1887

Microbial Genomics logo

Volume 9, Issue 12

Distribution and diversity of type VI secretion system clusters in and Open Access

Abstract

Gram-negative bacteria use type VI secretion systems (T6SSs) to antagonize neighbouring cells. Although primarily involved in bacterial competition, the T6SS is also implicated in pathogenesis, biofilm formation and ion scavenging. species belong to the ESKAPE pathogens, and while their antibiotic resistance has been well studied, less is known about their pathogenesis. Here, we investigated the distribution and diversity of T6SS components in isolates of two clinically relevant species, and . T6SS clusters are grouped into four types (T6SS-T6SS), of which type i can be further divided into six subtypes (i1, i2, i3, i4a, i4b, i5). Analysis of a curated dataset of 31 strains demonstrated that most of them encode T6SS clusters belonging to the T6SS type. All T6SS-positive strains possessed a conserved i3 cluster, and many harboured one or two additional i2 clusters. These clusters were less conserved, and some strains displayed evidence of deletion. We focused on a pathogenic clinical isolate for comprehensive effector prediction, with comparative analyses across the 31 isolates. Several new effector candidates were identified, including an evolved VgrG with a metallopeptidase domain and a Tse6-like protein. Additional effectors included an anti-eukaryotic catalase (KatN), M23 peptidase, PAAR and VgrG proteins. Our findings highlight the diversity of T6SSs and reveal new putative effectors that may be important for the interaction of these species with neighbouring cells and their environment.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): comparative genomics , T6SS effectors , T6SS gene cluster , T6SS gene organization and T6SS subtype
Funding
This study was supported by the:
  • Biotechnology and Biological Sciences Research Council (Award BB/S006281/1)
    • Principle Award Recipient: MiguelA Valvano
  • Biotechnology and Biological Sciences Research Council (Award BB/T005807/1)
    • Principle Award Recipient: MiguelA Valvano
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001148
2023-12-06
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/12/mgen001148.html?itemId=/content/journal/mgen/10.1099/mgen.0.001148&mimeType=html&fmt=ahah

References

  1. Jean-Pierre F, Vyas A, Hampton TH, Henson MA, O’Toole GA et al. One versus many: polymicrobial communities and the cystic fibrosis airway. mBio 2021; 12: [View Article] [PubMed]
     [Google Scholar]
  2. García-Bayona L, Comstock LE. Bacterial antagonism in host-associated microbial communities. Science 2018; 361: [View Article] [PubMed]
     [Google Scholar]
  3. Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 2010; 8:15–25 [View Article] [PubMed]
     [Google Scholar]
  4. Whitney JC, Peterson SB, Kim J, Pazos M, Verster AJ et al. A broadly distributed toxin family mediates contact-dependent antagonism between gram-positive bacteria. Elife 2017; 6:e26938 [View Article] [PubMed]
     [Google Scholar]
  5. Aoki SK, Pamma R, Hernday AD, Bickham JE, Braaten BA et al. Contact-dependent inhibition of growth in Escherichia coli. Science 2005; 309:1245–1248 [View Article] [PubMed]
     [Google Scholar]
  6. Cascales E, Buchanan SK, Duché D, Kleanthous C, Lloubès R et al. Colicin biology. Microbiol Mol Biol Rev 2007; 71:158–229 [View Article] [PubMed]
     [Google Scholar]
  7. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W et al. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 2011; 475:343–347 [View Article] [PubMed]
     [Google Scholar]
  8. Hespanhol JT, Sanchez-Limache DE, Nicastro GG, Mead L, Llontop EE et al. Antibacterial T6SS effectors with a VRR-Nuc domain are structure-specific nucleases. eLife 2022; 11: [View Article] [PubMed]
     [Google Scholar]
  9. Le NH, Pinedo V, Lopez J, Cava F, Feldman MF. Killing of Gram-negative and Gram-positive bacteria by a bifunctional cell wall-targeting T6SS effector. Proc Natl Acad Sci USA 2021; 118: [View Article] [PubMed]
     [Google Scholar]
  10. Park YJ, Lacourse KD, Cambillau C, DiMaio F, Mougous JD et al. Structure of the type VI secretion system TssK–TssF–TssG baseplate subcomplex revealed by cryo-electron microscopy. Nat Commun 2018; 9: [View Article] [PubMed]
     [Google Scholar]
  11. Durand E, Nguyen VS, Zoued A, Logger L, Péhau-Arnaudet G et al. Biogenesis and structure of a type VI secretion membrane core complex. Nature 2015; 523:555–560 [View Article] [PubMed]
     [Google Scholar]
  12. Zoued A, Brunet YR, Durand E, Aschtgen M-S, Logger L et al. Architecture and assembly of the Type VI secretion system. Biochim Biophys Acta 2014; 1843:1664–1673 [View Article] [PubMed]
     [Google Scholar]
  13. Douzi B, Spinelli S, Blangy S, Roussel A, Durand E et al. Crystal structure and self-interaction of the type VI secretion tail-tube protein from enteroaggregative Escherichia coli. PLoS One 2014; 9:e86918 [View Article] [PubMed]
     [Google Scholar]
  14. Stietz MS, Liang X, Li H, Zhang X, Dong TG. TssA-TssM-TagA interaction modulates type VI secretion system sheath-tube assembly in Vibrio cholerae. Nat Commun 2020; 11:5065 [View Article] [PubMed]
     [Google Scholar]
  15. Dix SR, Owen HJ, Sun R, Ahmad A, Shastri S et al. Structural insights into the function of type VI secretion system TssA subunits. Nat Commun 2018; 9: [View Article] [PubMed]
     [Google Scholar]
  16. Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 2012; 483:182–186 [View Article] [PubMed]
     [Google Scholar]
  17. Zhou Y, Tao J, Yu H, Ni J, Zeng L et al. Hcp family proteins secreted via the type VI secretion system coordinately regulate Escherichia coli K1 interaction with human brain microvascular endothelial cells. Infect Immun 2012; 80:1243–1251 [View Article] [PubMed]
     [Google Scholar]
  18. Pissaridou P, Allsopp LP, Wettstadt S, Howard SA, Mavridou DAI et al. The Pseudomonas aeruginosa T6SS-VgrG1b spike is topped by a PAAR protein eliciting DNA damage to bacterial competitors. Proc Natl Acad Sci U S A 2018; 115:12519–12524 [View Article] [PubMed]
     [Google Scholar]
  19. Suarez G, Sierra JC, Erova TE, Sha J, Horneman AJ et al. A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J Bacteriol 2010; 192:155–168 [View Article] [PubMed]
     [Google Scholar]
  20. Flaugnatti N, Le TTH, Canaan S, Aschtgen M-S, Nguyen VS et al. A phospholipase A1 antibacterial Type VI secretion effector interacts directly with the C-terminal domain of the VgrG spike protein for delivery. Mol Microbiol 2016; 99:1099–1118 [View Article] [PubMed]
     [Google Scholar]
  21. Ma S, Dong Y, Wang N, Liu J, Lu C et al. Identification of a new effector-immunity pair of Aeromonas hydrophila type VI secretion system. Vet Res 2020; 51: [View Article] [PubMed]
     [Google Scholar]
  22. Dong TG, Ho BT, Yoder-Himes DR, Mekalanos JJ. Identification of T6SS-dependent effector and immunity proteins by Tn-seq in Vibrio cholerae. Proc Natl Acad Sci U S A 2013; 110:2623–2628 [View Article] [PubMed]
     [Google Scholar]
  23. Lin J, Zhang W, Cheng J, Yang X, Zhu K et al. A Pseudomonas T6SS effector recruits PQS-containing outer membrane vesicles for iron acquisition. Nat Commun 2017; 8:14888 [View Article] [PubMed]
     [Google Scholar]
  24. Jiang F, Wang X, Wang B, Chen L, Zhao Z et al. The Pseudomonas aeruginosa type VI secretion PGAP1-like effector induces host autophagy by activating endoplasmic reticulum stress. Cell Reports 2016; 16:1502–1509 [View Article] [PubMed]
     [Google Scholar]
  25. Russell AB, LeRoux M, Hathazi K, Agnello DM, Ishikawa T et al. Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 2013; 496:508–512 [View Article] [PubMed]
     [Google Scholar]
  26. Sana TG, Baumann C, Merdes A, Soscia C, Rattei T et al. Internalization of Pseudomonas aeruginosa strain PAO1 into epithelial cells is promoted by interaction of a T6SS effector with the microtubule network. mBio 2015; 6:e00712 [View Article] [PubMed]
     [Google Scholar]
  27. Jiang F, Waterfield NR, Yang J, Yang G, Jin Q. A Pseudomonas aeruginosa type VI secretion phospholipase D effector targets both prokaryotic and eukaryotic cells. Cell Host Microbe 2014; 15:600–610 [View Article] [PubMed]
     [Google Scholar]
  28. Jana B, Keppel K, Fridman CM, Bosis E, Salomon D. Multiple T6SSs, mobile auxiliary modules, and effectors revealed in a systematic analysis of the Vibrio parahaemolyticus pan-genome. mSystems 2022; 7:e0072322 [View Article] [PubMed]
     [Google Scholar]
  29. Morgado S, Vicente AC. Diversity and distribution of type VI secretion system gene clusters in bacterial plasmids. Sci Rep 2022; 12:8249 [View Article] [PubMed]
     [Google Scholar]
  30. Crisan CV, Chande AT, Williams K, Raghuram V, Rishishwar L et al. Analysis of Vibrio cholerae genomes identifies new type VI secretion system gene clusters. Genome Biol 2019; 20:163 [View Article] [PubMed]
     [Google Scholar]
  31. Han Y, Wang T, Chen G, Pu Q, Liu Q et al. A Pseudomonas aeruginosa type VI secretion system regulated by CueR facilitates copper acquisition. PLOS Pathog 2019; 15:e1008198 [View Article] [PubMed]
     [Google Scholar]
  32. Aubert DF, Xu H, Yang J, Shi X, Gao W et al. A Burkholderia type VI effector deamidates rho GTPases to activate the pyrin inflammasome and trigger inflammation. Cell Host Microbe 2016; 19:664–674 [View Article] [PubMed]
     [Google Scholar]
  33. Yang Y, Pan D, Tang Y, Li J, Zhu K et al. H3-T6SS of Pseudomonas aeruginosa PA14 contributes to environmental adaptation via secretion of a biofilm-promoting effector. Stress Biol 2022; 2:55 [View Article] [PubMed]
     [Google Scholar]
  34. Trunk K, Peltier J, Liu Y-C, Dill BD, Walker L et al. The type VI secretion system deploys antifungal effectors against microbial competitors. Nat Microbiol 2018; 3:920–931 [View Article] [PubMed]
     [Google Scholar]
  35. Wenren LM, Sullivan NL, Cardarelli L, Septer AN, Gibbs KA. Two independent pathways for self-recognition in Proteus mirabilis are linked by type VI-dependent export. mBio 2013; 4:e00374-13 [View Article] [PubMed]
     [Google Scholar]
  36. Eshraghi A, Kim J, Walls AC, Ledvina HE, Miller CN et al. Secreted effectors encoded within and outside of the Francisella pathogenicity island promote intramacrophage growth. Cell Host Microbe 2016; 20:573–583 [View Article] [PubMed]
     [Google Scholar]
  37. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci USA 2007; 104:15508–15513 [View Article] [PubMed]
     [Google Scholar]
  38. Zong B, Zhang Y, Wang X, Liu M, Zhang T et al. Characterization of multiple type-VI secretion system (T6SS) VgrG proteins in the pathogenicity and antibacterial activity of porcine extra-intestinal pathogenic Escherichia coli. Virulence 2019; 10:118–132 [View Article] [PubMed]
     [Google Scholar]
  39. Ringel PD, Hu D, Basler M. The role of type VI secretion system effectors in target cell lysis and subsequent horizontal gene transfer. Cell Reports 2017; 21:3927–3940 [View Article] [PubMed]
     [Google Scholar]
  40. Soria-Bustos J, Ares MA, Gómez-Aldapa CA, González-Y-Merchand JA, Girón JA et al. Two type VI secretion systems of Enterobacter cloacae are required for bacterial competition, cell adherence, and intestinal colonization. Front Microbiol 2020; 11:560488 [View Article] [PubMed]
     [Google Scholar]
  41. Zhang H, Zhang H, Gao Z-Q, Wang W-J, Liu G-F et al. Structure of the type VI effector-immunity complex (Tae4-Tai4) provides novel insights into the inhibition mechanism of the effector by its immunity protein. J Biol Chem 2013; 288:5928–5939 [View Article] [PubMed]
     [Google Scholar]
  42. Lery LMS, Frangeul L, Tomas A, Passet V, Almeida AS et al. Comparative analysis of Klebsiella pneumoniae genomes identifies a phospholipase D family protein as a novel virulence factor. BMC Biol 2014; 12:41 [View Article] [PubMed]
     [Google Scholar]
  43. Carruthers MD, Nicholson PA, Tracy EN, Munson RS, Cascales E. Acinetobacter baumannii utilizes a type VI secretion system for bacterial competition. PLoS One 2013; 8:e59388 [View Article] [PubMed]
     [Google Scholar]
  44. Wang J, Zhou Z, He F, Ruan Z, Jiang Y et al. The role of the type VI secretion system vgrG gene in the virulence and antimicrobial resistance of Acinetobacter baumannii ATCC 19606. PLoS One 2018; 13:e0192288 [View Article] [PubMed]
     [Google Scholar]
  45. Wu W, Feng Y, Zong Z. Precise species identification for Enterobacter: a genome sequence-based study with reporting of two novel species, Enterobacter quasiroggenkampii sp. nov. and Enterobacter quasimori sp. nov. mSystems 2020; 5:e00527-20 [View Article] [PubMed]
     [Google Scholar]
  46. Zong Z, Feng Y, McNally A. Carbapenem and colistin resistance in Enterobacter: determinants and clones. Trends Microbiol 2021; 29:473–476 [View Article] [PubMed]
     [Google Scholar]
  47. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70:5607–5612 [View Article] [PubMed]
     [Google Scholar]
  48. Girlich D, Ouzani S, Emeraud C, Gauthier L, Bonnin RA et al. Uncovering the novel Enterobacter cloacae complex species responsible for septic shock deaths in newborns: a cohort study. Lancet Microbe 2021; 2:e536–e544 [View Article] [PubMed]
     [Google Scholar]
  49. Maheshwari N, Shefler A. . Enterobacter cloacae: an “ICU bug” causing community acquired necrotizing meningo-encephalitis. Eur J Pediatr 2009; 168:503–505 [View Article] [PubMed]
     [Google Scholar]
  50. Ferry A, Plaisant F, Ginevra C, Dumont Y, Grando J et al.. Enterobacter cloacae colonisation and infection in a neonatal intensive care unit: retrospective investigation of preventive measures implemented after a multiclonal outbreak. BMC Infect Dis 2020; 20:682 [View Article] [PubMed]
     [Google Scholar]
  51. Hernandez-Alonso E, Bourgeois-Nicolaos N, Lepainteur M, Derouin V, Barreault S et al. Contaminated incubators: source of a multispecies Enterobacter outbreak of neonatal sepsis. Microbiol Spectr 2022; 10:e00964–22 [View Article] [PubMed]
     [Google Scholar]
  52. Donato SL, Beck CM, Garza-Sánchez F, Jensen SJ, Ruhe ZC et al. The β-encapsulation cage of rearrangement hotspot (Rhs) effectors is required for type VI secretion. Proc Natl Acad Sci USA 2020; 117:33540–33548 [View Article] [PubMed]
     [Google Scholar]
  53. Doijad S, Imirzalioglu C, Yao Y, Pati NB, Falgenhauer L et al. Enterobacter bugandensis sp. nov., isolated from neonatal blood. Int J Syst Evol Microbiol 2016; 66:968–974 [View Article] [PubMed]
     [Google Scholar]
  54. Pati NB, Doijad SP, Schultze T, Mannala GK, Yao Y et al. Enterobacter bugandensis: a novel enterobacterial species associated with severe clinical infection. Sci Rep 2018; 8:5392 [View Article] [PubMed]
     [Google Scholar]
  55. Hervas JA, Ballesteros F, Alomar A, Gil J, Benedi VJ et al. Increase of Enterobacter in neonatal sepsis: a twenty-two-year study. Pediatr Infect Dis J 2001; 20:134–140 [View Article] [PubMed]
     [Google Scholar]
  56. Dalben M, Varkulja G, Basso M, Krebs VLJ, Gibelli MA et al. Investigation of an outbreak of Enterobacter cloacae in a neonatal unit and review of the literature. J Hosp Infect 2008; 70:7–14 [View Article] [PubMed]
     [Google Scholar]
  57. Mezzatesta ML, Gona F, Stefani S. . Enterobacter cloacae complex: clinical impact and emerging antibiotic resistance. Future Microbiol 2012; 7:887–902 [View Article] [PubMed]
     [Google Scholar]
  58. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10: [View Article] [PubMed]
     [Google Scholar]
  59. Zhang J, Guan J, Wang M, Li G, Djordjevic M et al. SecReT6 update: a comprehensive resource of bacterial type VI secretion systems. Sci China Life Sci 2023; 66:626–634 [View Article] [PubMed]
     [Google Scholar]
  60. Li J, Yao Y, Xu HH, Hao L, Deng Z et al. SecReT6: a web-based resource for type VI secretion systems found in bacteria. Environ Microbiol 2015; 17:2196–2202 [View Article] [PubMed]
     [Google Scholar]
  61. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
     [Google Scholar]
  62. Gilchrist CLM, Booth TJ, van Wersch B, van Grieken L, Medema MH et al. cblaster: a remote search tool for rapid identification and visualization of homologous gene clusters. Bioinform Adv 2021; 1:vbab016 [View Article] [PubMed]
     [Google Scholar]
  63. Gilchrist CLM, Chooi Y-H, Robinson P. clinker & clustermap.js: automatic generation of gene cluster comparison figures. Bioinformatics 2021; 37:2473–2475 [View Article] [PubMed]
     [Google Scholar]
  64. Wang J, Yang B, Leier A, Marquez-Lago TT, Hayashida M et al. Bastion6: a bioinformatics approach for accurate prediction of type VI secreted effectors. Bioinformatics 2018; 34:2546–2555 [View Article] [PubMed]
     [Google Scholar]
  65. Söding J, Biegert A, Lupas AN. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 2005; 33:W244–8 [View Article] [PubMed]
     [Google Scholar]
  66. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 2015; 10:845–858 [View Article] [PubMed]
     [Google Scholar]
  67. Holm L. Dali server: structural unification of protein families. Nucleic Acids Res 2022; 50:W210–W215 [View Article] [PubMed]
     [Google Scholar]
  68. McGinnis S, Madden TL. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 2004; 32:W20–5 [View Article] [PubMed]
     [Google Scholar]
  69. Marchler-Bauer A, Bryant SH. CD-Search: protein domain annotations on the fly. Nucleic Acids Res 2004; 32:W327–31 [View Article] [PubMed]
     [Google Scholar]
  70. Teufel F, Almagro Armenteros JJ, Johansen AR, Gíslason MH, Pihl SI et al. SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat Biotechnol 2022; 40:1023–1025 [View Article] [PubMed]
     [Google Scholar]
  71. Bendtsen JD, Kiemer L, Fausbøll A, Brunak S. Non-classical protein secretion in bacteria. BMC Microbiol 2005; 5: [View Article] [PubMed]
     [Google Scholar]
  72. Mirdita M, Schütze K, Moriwaki Y, Heo L, Ovchinnikov S et al. ColabFold: making protein folding accessible to all. Nat Methods 2022; 19:679–682 [View Article] [PubMed]
     [Google Scholar]
  73. Russell AB, Wexler AG, Harding BN, Whitney JC, Bohn AJ et al. A type VI secretion-related pathway in bacteroidetes mediates interbacterial antagonism. Cell Host Microbe 2014; 16:227–236 [View Article] [PubMed]
     [Google Scholar]
  74. Barret M, Egan F, O’Gara F. Distribution and diversity of bacterial secretion systems across metagenomic datasets. Environ Microbiol Rep 2013; 5:117–126 [View Article] [PubMed]
     [Google Scholar]
  75. Barret M, Egan F, Fargier E, Morrissey JP, O’Gara F. Genomic analysis of the type VI secretion systems in Pseudomonas spp.: novel clusters and putative effectors uncovered. Microbiology 2011; 157:1726–1739 [View Article] [PubMed]
     [Google Scholar]
  76. Mushtaq S, Reynolds R, Gilmore MC, Esho O, Adkin R et al. Inherent colistin resistance in genogroups of the Enterobacter cloacae complex: epidemiological, genetic and biochemical analysis from the BSAC Resistance Surveillance Programme. J Antimicrob Chemother 2020; 75:2452–2461 [View Article] [PubMed]
     [Google Scholar]
  77. Schmidt H, Hensel M. Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 2004; 17:14–56 [View Article] [PubMed]
     [Google Scholar]
  78. Wood TE, Howard SA, Förster A, Nolan LM, Manoli E et al. The Pseudomonas aeruginosa T6SS delivers a periplasmic toxin that disrupts bacterial cell morphology. Cell Reports 2019; 29:187–201 [View Article] [PubMed]
     [Google Scholar]
  79. Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ et al. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 2013; 500:350–353 [View Article] [PubMed]
     [Google Scholar]
  80. Uchida K, Leiman PG, Arisaka F, Kanamaru S. Structure and properties of the C-terminal β-helical domain of VgrG protein from Escherichia coli O157. J Biochem 2014; 155:173–182 [View Article] [PubMed]
     [Google Scholar]
  81. Quentin D, Ahmad S, Shanthamoorthy P, Mougous JD, Whitney JC et al. Mechanism of loading and translocation of type VI secretion system effector Tse6. Nat Microbiol 2018; 3:1142–1152 [View Article] [PubMed]
     [Google Scholar]
  82. Alcoforado Diniz J, Coulthurst SJ, Christie PJ. Intraspecies competition in Serratia marcescens is mediated by type VI-secreted Rhs effectors and a conserved effector-associated accessory protein. J Bacteriol 2015; 197:2350–2360 [View Article] [PubMed]
     [Google Scholar]
  83. Günther P, Quentin D, Ahmad S, Sachar K, Gatsogiannis C et al. Structure of a bacterial Rhs effector exported by the type VI secretion system. PLoS Pathog 2022; 18:e1010182 [View Article] [PubMed]
     [Google Scholar]
  84. Kung VL, Khare S, Stehlik C, Bacon EM, Hughes AJ et al. An rhs gene of Pseudomonas aeruginosa encodes a virulence protein that activates the inflammasome. Proc Natl Acad Sci U S A 2012; 109:1275–1280 [View Article] [PubMed]
     [Google Scholar]
  85. Lu W, Tan J, Lu H, Wang G, Dong W et al. Function of Rhs proteins in porcine extraintestinal pathogenic Escherichia coli PCN033. J Microbiol 2021; 59:854–860 [View Article] [PubMed]
     [Google Scholar]
  86. Whitney JC, Quentin D, Sawai S, LeRoux M, Harding BN et al. An interbacterial NAD(P)+ glycohydrolase toxin requires elongation factor tu for delivery to target cells. Cell 2015; 163:607–619 [View Article] [PubMed]
     [Google Scholar]
  87. Ting S-Y, Bosch DE, Mangiameli SM, Radey MC, Huang S et al. Bifunctional immunity proteins protect bacteria against FtsZ-targeting ADP-ribosylating toxins. Cell 2018; 175:1380–1392 [View Article] [PubMed]
     [Google Scholar]
  88. Razew A, Schwarz JN, Mitkowski P, Sabala I, Kaus-Drobek M. One fold, many functions—M23 family of peptidoglycan hydrolases. Front Microbiol 2022; 13: [View Article] [PubMed]
     [Google Scholar]
  89. Zhang Z, Liu Y, Zhang P, Wang J, Li D et al. PAAR proteins are versatile clips that enrich the antimicrobial weapon arsenals of prokaryotes. mSystems 2021; 6:e00953–21 [View Article] [PubMed]
     [Google Scholar]
  90. Dingemans J, Ghequire MGK, Craggs M, De Mot R, Cornelis P. Identification and functional analysis of a bacteriocin, pyocin S6, with ribonuclease activity from a Pseudomonas aeruginosa cystic fibrosis clinical isolate. Microbiologyopen 2016; 5:413–423 [View Article] [PubMed]
     [Google Scholar]
  91. Carr S, Walker D, James R, Kleanthous C, Hemmings AM. Inhibition of a ribosome-inactivating ribonuclease: the crystal structure of the cytotoxic domain of colicin E3 in complex with its immunity protein. Structure 2000; 8:949–960 [View Article] [PubMed]
     [Google Scholar]
  92. Ma J, Pan Z, Huang J, Sun M, Lu C et al. The Hcp proteins fused with diverse extended-toxin domains represent a novel pattern of antibacterial effectors in type VI secretion systems. Virulence 2017; 8:1189–1202 [View Article] [PubMed]
     [Google Scholar]
  93. Doijad SP, Gisch N, Frantz R, Kumbhar BV, Falgenhauer J et al. Resolving colistin resistance and heteroresistance in Enterobacter species. Nat Commun 2023; 14:140 [View Article] [PubMed]
     [Google Scholar]
  94. Vettiger A, Basler M. Type VI secretion system substrates are transferred and reused among sister cells. Cell 2016; 167:99–110 [View Article] [PubMed]
     [Google Scholar]
  95. Wan B, Zhang Q, Ni J, Li S, Wen D et al. Type VI secretion system contributes to Enterohemorrhagic Escherichia coli virulence by secreting catalase against host reactive oxygen species (ROS). PLoS Pathog 2017; 13:e1006246 [View Article] [PubMed]
     [Google Scholar]
  96. Lopez J, Ly PM, Feldman MF. The tip of the VgrG spike is essential to functional type VI secretion system assembly in Acinetobacter baumannii. mBio 2020; 11:e02761-19 [View Article] [PubMed]
     [Google Scholar]
  97. Storey D, McNally A, Åstrand M, sa-Pessoa Graca Santos J, Rodriguez-Escudero I et al. Klebsiella pneumoniae type VI secretion system-mediated microbial competition is PhoPQ controlled and reactive oxygen species dependent. PLoS Pathog 2020; 16:e1007969 [View Article] [PubMed]
     [Google Scholar]
  98. Sá-Pessoa J, López-Montesino S, Przybyszewska K, Rodríguez-Escudero I, Marshall H et al. A trans-kingdom T6SS effector induces the fragmentation of the mitochondrial network and activates innate immune receptor NLRX1 to promote infection. Nat Commun 2023; 14:871 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.001148
Loading
Distribution and diversity of type VI secretion system clusters in Enterobacter bugandensis and Enterobacter cloacae
M Gen 9, 001148 (2023); https://doi.org/10.1099/mgen.0.001148
/content/journal/mgen/10.1099/mgen.0.001148
/content/journal/mgen/10.1099/mgen.0.001148
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error