CoChat
Sign Up
Cited by 8Bacteriophages and microbial interactionsBacterial Genetics and BiotechnologyCRISPR and Genetic Engineering

The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.

Multi-conflict islands are a widespread trend within Serratia spp.

Open access
Cummins, Thomas, Songra, Suraj, Garrett, Stephen R., Blower, Tim R., Mariano, Giuseppina·2024·Cell Reports
DOI 10.1016/j.celrep.2024.115055

Published version of a preprint

Open this paper in CoChat — free account

Abstract

Bacteria carry numerous anti-phage systems in "defense islands" or hotspots. Recent studies have delineated the content and boundaries of these islands in various species, revealing instances of islands that encode additional factors, including antibiotic resistance genes, stress genes, type VI secretion system (T6SS)-dependent effectors, and virulence factors. Our study identifies three defense islands in the Serratia genus with a mixed cargo of anti-phage systems, virulence factors, and different types of anti-bacterial modules, revealing a widespread trend of co-accumulation that extends beyond T6SS-dependent effectors to colicins and contact-dependent inhibition systems. We further report the identification of four distinct anti-phage system/subtypes, including a previously unreported Toll/interleukin (IL)-1 receptor (TIR)-domain-containing system with population-wide immunity, and two loci co-opting a predicted T6SS-related protein for phage defense. This study enhances our understanding of the protein domains that can be co-opted for phage defense, resulting in a highly diversified anti-phage arsenal.

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 · 10.1016/j.celrep.2024.115055

Cites

4 of 4 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: 88

  1. Mayo-Muñoz, 2023, A host of armor: Prokaryotic immune strategies against mobile genetic elements, Cell Rep., 42, 10.1016/j.celrep.2023.112672 · DOI
  2. Doron, 2018, Systematic discovery of antiphage defense systems in the microbial pangenome, Science, 359, 10.1126/science.aar4120 · DOI
  3. Vassallo, 2022, A functional selection reveals previously undetected anti-phage defence systems in the E. coli pangenome, Nat. Microbiol., 7, 1568, 10.1038/s41564-022-01219-4 · DOI
  4. Millman, 2022, An expanded arsenal of immune systems that protect bacteria from phages, Cell Host Microbe, 30, 1556, 10.1016/j.chom.2022.09.017 · DOI · Paper page
  5. Gao, 2020, Diverse Enzymatic Activities Mediate Antiviral Immunity in Prokaryotes, Science, 369, 1077, 10.1126/science.aba0372 · DOI
  6. Millman, 2020, Bacterial Retrons Function In Anti-Phage Defense, Cell, 183, 1551, 10.1016/j.cell.2020.09.065 · DOI
  7. Johnson, 2022, Bacterial gasdermins reveal an ancient mechanism of cell death, Science, 375, 221, 10.1126/science.abj8432 · DOI
  8. Wein, 2023, CARD-like domains mediate anti-phage defense in bacterial gasdermin systems, Preprint at bioRxiv
  9. Duncan-Lowey, 2022, CBASS phage defense and evolution of antiviral nucleotide signaling, Curr. Opin. Immunol., 74, 156, 10.1016/j.coi.2022.01.002 · DOI
  10. Chambers, 2024, A eukaryotic-like ubiquitination system in bacterial antiviral defence, Nature, 631, 843, 10.1038/s41586-024-07730-4 · DOI
  11. Hör, 2024, Bacteria conjugate ubiquitin-like proteins to interfere with phage assembly, Nature, 631, 1, 10.1038/s41586-024-07616-5 · DOI
  12. Ofir, 2021, Antiviral activity of bacterial TIR domains via immune signalling molecules, Nature, 600, 116, 10.1038/s41586-021-04098-7 · DOI
  13. Mariano, 2023, Conserved domains can be found across distinct phage defence systems, Mol. Microbiol., 120, 45, 10.1111/mmi.15047 · DOI
  14. Koopal, 2022, Short prokaryotic Argonaute systems trigger cell death upon detection of invading DNA, Cell, 185, 1471, 10.1016/j.cell.2022.03.012 · DOI
  15. Sparrer, 2023, Editorial: Ubiquitin and ubiquitin-like modifications in viral infection and innate immunity, Front. Immunol., 14, 10.3389/fimmu.2023.1148296 · DOI
  16. Vozandychova, 2021, The Ubiquitination System within Bacterial Host–Pathogen Interactions, Microorganisms, 9, 638, 10.3390/microorganisms9030638 · DOI
  17. Hu, 2016, Ubiquitin signaling in immune responses, Cell Res., 26, 457, 10.1038/cr.2016.40 · DOI
  18. Makarova, 2011, Defense islands in bacterial and archaeal genomes and prediction of novel defense systems, J. Bacteriol., 193, 6039, 10.1128/JB.05535-11 · DOI
  19. Picton, 2021, The phage defence island of a multidrug resistant plasmid uses both BREX and type IV restriction for complementary protection from viruses, Nucleic Acids Res., 49, 11257, 10.1093/nar/gkab906 · DOI
  20. Hochhauser, 2023, The defense island repertoire of the Escherichia coli pan-genome, PLoS Genet., 19, 10.1371/journal.pgen.1010694 · DOI
  21. Rousset, 2022, Phages and their satellites encode hotspots of antiviral systems, Cell Host Microbe, 30, 740, 10.1016/j.chom.2022.02.018 · DOI
  22. Fillol-Salom, 2022, Bacteriophages benefit from mobilizing pathogenicity islands encoding immune systems against competitors, Cell, 185, 3248, 10.1016/j.cell.2022.07.014 · DOI
  23. Kushwaha, 2023, Genomic plasticity is a blueprint of diversity in Salmonella lineages, Preprint at bioRxiv
  24. Johnson, 2023, Core defense hotspots within Pseudomonas aeruginosa are a consistent and rich source of anti-phage defense systems, Nucleic Acids Res., 51, 4995, 10.1093/nar/gkad317 · DOI
  25. Mahata, 2024, Gamma-Mobile-Trio systems define a new class of mobile elements rich in bacterial defensive and offensive tools, Preprint at bioRxiv
  26. Guzman, 1995, Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter, J. Bacteriol., 177, 4121, 10.1128/jb.177.14.4121-4130.1995 · DOI
  27. Williams, 2022, The genus Serratia revisited by genomics, Nat. Commun., 13, 5195, 10.1038/s41467-022-32929-2 · DOI
  28. Luttmann, 2022, Serratia Marcescens, a Rare and Devastating Cause of Endocarditis: A Case Report and Review of the Literature, Cureus, 14
  29. Tavares-Carreon, 2023, Serratia marcescens antibiotic resistance mechanisms of an opportunistic pathogen: a literature review, PeerJ, 11, 10.7717/peerj.14399 · DOI
  30. Moradigaravand, 2016, Recent independent emergence of multiple multidrug-resistant Serratia marcescens clones within the United Kingdom and Ireland, Genome Res., 26, 1101, 10.1101/gr.205245.116 · DOI
  31. Payne, 2024, New antiviral defences are genetically embedded within prokaryotic immune systems, Preprint at bioRxiv
  32. Steinegger, 2017, MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets, Nat. Biotechnol., 35, 1026, 10.1038/nbt.3988 · DOI · Paper page
  33. Gilchrist, 2021, cblaster: a remote search tool for rapid identification and visualization of homologous gene clusters, Bioinform. Adv., 1, vbab016, 10.1093/bioadv/vbab016 · DOI
  34. Mistry, 2021, Pfam: The protein families database in 2021, Nucleic Acids Res., 49, D412, 10.1093/nar/gkaa913 · DOI · Paper page
  35. Liu, 2022, VFDB 2022: a general classification scheme for bacterial virulence factors, Nucleic Acids Res., 50, D912, 10.1093/nar/gkab1107 · DOI
  36. Shimuta, 2009, The hemolytic and cytolytic activities of Serratia marcescens phospholipase A (PhlA) depend on lysophospholipid production by PhlA, BMC Microbiol., 9, 261, 10.1186/1471-2180-9-261 · DOI
  37. Zhang, 2012, Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics, Biol. Direct, 7, 18, 10.1186/1745-6150-7-18 · DOI
  38. Wood, 2019, The Pseudomonas aeruginosa T6SS Delivers a Periplasmic Toxin that Disrupts Bacterial Cell Morphology, Cell Rep., 29, 187, 10.1016/j.celrep.2019.08.094 · DOI
  39. Ernits, 2023, The structural basis of hyperpromiscuity in a core combinatorial network of type II toxin–antitoxin and related phage defense systems, Proc. Natl. Acad. Sci. USA, 120, 10.1073/pnas.2305393120 · DOI
  40. Zheng, 2011, Genetic Analysis of Anti-Amoebae and Anti-Bacterial Activities of the Type VI Secretion System in Vibrio cholerae, PLoS One, 6, 10.1371/journal.pone.0023876 · DOI
  41. Blankenchip, 2022, Control of bacterial immune signaling by a WYL domain transcription factor, Nucleic Acids Res., 50, 5239, 10.1093/nar/gkac343 · DOI
  42. Picton, 2022, A widespread family of WYL-domain transcriptional regulators co-localizes with diverse phage defence systems and islands, Nucleic Acids Res., 50, 5191, 10.1093/nar/gkac334 · DOI
  43. Iyer, 2008, MutL homologs in restriction-modification systems and the origin of eukaryotic MORC ATPases, Biol. Direct, 3, 8, 10.1186/1745-6150-3-8 · DOI
  44. Kelly, 2023, Diverse Durham collection phages demonstrate complex BREX defense responses, Appl. Environ. Microbiol., 89, e0062323, 10.1128/aem.00623-23 · DOI
  45. Tesson, 2022, Systematic and quantitative view of the antiviral arsenal of prokaryotes, Nat. Commun., 13, 2561, 10.1038/s41467-022-30269-9 · DOI
  46. Ve, 2017, Structural basis of TIR-domain-assembly formation in MAL- and MyD88-dependent TLR4 signaling, Nat. Struct. Mol. Biol., 24, 743, 10.1038/nsmb.3444 · DOI
  47. LeRoux, 2022, The DarTG toxin-antitoxin system provides phage defense by ADP-ribosylating viral DNA, Nat. Microbiol., 7, 1028, 10.1038/s41564-022-01153-5 · DOI
  48. Wang, 2023, NAD+ depletion and defense in bacteria, Trends Microbiol., 31, 435, 10.1016/j.tim.2022.06.002 · DOI
  49. Rao, 2008, The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating Mycobacterium tuberculosis, Proc. Natl. Acad. Sci. USA, 105, 11945, 10.1073/pnas.0711697105 · DOI · Paper page
  50. Karimova, 1998, A bacterial two-hybrid system based on a reconstituted signal transduction pathway, Proc. Natl. Acad. Sci. USA, 95, 5752, 10.1073/pnas.95.10.5752 · DOI
  51. Saha, 2021, FlaGs and webFlaGs: discovering novel biology through the analysis of gene neighbourhood conservation, Bioinformatics, 37, 1312, 10.1093/bioinformatics/btaa788 · DOI
  52. Chatterjee, 2021, Immunoglobulin-fold containing bacterial adhesins: molecular and structural perspectives in host tissue colonization and infection, FEMS Microbiol. Lett., 368, 10.1093/femsle/fnaa220 · DOI
  53. Hallgren, 2022, DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural network, Preprint
  54. Holm, 2020, Using Dali for Protein Structure Comparison, Methods Mol. Biol., 2112, 29, 10.1007/978-1-0716-0270-6_3 · DOI
  55. Deng, 2016, Identification and functional analysis of invasion associated locus B (IalB) in Bartonella species, Microb. Pathog., 98, 171, 10.1016/j.micpath.2016.05.007 · DOI
  56. Botelho, 2023, Phylogroup-specific variation shapes the clustering of antimicrobial resistance genes and defence systems across regions of genome plasticity in Pseudomonas aeruginosa, EBioMedicine, 90, 10.1016/j.ebiom.2023.104532 · DOI
  57. Mahata, 2024, GMT systems define a new class of mobile elements rich in bacterial defensive and offensive tools, Preprint at bioRxiv
  58. Payne, 2021, Identification and classification of antiviral defence systems in bacteria and archaea with PADLOC reveals new system types, Nucleic Acids Res., 49, 10868, 10.1093/nar/gkab883 · DOI
  59. Carabias, 2024, Retron-Eco1 assembles NAD+-hydrolyzing filaments that provide immunity against bacteriophages, Mol. Cell, 84, 2185, 10.1016/j.molcel.2024.05.001 · DOI
  60. Garb, 2022, Multiple phage resistance systems inhibit infection via SIR2-dependent NAD+ depletion, Nat. Microbiol., 7, 1849, 10.1038/s41564-022-01207-8 · DOI
  61. Andryka-Cegielski, 2023, Unexpected bonds: ubiquitin-like conjugation of cGAS/CD-NTases supports their enzymatic activity and antiphage defense, Sig. Transduct. Target Ther., 8, 308, 10.1038/s41392-023-01549-7 · DOI
  62. Jenson, 2023, Ubiquitin-like conjugation by bacterial cGAS enhances anti-phage defence, Nature, 616, 326, 10.1038/s41586-023-05862-7 · DOI
  63. Kelly, 2023, Toxin-antitoxin systems as mediators of phage defence and the implications for abortive infection, Curr. Opin. Microbiol., 73, 10.1016/j.mib.2023.102293 · DOI
  64. Song, 2020, A Primary Physiological Role of Toxin/Antitoxin Systems Is Phage Inhibition, Front. Microbiol., 11, 1895, 10.3389/fmicb.2020.01895 · DOI
  65. Keating, 2009, Role of Non-degradative Ubiquitination in Interleukin-1 and Toll-like Receptor Signaling, J. Biol. Chem., 284, 8211, 10.1074/jbc.R800038200 · DOI
  66. Yang, 2024, Molecular basis of Gabija anti-phage supramolecular assemblies, Nat. Struct. Mol. Biol., 31, 1243, 10.1038/s41594-024-01283-w · DOI · Paper page
  67. Burman, 2024, Viral proteins activate PARIS-mediated tRNA degradation and viral tRNAs rescue infection, bioRxiv, 2024
  68. Macdonald, 2023, The novel anti-phage system Shield co-opts an RmuC domain to mediate phage defense across Pseudomonas species, PLoS Genet., 19, 10.1371/journal.pgen.1010784 · DOI
  69. Gerdes, 2024, Diverse genetic contexts of HicA toxin domains propose a role in anti-phage defense, mBio, 15, 10.1128/mbio.03293-23 · DOI · Paper page
  70. LeRoux, 2022, Toxin-Antitoxin Systems as Phage Defense Elements, Annu. Rev. Microbiol., 76, 21, 10.1146/annurev-micro-020722-013730 · DOI
  71. Fraser, 2007, Immunoglobulin-like domains on bacteriophage: weapons of modest damage?, Curr. Opin. Microbiol., 10, 382, 10.1016/j.mib.2007.05.018 · DOI
  72. Orzechowska, B., Mohammed, M., Orzechowska, B., and Mohammed, M. (2019). The War between Bacteria and Bacteriophages. In Growing and Handling of Bacterial Cultures (IntechOpen). 10.5772/intechopen.87247. · DOI
  73. Labrie, 2010, Bacteriophage resistance mechanisms, Nat. Rev. Microbiol., 8, 317, 10.1038/nrmicro2315 · DOI
  74. Yamada, 1981, Arrangement of bacteriophage lambda receptor protein (LamB) in the cell surface of Escherichia coli: a reconstitution study, J. Bacteriol., 147, 660, 10.1128/jb.147.2.660-669.1981 · DOI
  75. Maier, 1988, Pore-forming activity of the Tsx protein from the outer membrane of Escherichia coli. Demonstration of a nucleoside-specific binding site, J. Biol. Chem., 263, 2493, 10.1016/S0021-9258(18)69233-6 · DOI
  76. Achtman, 1977, Cell--cell interactions in conjugating Escherichia coli: role of traT protein in surface exclusion, Proc. Natl. Acad. Sci. USA, 74, 5104, 10.1073/pnas.74.11.5104 · DOI
  77. Smug, 2023, Ongoing shuffling of protein fragments diversifies core viral functions linked to interactions with bacterial hosts, Nat. Commun., 14, 7460, 10.1038/s41467-023-43236-9 · DOI
  78. Gencay, 2018, Phase Variable Expression of a Single Phage Receptor in Campylobacter jejuni NCTC12662 Influences Sensitivity Toward Several Diverse CPS-Dependent Phages, Front. Microbiol., 9, 82, 10.3389/fmicb.2018.00082 · DOI
  79. Ostrowski, 2018, Killing with proficiency: Integrated post-translational regulation of an offensive Type VI secretion system, PLoS Pathog., 14, 10.1371/journal.ppat.1007230 · DOI
  80. Quinlan, 2010, BEDTools: a flexible suite of utilities for comparing genomic features, Bioinformatics, 26, 841, 10.1093/bioinformatics/btq033 · DOI · Paper page
  81. Shirley, M.D., Ma, Z., Pedersen, B.S., and Wheelan, S.J. (2015). Efficient “Pythonic” Access to FASTA Files Using Pyfaidx (PeerJ Inc.) 10.7287/peerj.preprints.970v1. · DOI
  82. Cock, 2009, Biopython: freely available Python tools for computational molecular biology and bioinformatics, Bioinformatics, 25, 1422, 10.1093/bioinformatics/btp163 · DOI · Paper page
  83. Akhter, 2012, PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies, Nucleic Acids Res., 40, 10.1093/nar/gks406 · DOI
  84. Jain, 2018, High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries, Nat. Commun., 9, 5114, 10.1038/s41467-018-07641-9 · DOI · Paper page
  85. Néron, 2022, IntegronFinder 2.0: Identification and Analysis of Integrons across Bacteria, with a Focus on Antibiotic Resistance in Klebsiella, Microorganisms, 10, 700, 10.3390/microorganisms10040700 · DOI
  86. Feldgarden, 2021, AMRFinderPlus and the Reference Gene Catalog facilitate examination of the genomic links among antimicrobial resistance, stress response, and virulence, Sci. Rep., 11, 10.1038/s41598-021-91456-0 · DOI
  87. Zhang, 2023, SecReT6 update: a comprehensive resource of bacterial Type VI Secretion Systems, Sci. China Life Sci., 66, 626, 10.1007/s11427-022-2172-x · DOI
  88. Söding, 2005, The HHpred interactive server for protein homology detection and structure prediction, Nucleic Acids Res., 33, W244, 10.1093/nar/gki408 · DOI

Metadata

Authors
Cummins, T., Songra, S., Garrett, S. R., Blower, T. R., & Mariano, G.
Affiliations
  • University of Surrey (GB)
  • Michael G. DeGroote Institute for Infectious Disease Research (CA)
  • Durham University (GB)
Corresponding author
Mariano, Giuseppina
ORCID
Venue
Cell Reports
Publisher
Elsevier BV
Published
2024-12
Volume
43
Issue
12
Pages
115055
ISSN
2211-1247 (ISSN-L)
DOI
10.1016/j.celrep.2024.115055
OpenAlex
W4405234112
Cited by
8
References
4
Citations by year
2026: 2 · 2025: 6
FWCI
2.20
Type
journal article
Language
en
Open access
Licence
Locations
  • Cell Reports (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed (publishedVersion)
  • Durham Research Online (Durham University) (publishedVersion, other-oa)
  • ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion, cc-by-sa)
Funders
  • Lister Institute of Preventive Medicine
  • University of Surrey
  • Wellcome Trust (218622/Z/19/Z)
Topics
  • Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
Keywords
Serratia, type VI secretion system, colicins, contact-dependent inhibition, virulence factors, antibiotic resistance genes, phage resistance
MeSH terms
Type VI Secretion Systems, Bacterial Proteins, Bacteriophages, Serratia, Virulence Factors, Genomic Islands

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