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Volume 170, Issue 2

utilises colicins during inter-bacterial competition Open Access

Abstract

The mammalian colon is one of the most densely populated habitats currently recognised, with 10–10 commensal bacteria per gram of colonic contents. Enteric pathogens must compete with the resident intestinal microbiota to cause infection. Among these enteric pathogens are species which cause approximately 125 million infections annually, of which over 90 % are caused by and was previously reported to use a Type VI Secretion System (T6SS) to outcompete and in and experiments. strains have also been reported to harbour colicinogenic plasmids, which are an alternative anti-bacterial mechanism that could provide a competitive advantage against the intestinal microbiota. We sought to determine the contribution of both T6SS and colicins to the anti-bacterial killing activity of . We reveal that whilst the T6SS operon is present in there is evidence of functional degradation of the system through SNPs, indels and IS within key components of the system. We created strains with synthetically inducible T6SS operons but were still unable to demonstrate anti-bacterial activity of the T6SS. We demonstrate that the anti-bacterial activity observed in our assays was due to colicin activity. We show that no longer displayed anti-bacterial activity against bacteria that were resistant to colicins, and removal of the colicin plasmid from abrogated anti-bacterial activity of . We propose that the anti-bacterial activity demonstrated by colicins may be sufficient for niche competition by within the gastrointestinal environment.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): anti-bacterial activity , colicins , Interbacterial competition , polymicrobial , Shigella and T6SS
Funding
This study was supported by the:
  • Wellcome Trust (Award 220057/Z/19/Z)
    • Principle Award Recipient: PokyinBrian Leung
  • Global Challenges Research Fund
    • Principle Award Recipient: AbigailClements
  • Medical Research Council (Award MR/X00080X/1)
    • Principle Award Recipient: AbigailClements
© 2024 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.
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2024-02-20
2024-05-20
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References

  1. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 2013; 382:209–222 [View Article] [PubMed]
     [Google Scholar]
  2. Ashkenazi S, Levy I, Kazaronovski V, Samra Z. Growing antimicrobial resistance of Shigella isolates. J Antimicrob Chemother 2003; 51:427–429 [View Article] [PubMed]
     [Google Scholar]
  3. Baker KS, Dallman TJ, Field N, Childs T, Mitchell H et al. Genomic epidemiology of Shigella in the United Kingdom shows transmission of pathogen sublineages and determinants of antimicrobial resistance. Sci Rep 2018; 8:7389 [View Article] [PubMed]
     [Google Scholar]
  4. Bardsley M, Jenkins C, Mitchell HD, Mikhail AFW, Baker KS et al. Persistent transmission of shigellosis in England is associated with a recently emerged multidrug-resistant strain of Shigella sonnei. J Clin Microbiol 2020; 58:e01692–01619 [View Article] [PubMed]
     [Google Scholar]
  5. Chung The H, Bodhidatta L, Pham DT, Mason CJ, Ha Thanh T et al. Evolutionary histories and antimicrobial resistance in Shigella flexneri and Shigella sonnei in Southeast Asia. Commun Biol 2021; 4:353 [View Article] [PubMed]
     [Google Scholar]
  6. Salleh MZ, Nik Zuraina NMN, Hajissa K, Ilias MI, Banga Singh KK et al. Prevalence of multidrug-resistant and extended-spectrum beta-lactamase-producing Shigella Species in Asia: a systematic review and meta-analysis. Antibiotics 2022; 11:1653 [View Article] [PubMed]
     [Google Scholar]
  7. Tajbakhsh M, García Migura L, Rahbar M, Svendsen CA, Mohammadzadeh M et al. Antimicrobial-resistant Shigella infections from Iran: an overlooked problem?. J Antimicrob Chemother 2012; 67:1128–1133 [View Article] [PubMed]
     [Google Scholar]
  8. Thompson CN, Duy PT, Baker S. The rising dominance of Shigella sonnei: an intercontinental shift in the etiology of bacillary dysentery. PLoS Negl Trop Dis 2015; 9:e0003708 [View Article] [PubMed]
     [Google Scholar]
  9. Vinh H, Nhu NTK, Nga TVT, Duy PT, Campbell JI et al. A changing picture of shigellosis in southern Vietnam: shifting species dominance, antimicrobial susceptibility and clinical presentation. BMC Infect Dis 2009; 9:204 [View Article] [PubMed]
     [Google Scholar]
  10. DuPont HL, Levine MM, Hornick RB, Formal SB. Inoculum size in shigellosis and implications for expected mode of transmission. J Infect Dis 1989; 159:1126–1128 [View Article] [PubMed]
     [Google Scholar]
  11. Yang F, Yang J, Zhang X, Chen L, Jiang Y et al. Genome dynamics and diversity of Shigella species, the etiologic agents of bacillary dysentery. Nucleic Acids Res 2005; 33:6445–6458 [View Article] [PubMed]
     [Google Scholar]
  12. Hershberg R, Tang H, Petrov DA. Reduced selection leads to accelerated gene loss in Shigella. Genome Biol 2007; 8:R164 [View Article] [PubMed]
     [Google Scholar]
  13. Holt KE, Thieu Nga TV, Thanh DP, Vinh H, Kim DW et al. Tracking the establishment of local endemic populations of an emergent enteric pathogen. Proc Natl Acad Sci U S A 2013; 110:17522–17527 [View Article] [PubMed]
     [Google Scholar]
  14. Kotloff KL, Winickoff JP, Ivanoff B, Clemens JD, Swerdlow DL et al. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull World Health Organ 1999; 77:651–666 [PubMed]
     [Google Scholar]
  15. Lima IFN, Havt A, Lima AAM. Update on molecular epidemiology of Shigella infection. Curr Opin Gastroenterol 2015; 31:30–37 [View Article] [PubMed]
     [Google Scholar]
  16. Matanza XM, Clements A. Pathogenicity and virulence of Shigella sonnei: a highly drug-resistant pathogen of increasing prevalence. Virulence 2023; 14:2280838 [View Article] [PubMed]
     [Google Scholar]
  17. Anderson MC, Vonaesch P, Saffarian A, Marteyn BS, Sansonetti PJ. Shigella sonnei encodes a functional T6SS used for interbacterial competition and niche cccupancy. Cell Host Microbe 2017; 21:769–776 [View Article] [PubMed]
     [Google Scholar]
  18. Journet L, Cascales E. The type VI secretion system in Escherichia coli and related species. EcoSal Plus 2016; 7: [View Article] [PubMed]
     [Google Scholar]
  19. Bingle LE, Bailey CM, Pallen MJ. Type VI secretion: a beginner’s guide. Curr Opin Microbiol 2008; 11:3–8 [View Article] [PubMed]
     [Google Scholar]
  20. Salomon D, Gonzalez H, Updegraff BL, Orth K. Vibrio parahaemolyticus type VI secretion system 1 is activated in marine conditions to target bacteria, and is differentially regulated from system 2. PLoS One 2013; 8:e61086 [View Article] [PubMed]
     [Google Scholar]
  21. 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]
  22. Ma AT, Mekalanos JJ. In vivo actin cross-linking induced by Vibrio cholerae type. Proc Natl Acad Sci U S A 2010; 107:4365–4370 [View Article]
     [Google Scholar]
  23. 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]
  24. Si M, Zhao C, Burkinshaw B, Zhang B, Wei D et al. Manganese scavenging and oxidative stress response mediated by type VI secretion system in Burkholderia thailandensis. Proc Natl Acad Sci U S A 2017; 114:E2233–E2242 [View Article] [PubMed]
     [Google Scholar]
  25. Bernard CS, Brunet YR, Gueguen E, Cascales E. Nooks and crannies in type VI secretion regulation. J Bacteriol 2010; 192:3850–3860 [View Article] [PubMed]
     [Google Scholar]
  26. Bernard CS, Brunet YR, Gavioli M, Lloubès R, Cascales E. Regulation of type VI secretion gene clusters by sigma54 and cognate enhancer binding proteins. J Bacteriol 2011; 193:2158–2167 [View Article] [PubMed]
     [Google Scholar]
  27. Stolle A-S, Meader BT, Toska J, Mekalanos JJ. Endogenous membrane stress induces T6Ss activity in pseudo. Proc Natl Acad Sci U S A 2021; 118:e2018365118 [View Article]
     [Google Scholar]
  28. Monjarás Feria J, Valvano MA. An overview of anti-eukaryotic T6SS effectors. Front Cell Infect Microbiol 2020; 10:584751 [View Article] [PubMed]
     [Google Scholar]
  29. Hernandez RE, Gallegos-Monterrosa R, Coulthurst SJ. Type VI secretion system effector proteins: effective weapons for bacterial competitiveness. Cell Microbiol 2020; 22:e13241 [View Article] [PubMed]
     [Google Scholar]
  30. Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources?. BMC Genomics 2009; 10:104 [View Article] [PubMed]
     [Google Scholar]
  31. Jani AJ, Cotter PA. Type VI secretion: not just for pathogenesis anymore. Cell Host Microbe 2010; 8:2–6 [View Article] [PubMed]
     [Google Scholar]
  32. Allsopp LP, Bernal P, Nolan LM, Filloux A. Causalities of war: the connection between type VI secretion system and microbiota. Cell Microbiol 2020; 22:e13153 [View Article] [PubMed]
     [Google Scholar]
  33. De Silva PM, Bennett RJ, Kuhn L, Ngondo P, Debande L et al. Escherichia coli killing by epidemiologically successful sublineages of Shigella sonnei is mediated by colicins. EBioMedicine 2023; 97:104822 [View Article] [PubMed]
     [Google Scholar]
  34. 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]
  35. Smarda J, Obdrzálek V. Incidence of colicinogenic strains among human Escherichia coli. J Basic Microbiol 2001; 41:367–374 [View Article] [PubMed]
     [Google Scholar]
  36. Pukatzki S, McAuley SB, Miyata ST. The type VI secretion system: translocation of effectors and effector-domains. Curr Opin Microbiol 2009; 12:11–17 [View Article] [PubMed]
     [Google Scholar]
  37. Alam A, Golovliov I, Javed E, Sjöstedt A. ClpB mutants of Francisella tularensis subspecies holarctica and tularensis are defective for type VI secretion and intracellular replication. Sci Rep 2018; 8:11324 [View Article] [PubMed]
     [Google Scholar]
  38. Dong T, Kirchhof MG, Schellhorn HE. RpoS regulation of gene expression during exponential growth of Escherichia coli K12. Mol Genet Genomics 2008; 279:267–277 [View Article] [PubMed]
     [Google Scholar]
  39. Gomes AÉI, Stuchi LP, Siqueira NMG, Henrique JB, Vicentini R et al. Selection and validation of reference genes for gene expression studies in Klebsiella pneumoniae using reverse transcription quantitative real-time PCR. Sci Rep 2018; 8:9001 [View Article] [PubMed]
     [Google Scholar]
  40. Choi U, Lee C-R. Distinct roles of outer membrane porins in antibiotic resistance and membrane integrity in Escherichia coli. Front Microbiol 2019; 10:953 [View Article] [PubMed]
     [Google Scholar]
  41. Ho BT, Basler M, Mekalanos JJ. Type 6 secretion system-mediated immunity to type 4 secretion system-mediated gene transfer. Science 2013; 342:250–253 [View Article] [PubMed]
     [Google Scholar]
  42. Gueguen E, Cascales E. Promoter swapping unveils the role of the citrobacter rodentium CTS1 type VI secretion system in interbacterial competition. Appl Environ Microbiol 2013; 79:32–38 [View Article] [PubMed]
     [Google Scholar]
  43. Calcuttawala F, Hariharan C, Pazhani GP, Ghosh S, Ramamurthy T. Activity spectrum of colicins produced by Shigella sonnei and genetic mechanism of colicin resistance in conspecific S. sonnei strains and Escherichia coli. Antimicrob Agents Chemother 2015; 59:152–158 [View Article] [PubMed]
     [Google Scholar]
  44. Lauritsen I, Porse A, Sommer MOA, Nørholm MHH. A versatile one-step CRISPR-Cas9 based approach to plasmid-curing. Microb Cell Fact 2017; 16:135 [View Article] [PubMed]
     [Google Scholar]
  45. Gordon DM, O’Brien CL. Bacteriocin diversity and the frequency of multiple bacteriocin production in Escherichia coli. Microbiology 2006; 152:3239–3244 [View Article] [PubMed]
     [Google Scholar]
  46. Kleanthous C. Swimming against the tide: progress and challenges in our understanding of colicin translocation. Nat Rev Microbiol 2010; 8:843–848 [View Article] [PubMed]
     [Google Scholar]
  47. Schendel SL, Click EM, Webster RE, Cramer WA. The TolA protein interacts with colicin E1 differently than with other group A colicins. J Bacteriol 1997; 179:3683–3690 [View Article] [PubMed]
     [Google Scholar]
  48. Holt KE, Baker S, Weill F-X, Holmes EC, Kitchen A et al. Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe. Nat Genet 2012; 44:1056–1059 [View Article] [PubMed]
     [Google Scholar]
  49. Hawkey J, Paranagama K, Baker KS, Bengtsson RJ, Weill F-X et al. Global population structure and genotyping framework for genomic surveillance of the major dysentery pathogen, Shigella sonnei. Nat Commun 2021; 12:2684 [View Article] [PubMed]
     [Google Scholar]
  50. Gueguen E, Wills NM, Atkins JF, Cascales E. Transcriptional frameshifting rescues Citrobacter rodentium type VI secretion by the production of two length variants from the prematurely interrupted tssM gene. PLoS Genet 2014; 10:e1004869 [View Article] [PubMed]
     [Google Scholar]
  51. Mock M, Pugsley AP. The BtuB group col plasmids and homology between the colicins they encode. J Bacteriol 1982; 150:1069–1076 [View Article] [PubMed]
     [Google Scholar]
  52. Pugsley AP. Escherichia coli K12 strains for use in the identification and characterization of colicins. J Gen Microbiol 1985; 131:369–376 [View Article] [PubMed]
     [Google Scholar]
  53. Caboni M, Pédron T, Rossi O, Goulding D, Pickard D et al. An O antigen capsule modulates bacterial pathogenesis in Shigella sonnei. PLoS Pathog 2015; 11:e1004749 [View Article] [PubMed]
     [Google Scholar]
  54. The HC, Thanh DP, Holt KE, Thomson NR, Baker S. The genomic signatures of Shigella evolution, adaptation and geographical spread. Nat Rev Microbiol 2016; 14:235–250 [View Article] [PubMed]
     [Google Scholar]
  55. Herrero M, de Lorenzo V, Timmis KN. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 1990; 172:6557–6567 [View Article] [PubMed]
     [Google Scholar]
  56. Ruano-Gallego D, Sanchez-Garrido J, Kozik Z, Núñez-Berrueco E, Cepeda-Molero M et al. Type III secretion system effectors form robust and flexible intracellular virulence networks. Science 2021; 371:eabc9531 [View Article] [PubMed]
     [Google Scholar]
  57. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27:1009–1010 [View Article] [PubMed]
     [Google Scholar]
  58. Grant JR, Enns E, Marinier E, Mandal A, Herman EK et al. Proksee: in-depth characterization and visualization of bacterial genomes. Nucleic Acids Res 2023; 51:W484–W492 [View Article] [PubMed]
     [Google Scholar]
  59. Kopecko DJ, Washington O, Formal SB. Genetic and physical evidence for plasmid control of Shigella sonnei form I cell surface antigen. Infect Immun 1980; 29:207–214 [View Article]
     [Google Scholar]
  60. O’Brien AO, Lively TA, Chen ME, Rothman SW, Formal SB. Escherichia coli O157:H7 strains associated with haemorrhagic colitis in the United States produce a Shigella dysenteriae 1 (SHIGA) like cytotoxin. Lancet 1983; 1:702 [View Article]
     [Google Scholar]
  61. Levine MM, Bergquist EJ, Nalin DR, Waterman DH, Hornick RB et al. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1978; 1:1119–1122 [View Article]
     [Google Scholar]
  62. Figurski DH, Helinski DR. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A 1979; 76:1648–1652 [View Article] [PubMed]
     [Google Scholar]
  63. Aswad D, Koshland DE Jr. Isolation, characterization and complementation of Salmonella typhimurium chemotaxis mutants. J Mol Biol 1975; 97:225–235 [View Article]
     [Google Scholar]
  64. Chen Y, Brook TC, Alcon-Giner C, Clarke P, Hall LJ et al. Draft genome sequences of citrobacter freundii and citrobacter murliniae strains isolated from the feces of preterm infants. Microbiol Resour Announc 2019; 8:33 [View Article] [PubMed]
     [Google Scholar]
  65. Ruano-Gallego D, Álvarez B, Fernández LÁ. Engineering the controlled assembly of filamentous injectisomes in E. coli K-12 for protein translocation into mammalian cells. ACS Synth Biol 2015; 4:1030–1041 [View Article] [PubMed]
     [Google Scholar]
  66. Clements A, Stoneham CA, Furniss RCD, Frankel G. Enterohaemorrhagic Escherichia coli inhibits recycling endosome function and trafficking of surface receptors. Cell Microbiol 2014; 16:1693–1705 [View Article] [PubMed]
     [Google Scholar]
  67. Mavridou DAI, Gonzalez D, Clements A, Foster KR. The pUltra plasmid series: a robust and flexible tool for fluorescent labeling of Enterobacteria. Plasmid 2016; 87–88:65–71 [View Article] [PubMed]
     [Google Scholar]
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Shigella sonnei utilises colicins during inter-bacterial competition
Microbiology 170, 001434 (2024); https://doi.org/10.1099/mic.0.001434
/content/journal/micro/10.1099/mic.0.001434
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