skovgaard, 2005, Dam Methylation: Coordinating Cellular Processes, Curr. Opin. Microbiol., 8, 154, 10.1016/j.mib.2005.02.009 · DOI
  17. Katayama, 2017, Initiation of DNA Replication at the Chromosomal Origin of E. Coli, OriC, Adv. Exp. Med. Biol., 1042, 79, 10.1007/978-981-10-6955-0_4 · DOI
  18. Mruk, 2014, To Be or Not to Be: Regulation of Restriction-Modification Systems and Other Toxin-Antitoxin Systems, Nucleic Acids Res., 42, 70, 10.1093/nar/gkt711 · DOI
  19. Kobayashi, 2001, Behavior of Restriction-Modification Systems as Selfish Mobile Elements and Their Impact on Genome Evolution, Nucleic Acids Res., 29, 3742, 10.1093/nar/29.18.3742 · DOI · Paper page
  20. Kong, 2013, Homologous Recombination Drives Both Sequence Diversity and Gene Content Variation in Neisseria Meningitidis, Genome Biol. Evol., 5, 1611, 10.1093/gbe/evt116 · DOI
  21. Fullmer, M.S., Ouellette, M., Louyakis, A.S., Papke, R.T., and Gogarten, J.P. (2019). The Patchy Distribution of Restriction–Modification System Genes and the Conservation of Orphan Methyltransferases in Halobacteria. Genes, 10. · DOI
  22. Smith, 2014, TstI, a Type II Restriction-Modification Protein with DNA Recognition, Cleavage and Methylation Functions in a Single Polypeptide, Nucleic Acids Res., 42, 5809, 10.1093/nar/gku187 · DOI
  23. Mavrich, 2017, Bacteriophage Evolution Differs by Host, Lifestyle and Genome, Nat. Microbiol., 2, 17112, 10.1038/nmicrobiol.2017.112 · DOI
  24. Cresawn, S.G., Bogel, M., Day, N., Jacobs-Sera, D., Hendrix, R.W., and Hatfull, G.F. (2011). Phamerator: A Bioinformatic Tool for Comparative Bacteriophage Genomics. BMC Bioinform., 12. · DOI
  25. Altschul, 1997, Gapped BLAST and PSI-BLAST: A New Generation of Protein Database Search Programs, Nucleic Acids Res., 25, 3389, 10.1093/nar/25.17.3389 · DOI · Paper page
  26. Zimmermann, 2018, A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at Its Core, J. Mol. Biol., 430, 2237, 10.1016/j.jmb.2017.12.007 · DOI · Paper page
  27. Katoh, 2013, MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability, Mol. Biol. Evol., 30, 772, 10.1093/molbev/mst010 · DOI · Paper page
  28. Gouy, 2021, Seaview Version 5: A Multiplatform Software for Multiple Sequence Alignment, Molecular Phylogenetic Analyses, and Tree Reconciliation, Methods Mol. Biol., 2231, 241, 10.1007/978-1-0716-1036-7_15 · DOI
  29. Minh, 2020, IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era, Mol. Biol. Evol., 37, 1530, 10.1093/molbev/msaa015 · DOI · Paper page
  30. Meng, E.C., Pettersen, E.F., Couch, G.S., Huang, C.C., and Ferrin, T.E. (2006). Tools for Integrated Sequence-Structure Analysis with UCSF Chimera. BMC Bioinform., 7. · DOI
  31. Kishino, 1989, Evaluation of the Maximum Likelihood Estimate of the Evolutionary Tree Topologies from DNA Sequence Data, and the Branching Order in Hominoidea, J. Mol. Evol., 29, 170, 10.1007/BF02100115 · DOI
  32. Shimodaira, 1999, Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference, Mol. Biol. Evol., 16, 1114, 10.1093/oxfordjournals.molbev.a026201 · DOI · Paper page
  33. Shimodaira, 2002, An Approximately Unbiased Test of Phylogenetic Tree Selection, Syst. Biol., 51, 492, 10.1080/10635150290069913 · DOI · Paper page
  34. Nguyen, 2015, IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies, Mol. Biol. Evol., 32, 268, 10.1093/molbev/msu300 · DOI · Paper page
  35. Labrie, 2010, Bacteriophage Resistance Mechanisms, Nat. Rev. Microbiol., 8, 317, 10.1038/nrmicro2315 · DOI
  36. Bellas, 2020, Flexible Genes Establish Widespread Bacteriophage Pan-Genomes in Cryoconite Hole Ecosystems, Nat. Commun., 11, 4403, 10.1038/s41467-020-18236-8 · DOI
  37. HERSHEY, 1952, Independent Functions of Viral Protein and Nucleic Acid in Growth of Bacteriophage, J. Gen. Physiol., 36, 39, 10.1085/jgp.36.1.39 · DOI
  38. Luria, 1947, Reactivation of Irradiated Bacteriophage by Transfer of Self-Reproducing Units, Proc. Natl. Acad. Sci. USA, 33, 253, 10.1073/pnas.33.9.253 · DOI

Metadata

Authors
Gosselin, S., Arsenault, D., Jennings, C., & Gogarten, J.
Affiliations
University of Connecticut (US)
Corresponding author
Gogarten, Johann
ORCID
Venue
Genes
Publisher
MDPI AG
Published
2023-01-21
Volume
14
Issue
2
Pages
288
ISSN
2073-4425 (ISSN-L)
DOI
10.3390/genes14020288
PMC
PMC9957025
OpenAlex
W4317930438
Cited by
3
References
2
Citations by year
2025: 2 · 2023: 1
FWCI
0.49
Type
journal article
Language
en
Open access
Licence
Locations
  • Genes (publishedVersion, cc-by)
  • Preprints.org (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
National Science Foundation (NSF/MCB 1716046)
Topics
  • Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
DNA methyltransferases, intein, horizontal gene transfer, actinophages, homing endonucleases, restriction-modification systems, phage evolution, insertion elements, reticulate evolution
MeSH terms
DNA, Endonucleases, Evolution, Molecular, Gene Transfer, Horizontal, Inteins

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