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Volume 8, Issue 10

investigation of the genus type VI secretion system reveals genetic diversity in organization and putative effectors Open Access

This article is part of the 'Genomics, Epidemiology and Evolution of Campylobacter, Helicobacter and Related Organisms' collection.

Abstract

Bacterial type VI secretion systems (T6SSs) are contractile nanomachines that deliver proteinic substrates into target prokaryotic or eukaryotic cells and the surrounding milieu. The genus encompasses 39 recognized species and 13 subspecies, with many belonging to a group known as ‘emerging pathogens’. Within , seven species have been identified to harbour a complete T6SS cluster but have yet to be comparatively assessed. In this study, using systematic bioinformatics approaches and the T6SS-positive 488 strain as a reference, we explored the genus-wide prevalence, similarity and make-up of the T6SS amongst 372 publicly available ‘complete’ genomes. Our analyses predict that approximately one-third of species possess a T6SS. We also putatively report the first identification of a T6SS in four species: and . The T6SSs cluster into three distinct organizations (I–III), of which two break down into further variants. Thirty T6SS-containing genomes were found to harbour more than one gene, with strain NCTC 11845 possessing five. Analysis of the Pathogenicity Island-1 confirmed its conservation amongst T6SS-positive strains, as well as highlighting its diverse genetic composition, including additional putative effector–immunity pairs (e.g. PoNe and DUF1911 domains). Effector–immunity pairs were also observed neighbouring s in several other species, in addition to putative genes encoding nucleases, lysozymes, ATPases and a ferric ATP-binding cassette uptake system. These observations highlight the diverse genetic make-up of the T6SS within and provide further evidence of its role in pathogenesis.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Campylobacter , effectors , pathogenicity island , T6SS organization and type VI secretion system (T6SS)
© 2022 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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2022-10-31
2024-04-29
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References

  1. Robinson L, Liaw J, Omole Z, Xia D, van Vliet AHM et al. Bioinformatic analysis of the Campylobacter jejuni type VI secretion system and effector prediction. Front Microbiol 2021; 12:694824 [View Article]
     [Google Scholar]
  2. Costa TRD, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A et al. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 2015; 13:343–359 [View Article] [PubMed]
     [Google Scholar]
  3. Gorasia DG, Veith PD, Reynolds EC. The type IX secretion system: advances in structure, function and organisation. Microorganisms 2020; 8:1173 [View Article]
     [Google Scholar]
  4. Palmer T, Finney AJ, Saha CK, Atkinson GC, Sargent F. A holin/peptidoglycan hydrolase-dependent protein secretion system. Mol Microbiol 2021; 115:345–355 [View Article]
     [Google Scholar]
  5. Coulthurst S. The type VI secretion system: a versatile bacterial weapon. Microbiology 2019; 165:503–515 [View Article]
     [Google Scholar]
  6. Lin H-H, Filloux A, Lai E-M. Role of recipient susceptibility factors during contact-dependent interbacterial competition. Front Microbiol 2020; 11:603652 [View Article]
     [Google Scholar]
  7. Matthey N, Stutzmann S, Stoudmann C, Guex N, Iseli C et al. Neighbor predation linked to natural competence fosters the transfer of large genomic regions in vibrio cholerae. Elife 2019; 8: [View Article]
     [Google Scholar]
  8. Chen C, Yang X, Shen X. Confirmed and potential roles of bacterial T6SSs in the intestinal ecosystem. Front Microbiol 2019; 10:1484 [View Article]
     [Google Scholar]
  9. Hood RD, Singh P, Hsu F, Güvener T, Carl MA et al. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 2010; 7:25–37 [View Article]
     [Google Scholar]
  10. Ma LS, Hachani A, Lin JS, Filloux A, Lai EM. Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe 2014; 16:94–104 [View Article] [PubMed]
     [Google Scholar]
  11. 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]
  12. Hachani A, Wood TE, Filloux A. Type VI secretion and anti-host effectors. Curr Opin Microbiol 2016; 29:81–93 [View Article] [PubMed]
     [Google Scholar]
  13. Wang J, Brodmann M, Basler M. Assembly and subcellular localization of bacterial type VI secretion systems. Annu Rev Microbiol 2019; 73:621–638 [View Article]
     [Google Scholar]
  14. 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]
  15. Coyne MJ, Roelofs KG, Comstock LE. Type VI secretion systems of human gut Bacteroidales segregate into three genetic architectures, two of which are contained on mobile genetic elements. BMC Genomics 2016; 17:1–21 [View Article] [PubMed]
     [Google Scholar]
  16. Ho BT, Dong TG, Mekalanos JJ. A view to A kill: the bacterial type VI secretion system. Cell Host Microbe 2014; 15:9–21 [View Article]
     [Google Scholar]
  17. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM et al. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci 2009; 106:4154–4159 [View Article]
     [Google Scholar]
  18. Zoued A, Brunet YR, Durand E, Aschtgen MS, Logger L et al. Architecture and assembly of the type VI secretion system. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 2014; 1843:1664–1673 [View Article]
     [Google Scholar]
  19. 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 2007; 104:15508–15513 [View Article]
     [Google Scholar]
  20. 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]
  21. Kapitein N, Bönemann G, Pietrosiuk A, Seyffer F, Hausser I et al. ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion. Mol Microbiol 2013; 87:1013–1028 [View Article]
     [Google Scholar]
  22. Bleumink-Pluym NMC, van Alphen LB, Bouwman LI, Wösten M, van Putten JPM. Identification of a functional type VI secretion system in Campylobacter jejuni conferring capsule polysaccharide sensitive cytotoxicity. PLoS Pathog 2013; 9:e1003393 [View Article]
     [Google Scholar]
  23. Liaw J, Hong G, Davies C, Elmi A, Sima F et al. The Campylobacter jejuni type VI secretion system enhances the oxidative stress response and host colonization. Front Microbiol 2019; 10:2864 [View Article]
     [Google Scholar]
  24. Hachani A, Allsopp LP, Oduko Y, Filloux A. The VgrG proteins are “à la carte” delivery systems for bacterial type VI effectors. J Biol Chem 2014; 289:17872–17884 [View Article] [PubMed]
     [Google Scholar]
  25. 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]
  26. 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 2018; 115:12519–12524 [View Article]
     [Google Scholar]
  27. Koskiniemi S, Lamoureux JG, Nikolakakis KC, t’Kint de Roodenbeke C, Kaplan MD et al. Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci 2013; 110:7032–7037 [View Article]
     [Google Scholar]
  28. Durand E, Cambillau C, Cascales E, Journet L. VgrG, Tae, Tle, and beyond: the versatile arsenal of Type VI secretion effectors. Trends Microbiol 2014; 22:498–507 [View Article] [PubMed]
     [Google Scholar]
  29. Costa D, Iraola G. Pathogenomics of emerging Campylobacter species. Clin Microbiol Rev 2019; 32: [View Article]
     [Google Scholar]
  30. Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM. Global epidemiology of campylobacter infection. Clin Microbiol Rev 2015; 28:687–720 [View Article]
     [Google Scholar]
  31. Bacterio.net List of Prokariotic Names with Standing in Nomenclature (LPSN). n.d https://www.bacterio.net/genus/campylobacter, https://www.bacterio.net/genus/campylobacter
  32. 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]
  33. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control (ECDC) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2014. EFS2 2015; 13: [View Article]
     [Google Scholar]
  34. Man SM. The clinical importance of emerging Campylobacter species. Nat Rev Gastroenterol Hepatol 2011; 8:669–685 [View Article]
     [Google Scholar]
  35. Kaakoush NO, Mitchell HM, Man SM. Role of emerging Campylobacter species in inflammatory bowel diseases. Inflamm Bowel Dis 2014; 20:2189–2197 [View Article] [PubMed]
     [Google Scholar]
  36. Genome list - genome - NCBI. n.d https://www.ncbi.nlm.nih.gov/genome/browse#!/overview/ accessed 1 October 2020
  37. Corcionivoschi N, Gundogdu O, Moran L, Kelly C, Scates P et al. Virulence characteristics of hcp (+) Campylobacter jejuni and Campylobacter coli isolates from retail chicken. Gut Pathog 2015; 7:1–11 [View Article] [PubMed]
     [Google Scholar]
  38. Ghatak S, He Y, Reed S, Strobaugh T, Irwin P. Whole genome sequencing and analysis of Campylobacter coli YH502 from retail chicken reveals a plasmid-borne type VI secretion system. Genom Data 2017; 11:128–131 [View Article] [PubMed]
     [Google Scholar]
  39. Liu F, Chen S, Luu LDW, Lee SA, Tay ACY et al. Analysis of complete Campylobacter concisus genomes identifies genomospecies features, secretion systems and novel plasmids and their association with severe ulcerative colitis. Microb Genom 2020; 6:1–13 [View Article] [PubMed]
     [Google Scholar]
  40. Bullman S, Lucid A, Corcoran D, Sleator RD, Lucey B. Genomic investigation into strain heterogeneity and pathogenic potential of the emerging gastrointestinal pathogen Campylobacter ureolyticus. PLOS ONE 2013; 8:e71515 [View Article]
     [Google Scholar]
  41. Miller WG, Yee E, Chapman MH, Smith TPL, Bono JL et al. Comparative genomics of the Campylobacter lari group. Genome Biol Evol 2014; 6:3252–3266 [View Article] [PubMed]
     [Google Scholar]
  42. Gemmell MR, Berry S, Mukhopadhya I, Hansen R, Nielsen HL et al. Comparative genomics of Campylobacter concisus: analysis of clinical strains reveals genome diversity and pathogenic potential. Emerg Microbes Infect 2018; 7:116 [View Article]
     [Google Scholar]
  43. Lertpiriyapong K, Gamazon ER, Feng Y, Park DS, Pang J et al. Campylobacter jejuni type VI secretion system roles in adaptation to deoxycholic acid, host cell adherence, invasion, and in vivo colonization. PLoS ONE 2012; 7:e42842
     [Google Scholar]
  44. Marasini D, Karki AB, Bryant JM, Sheaff RJ, Fakhr MK. Molecular characterization of megaplasmids encoding the type VI secretion system in Campylobacter jejuni isolated from chicken livers and gizzards. Sci Rep 2020; 10:12514 [View Article] [PubMed]
     [Google Scholar]
  45. Home - BioSample - NCBI. n.d https://www.ncbi.nlm.nih.gov/biosample accessed 1 October 2020
  46. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
     [Google Scholar]
  47. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:1–9 [View Article] [PubMed]
     [Google Scholar]
  48. Fridman CM, Keppel K, Gerlic M, Bosis E, Salomon D. A comparative genomics methodology reveals A widespread family of membrane-disrupting T6SS effectors. Nat Commun 2020; 11:1–14 [View Article]
     [Google Scholar]
  49. Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA. Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 2012; 28:464–469 [View Article] [PubMed]
     [Google Scholar]
  50. Gilchrist CLM, Chooi Y-H. Clinker & clustermap.js: automatic generation of gene cluster comparison figures. Bioinformatics 2021; 37:2473–2475 [View Article]
     [Google Scholar]
  51. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 2017; 45:D200–D203 [View Article]
     [Google Scholar]
  52. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article]
     [Google Scholar]
  53. Miller WG, Yee E, Jolley KA, Chapman MH. Use of an improved atpA amplification and sequencing method to identify members of the Campylobacteraceae and Helicobacteraceae. Lett Appl Microbiol 2014; 58:582–590 [View Article] [PubMed]
     [Google Scholar]
  54. Antezack A, Boxberger M, Rolland C, Ben Khedher M, Monnet-Corti V et al. Isolation and characterization of Campylobacter massiliensis sp. nov., a novel Campylobacter species detected in a gingivitis subject. Int J Syst Evol Microbiol 2021; 71:005039 [View Article] [PubMed]
     [Google Scholar]
  55. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
     [Google Scholar]
  56. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLOS ONE 2010; 5:e9490 [View Article]
     [Google Scholar]
  57. 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]
     [Google Scholar]
  58. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article]
     [Google Scholar]
  59. Carver TJ, Rutherford KM, Berriman M, Rajandream M-A, Barrell BG et al. ACT: the Artemis Comparison Tool. Bioinformatics 2005; 21:3422–3423 [View Article] [PubMed]
     [Google Scholar]
  60. De Maayer P, Venter SN, Kamber T, Duffy B, Coutinho TA et al. Comparative genomics of the type VI secretion systems of Pantoea and Erwinia species reveals the presence of putative effector islands that may be translocated by the VgrG and Hcp proteins. BMC Genomics 2011; 12:1–15 [View Article]
     [Google Scholar]
  61. Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 2019; 37:420–423 [View Article] [PubMed]
     [Google Scholar]
  62. Sonnhammer EL, von Heijne G, Krogh A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 1998; 6:175–182
     [Google Scholar]
  63. El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A et al. Pfam protein families database in 2019 | nucleic acids research | oxford academic. Nucleic Acids Research 2019; 47:427–432
     [Google Scholar]
  64. Madeira F, Park YM, Lee J, Buso N, Gur T et al. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res 2019; 47:W636–W641 [View Article]
     [Google Scholar]
  65. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004; 14:1188–1190 [View Article]
     [Google Scholar]
  66. Noreen Z, Jobichen C, Abbasi R, Seetharaman J, Sivaraman J et al. Structural basis for the pathogenesis of Campylobacter jejuni Hcp1, a structural and effector protein of the type VI Secretion System. FEBS J 2018; 285:4060–4070 [View Article]
     [Google Scholar]
  67. Jana B, Fridman CM, Bosis E, Salomon D. A modular effector with a DNase domain and a marker for T6SS substrates. Nat Commun 2019; 10:1–12 [View Article]
     [Google Scholar]
  68. Zhang D, de Souza RF, Anantharaman V, Iyer LM, Aravind L. Polymorphic toxin systems: comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol Direct 2012; 7:1–76 [View Article]
     [Google Scholar]
  69. Russell AB, Peterson SB, Mougous JD. Type VI secretion system effectors: poisons with a purpose. Nat Rev Microbiol 2014; 12:137–148 [View Article] [PubMed]
     [Google Scholar]
  70. Bryant E, Shen Z, Mannion A, Patterson M, Buczek J et al. Campylobacter taeniopygiae sp. nov., campylobacter aviculae sp. nov., and campylobacter estrildidarum sp. nov., novel species isolated from laboratory-maintained zebra finches. Avian Dis 2020; 64:457–466 [View Article]
     [Google Scholar]
  71. Silva MF, Pereira G, Carneiro C, Hemphill A, Mateus L. Campylobacter portucalensis sp. nov., a new species of Campylobacter isolated from the preputial mucosa of bulls. PLOS ONE 2020; 15:e0227500 [View Article]
     [Google Scholar]
  72. Bloomfield S, Wilkinson D, Rogers L, Biggs P, French N et al. Campylobacter novaezeelandiae sp. nov., isolated from birds and water in New Zealand. Int J Syst Evol Microbiol 2020; 70:3775–3784 [View Article] [PubMed]
     [Google Scholar]
  73. Antezack A, Boxberger M, Rolland C, Ben Khedher M, Monnet-Corti V et al. Isolation and characterization of Campylobacter massiliensis sp. nov., a novel Campylobacter species detected in a gingivitis subject. Int J Syst Evol Microbiol 2021; 71:005039 [View Article] [PubMed]
     [Google Scholar]
  74. Parisi A, Chiara M, Caffara M, Mion D, Miller WG et al. Campylobacter vulpis sp. nov. isolated from wild red foxes. Syst Appl Microbiol 2021; 44:126204 [View Article]
     [Google Scholar]
  75. Harrison JW, Dung TTN, Siddiqui F, Korbrisate S, Bukhari H et al. Identification of possible virulence marker from Campylobacter jejuni isolates. Emerg Infect Dis 2014; 20:1026–1029 [View Article]
     [Google Scholar]
  76. Ugarte-Ruiz M, Stabler RA, Domínguez L, Porrero MC, Wren BW et al. Prevalence of type VI secretion system in Spanish Campylobacter jejuni isolates. Zoonoses Public Health 2015; 62:497–500 [View Article]
     [Google Scholar]
  77. Repizo GD, Espariz M, Seravalle JL, Salcedo SP. Bioinformatic analysis of the type VI secretion system and its potential toxins in the acinetobacter genus. Front Microbiol 2019; 10:2519 [View Article]
     [Google Scholar]
  78. 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]
     [Google Scholar]
  79. Coyne MJ, Zitomersky NL, McGuire AM, Earl AM, Comstock LE. Evidence of extensive DNA transfer between bacteroidales species within the human gut. mBio 2014; 5:e01305-14 [View Article]
     [Google Scholar]
  80. 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]
     [Google Scholar]
  81. Mougous JD, Gifford CA, Ramsdell TL, Mekalanos JJ. Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat Cell Biol 2007; 9:797–803 [View Article] [PubMed]
     [Google Scholar]
  82. Blondel CJ, Jiménez JC, Contreras I, Santiviago CA. Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 2009; 10:1–17 [View Article]
     [Google Scholar]
  83. 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]
     [Google Scholar]
  84. Mougous JD, Gifford CA, Ramsdell TL, Mekalanos JJ. Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat Cell Biol 2007; 9:797–803 [View Article] [PubMed]
     [Google Scholar]
  85. Hacker J, Kaper JB. Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 2000; 54:641–679 [View Article] [PubMed]
     [Google Scholar]
  86. Fraikin N, Goormaghtigh F, Van Melderen L. Type II toxin-antitoxin systems: evolution and revolutions. J Bacteriol 2020; 202:e00763-19 [View Article]
     [Google Scholar]
  87. Shea CM, McIntosh MA. Nucleotide sequence and genetic organization of the ferric enterobactin transport system: homology to other periplasmic binding protein-dependent systems in Escherichia coli. Mol Microbiol 1991; 5:1415–1428 [View Article] [PubMed]
     [Google Scholar]
  88. Schalk IJ, Guillon L. Fate of ferrisiderophores after import across bacterial outer membranes: different iron release strategies are observed in the cytoplasm or periplasm depending on the siderophore pathways. Amino Acids 2013; 44:1267–1277 [View Article] [PubMed]
     [Google Scholar]
  89. 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; 8:1–12 [View Article]
     [Google Scholar]
  90. 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 2017; 114:E2233–E2242 [View Article]
     [Google Scholar]
  91. Andrews SC, Robinson AK, Rodríguez-Quiñones F. Bacterial iron homeostasis. FEMS Microbiol Rev 2003; 27:215–237 [View Article] [PubMed]
     [Google Scholar]
  92. Wandersman C, Delepelaire P. Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 2004; 58:611–647 [View Article]
     [Google Scholar]
  93. Delepelaire P. Bacterial ABC transporters of iron containing compounds. Res Microbiol 2019; 170:345–357 [View Article] [PubMed]
     [Google Scholar]
  94. Palyada K, Threadgill D, Stintzi A. Iron acquisition and regulation in Campylobacter jejuni. J Bacteriol 2004; 186:4714–4729 [View Article] [PubMed]
     [Google Scholar]
  95. Rigard M, Bröms JE, Mosnier A, Hologne M, Martin A et al. Francisella tularensis IglG belongs to a novel family of PAAR-like T6SS proteins and harbors a unique N-terminal extension required for virulence. PLOS Pathog 2016; 12:e1005821 [View Article]
     [Google Scholar]
  96. Bruck I, O’Donnell M. The DNA replication machine of a gram-positive organism. J Biol Chem 2000; 275:28971–28983 [View Article] [PubMed]
     [Google Scholar]
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In silico investigation of the genus Campylobacter type VI secretion system reveals genetic diversity in organization and putative effectors
M Gen 8, 000898 (2022); https://doi.org/10.1099/mgen.0.000898
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