Skip to content
1887

Microbial Genomics logo Microbial Genomics

Volume 9, Issue 11

Parallel loss of type VI secretion systems in two multi-drug-resistant lineages Open Access

Abstract

The repeated emergence of multi-drug-resistant (MDR) clones is a threat to public health globally. In recent work, drug-resistant were shown to be capable of displacing commensal in the human gut. Given the rapid colonization observed in travel studies, it is possible that the presence of a type VI secretion system (T6SS) may be responsible for the rapid competitive advantage of drug-resistant clones. We employed large-scale genomic approaches to investigate this hypothesis. First, we searched for T6SS genes across a curated dataset of over 20 000 genomes representing the full phylogenetic diversity of . This revealed large, non-phylogenetic variation in the presence of T6SS genes. No association was found between T6SS gene carriage and MDR lineages. However, multiple clades containing MDR clones have lost essential structural T6SS genes. We characterized the T6SS loci of ST410 and ST131 and identified specific recombination and insertion events responsible for the parallel loss of essential T6SS genes in two MDR clones.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Escherichia coli , multi-drug resistance , ST131 , ST410 and type VI secretion system
© 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.0.001133
2023-11-16
2025-06-12
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/11/mgen001133.html?itemId=/content/journal/mgen/10.1099/mgen.0.001133&mimeType=html&fmt=ahah

References

  1. Cummins EA, Hall RJ, Connor C, McInerney JO, McNally A. Distinct evolutionary trajectories in the Escherichia coli pangenome occur within sequence types. Microb Genom 2022; 8:11 [View Article] [PubMed]
     [Google Scholar]
  2. Murray CJL, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. The Lancet 2022; 399:629–655 [View Article]
     [Google Scholar]
  3. Connor CH, Zucoloto AZ, Yu I-L, Corander J, McDonald B et al. Multi-drug resistant E. coli displace commensal E. coli from the intestinal tract, a trait associated with elevated levels of genetic diversity in carbohydrate metabolism genes. bioRxiv 2022 [View Article] [PubMed]
     [Google Scholar]
  4. Arcilla MS, van Hattem JM, Haverkate MR, Bootsma MCJ, van Genderen PJJ et al. Import and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae by international travellers (COMBAT study): a prospective, multicentre cohort study. Lancet Infect Dis 2017; 17:78–85 [View Article] [PubMed]
     [Google Scholar]
  5. Bevan ER, McNally A, Thomas CM, Piddock LJV, Hawkey PM. Acquisition and loss of CTX-M-producing and non-producing Escherichia coli in the fecal microbiome of travelers to South Asia. mBio 2018; 9:e02408-18 [View Article] [PubMed]
     [Google Scholar]
  6. Kantele A, Kuenzli E, Dunn SJ, Dance DAB, Newton PN et al. Dynamics of intestinal multidrug-resistant bacteria colonisation contracted by visitors to a high-endemic setting: a prospective, daily, real-time sampling study. Lancet Microbe 2021; 2:e151–e158 [View Article] [PubMed]
     [Google Scholar]
  7. Kallonen T, Brodrick HJ, Harris SR, Corander J, Brown NM et al. Systematic longitudinal survey of invasive Escherichia coli in England demonstrates a stable population structure only transiently disturbed by the emergence of ST131. Genome Res 2017; 27:1437–1449 [View Article] [PubMed]
     [Google Scholar]
  8. Gladstone RA, McNally A, Pöntinen AK, Tonkin-Hill G, Lees JA et al. Emergence and dissemination of antimicrobial resistance in Escherichia coli causing bloodstream infections in Norway in 2002-17: a nationwide, longitudinal, microbial population genomic study. Lancet Microbe 2021; 2:e331–e341 [View Article] [PubMed]
     [Google Scholar]
  9. Davies M, Galazzo G, van Hattem JM, Arcilla MS, Melles DC et al. Enterobacteriaceae and Bacteroidaceae provide resistance to travel-associated intestinal colonization by multi-drug resistant Escherichia coli. Gut Microbes 2022; 14:
     [Google Scholar]
  10. Mariano G, Trunk K, Williams DJ, Monlezun L, Strahl H et al. A family of type VI secretion system effector proteins that form ion-selective pores. Nat Commun 2019; 10:5484 [View Article] [PubMed]
     [Google Scholar]
  11. 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 U S A 2007; 104:15508–15513 [View Article] [PubMed]
     [Google Scholar]
  12. Salomon D, Klimko JA, Trudgian DC, Kinch LN, Grishin NV et al. Type VI secretion system toxins horizontally shared between marine bacteria. PLoS Pathog 2015; 11:e1005128 [View Article] [PubMed]
     [Google Scholar]
  13. Bernal P, Allsopp LP, Filloux A, Llamas MA. The Pseudomonas putida T6SS is a plant warden against phytopathogens. ISME J 2017; 11:972–987 [View Article] [PubMed]
     [Google Scholar]
  14. Troselj V, Treuner-Lange A, Søgaard-Andersen L, Wall D. Physiological heterogeneity triggers sibling conflict mediated by the type VI secretion system in an aggregative multicellular bacterium. mBio 2018; 9:e01645-17 [View Article] [PubMed]
     [Google Scholar]
  15. Tang L, Yue S, Li G-Y, Li J, Wang X-R et al. Expression, secretion and bactericidal activity of type VI secretion system in Vibrio anguillarum. Arch Microbiol 2016; 198:751–760 [View Article] [PubMed]
     [Google Scholar]
  16. Unni R, Pintor KL, Diepold A, Unterweger D. Presence and absence of type VI secretion systems in bacteria. Microbiology 2022; 168: [View Article] [PubMed]
     [Google Scholar]
  17. Kempnich MW, Sison-Mangus MP. Presence and abundance of bacteria with the Type VI secretion system in a coastal environment and in the global oceans. PLoS One 2020; 15:e0244217 [View Article] [PubMed]
     [Google Scholar]
  18. García-Bayona L, Coyne MJ, Comstock LE. Mobile Type VI secretion system loci of the gut bacteroidales display extensive intra-ecosystem transfer, multi-species spread and geographical clustering. PLoS Genet 2021; 17:e1009541 [View Article] [PubMed]
     [Google Scholar]
  19. Abby SS, Cury J, Guglielmini J, Néron B, Touchon M et al. Identification of protein secretion systems in bacterial genomes. Sci Rep 2016; 6:23080 [View Article] [PubMed]
     [Google Scholar]
  20. 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]
  21. Journet L, Cascales E. The Type VI secretion system in Escherichia coli and related species. EcoSal Plus 2016; 7: [View Article] [PubMed]
     [Google Scholar]
  22. Ma J, Bao Y, Sun M, Dong W, Pan Z et al. Two functional type VI secretion systems in avian pathogenic Escherichia coli are involved in different pathogenic pathways. Infect Immun 2014; 82:3867–3879 [View Article] [PubMed]
     [Google Scholar]
  23. de Pace F, Nakazato G, Pacheco A, de Paiva JB, Sperandio V et al. The type VI secretion system plays a role in type 1 fimbria expression and pathogenesis of an avian pathogenic Escherichia coli strain. Infect Immun 2010; 78:4990–4998 [View Article] [PubMed]
     [Google Scholar]
  24. Brunet YR, Espinosa L, Harchouni S, Mignot T, Cascales E. Imaging type VI secretion-mediated bacterial killing. Cell Rep 2013; 3:36–41 [View Article] [PubMed]
     [Google Scholar]
  25. Weber BS, Ly PM, Irwin JN, Pukatzki S, Feldman MF. A multidrug resistance plasmid contains the molecular switch for type VI secretion in Acinetobacter baumannii. Proc Natl Acad Sci U S A 2015; 112:9442–9447 [View Article] [PubMed]
     [Google Scholar]
  26. Di Venanzio G, Moon KH, Weber BS, Lopez J, Ly PM et al. Multidrug-resistant plasmids repress chromosomally encoded T6SS to enable their dissemination. Proc Natl Acad Sci U S A 2019; 116:1378–1383 [View Article] [PubMed]
     [Google Scholar]
  27. Zhou Z, Alikhan NF, Mohamed K, Fan Y, Achtman M. The Enterobase user’s guide, with case studies on salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity. Genome Res 2020; 30:138–152 [View Article]
     [Google Scholar]
  28. 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]
  29. 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]
     [Google Scholar]
  30. 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]
     [Google Scholar]
  31. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 2006; 34:D32–6 [View Article] [PubMed]
     [Google Scholar]
  32. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article] [PubMed]
     [Google Scholar]
  33. Colpan A, Johnston B, Porter S, Clabots C, Anway R et al. Escherichia coli sequence type 131 (ST131) subclone H30 as an emergent multidrug-resistant pathogen among US veterans. Clin Infect Dis 2013; 57:1256–1265 [View Article] [PubMed]
     [Google Scholar]
  34. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
     [Google Scholar]
  35. Roer L, Overballe-Petersen S, Hansen F, Schønning K, Wang M et al. Escherichia coli sequence type 410 is causing new international high-risk clones. mSphere 2018; 3:00337–18 [View Article] [PubMed]
     [Google Scholar]
  36. Petty NK, Ben Zakour NL, Stanton-Cook M, Skippington E, Totsika M et al. Global dissemination of a multidrug resistant Escherichia coli clone. Proc Natl Acad Sci U S A 2014; 111:5694–5699 [View Article] [PubMed]
     [Google Scholar]
  37. Ma J, Sun M, Pan Z, Lu C, Yao H. Diverse toxic effectors are harbored by vgrG islands for interbacterial antagonism in type VI secretion system. Biochim Biophys Acta Gen Subj 2018; 1862:1635–1643 [View Article] [PubMed]
     [Google Scholar]
  38. Ma J, Sun M, Dong W, Pan Z, Lu C et al. PAAR-Rhs proteins harbor various C-terminal toxins to diversify the antibacterial pathways of type VI secretion systems. Environ Microbiol 2017; 19:345–360 [View Article] [PubMed]
     [Google Scholar]
  39. Kostiuk B, Santoriello FJ, Diaz-Satizabal L, Bisaro F, Lee K-J et al. Type VI secretion system mutations reduced competitive fitness of classical Vibrio cholerae biotype. Nat Commun 2021; 12:6457 [View Article] [PubMed]
     [Google Scholar]
  40. Salomon D, Kinch LN, Trudgian DC, Guo X, Klimko JA et al. Marker for type VI secretion system effectors. Proc Natl Acad Sci U S A 2014; 111:9271–9276 [View Article] [PubMed]
     [Google Scholar]
  41. Forde BM, Ben Zakour NL, Stanton-Cook M, Phan M-D, Totsika M et al. The complete genome sequence of Escherichia coli EC958: A high quality reference sequence for the globally disseminated multidrug resistant E. coli O25b:H4-ST131 clone. PLoS One 2014; 9:e104400 [View Article] [PubMed]
     [Google Scholar]
  42. Ma LS, Narberhaus F, Lai EM. IcmF family protein TssM exhibits ATPase activity and energizes type VI secretion. J Biol Chem 2012; 287:15610–15621 [View Article] [PubMed]
     [Google Scholar]
  43. Zhang L, Xu J, Xu J, Chen K, He L et al. TssM is essential for virulence and required for type VI secretion in Ralstonia solanacearum. J Plant Dis Prot 2012; 119:125–134 [View Article]
     [Google Scholar]
  44. Lipworth S, Vihta K-D, Chau K, Barker L, George S et al. Ten-year longitudinal molecular epidemiology study of Escherichia coli and Klebsiella species bloodstream infections in Oxfordshire, UK. Genome Med 2021; 13:144 [View Article] [PubMed]
     [Google Scholar]
  45. Feng Y, Liu L, Lin J, Ma K, Long H et al. Key evolutionary events in the emergence of a globally disseminated, carbapenem resistant clone in the Escherichia coli ST410 lineage. Commun Biol 2019; 2:322 [View Article] [PubMed]
     [Google Scholar]
  46. Stoesser N, Sheppard AE, Pankhurst L, De Maio N, Moore CE et al. Evolutionary history of the global emergence of the Escherichia coli epidemic clone ST131. mBio 2016; 7:e02162 [View Article] [PubMed]
     [Google Scholar]
  47. Cummins EA, Snaith AE, McNally A, Hall RJ. The role of potentiating mutations in the evolution of pandemic Escherichia coli clones. Eur J Clin Microbiol Infect Dis 2021 [View Article]
     [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001133
Loading
Parallel loss of type VI secretion systems in two multi-drug-resistant Escherichia coli lineages
M Gen 9, 001133 (2023); https://doi.org/10.1099/mgen.0.001133
/content/journal/mgen/10.1099/mgen.0.001133
/content/journal/mgen/10.1099/mgen.0.001133
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

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