1887

Abstract

Commensal non-pathogenic spp. live within the human host alongside the pathogenic and and due to natural competence, horizontal gene transfer within the genus is possible and has been observed. Four distinct spp. isolates taken from the throats of two human volunteers have been assessed here using a combination of microbiological and bioinformatics techniques. Three of the isolates have been identified as biovar and one as . Specific gene clusters have been identified within these commensal isolate genome sequences that are believed to encode a Type VI Secretion System, a newly identified CRISPR system, a Type IV Secretion System unlike that in other spp., a hemin transporter, and a haem acquisition and utilization system. This investigation is the first to investigate these systems in either the non-pathogenic or pathogenic spp. In addition, the biovar possess previously unreported capsule loci and sequences have been identified in all four isolates that are similar to genes seen within the pathogens that are associated with virulence. These data from the four commensal isolates provide further evidence for a spp. gene pool and highlight the presence of systems within the commensals with functions still to be explored.

Funding
This study was supported by the:
  • Lori AS Snyder , Swan Alliance
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000423
2020-08-26
2020-10-22
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/9/mgen000423.html?itemId=/content/journal/mgen/10.1099/mgen.0.000423&mimeType=html&fmt=ahah

References

  1. Gao Z, Kang Y, Yu J, Ren L. Human pharyngeal microbiome may play a protective role in respiratory tract infections. Genomics Proteomics Bioinformatics 2014; 12:144–150
    [Google Scholar]
  2. Verma D, Garg PK, Dubey AK. Insights into the human oral microbiome. Arch Microbiol 2018; 200:525–540
    [Google Scholar]
  3. Liu G, Tang CM, Exley RM. Non-pathogenic Neisseria: members of an abundant, multi-habitat, diverse genus. Microbiology 2015; 161:1297–1312
    [Google Scholar]
  4. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. Genbank. nucleic acids Res; 2009; 37D26–31
  5. Johnson AP. The pathogenic potential of commensal species of Neisseria . J Clin Pathol 1983; 36:213–223
    [Google Scholar]
  6. Rouphael NG, Stephens DS. Neisseria meningitidis: biology, microbiology, and epidemiology. Methods Mol Biol 2012; 799:1–20
    [Google Scholar]
  7. Clemence MEA, Maiden MCJ, Harrison OB. Characterization of capsule genes in non-pathogenic Neisseria species. Microb Genom 2018; 4:
    [Google Scholar]
  8. Ducey TF, Carson MB, Orvis J, Stintzi AP, Dyer DW. Identification of the iron-responsive genes of Neisseria gonorrhoeae by microarray analysis in defined medium. J Bacteriol 2005; 187:4865–4874
    [Google Scholar]
  9. Rohde KH, Dyer DW. Mechanisms of iron acquisition by the human pathogens Neisseria meningitidis and Neisseria gonorrhoeae . Front Biosci 2003; 8:d1186–1218
    [Google Scholar]
  10. Caza M, Kronstad JW. Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans. Front Cell Infect Microbiol 2013; 3:80
    [Google Scholar]
  11. Parrow NL, Fleming RE, Minnick MF. Sequestration and scavenging of iron in infection. Infect Immun 2013; 81:3503–3514
    [Google Scholar]
  12. Marri PR, Paniscus M, Weyand NJ, Rendón MA, Calton CM et al. Genome sequencing reveals widespread virulence gene exchange among human Neisseria species. PLoS One 2010; 5:e11835
    [Google Scholar]
  13. Coureuil M, Join-Lambert O, Lécuyer H, Bourdoulous S, Marullo S et al. Mechanism of meningeal invasion by Neisseria meningitidis . Virulence 2012; 3:164–172
    [Google Scholar]
  14. Mitchell L, Coley K, Morgan J. An unexpected increase in Neisseria meningitidis genital isolates among sexual health clinic attendees, Hamilton, New Zealand. Sex Transm Dis 2008; 35:469–471
    [Google Scholar]
  15. Retchless AC, Kretz CB, Chang HY, Bazan JA, Abrams AJ et al. Expansion of a urethritis-associated Neisseria meningitidis clade in the United States with concurrent acquisition of N. gonorrhoeae alleles. BMC Genomics 2018; 19:176
    [Google Scholar]
  16. Morris SR, Klausner JD, Buchbinder SP, Wheeler SL, Koblin B et al. Prevalence and incidence of pharyngeal gonorrhea in a longitudinal sample of men who have sex with men: the EXPLORE study. Clin Infect Dis 2006; 43:1284–1289
    [Google Scholar]
  17. Hananta IPY, De Vries HJC, van Dam AP, van Rooijen MS, Soebono H et al. Persistence after treatment of pharyngeal gonococcal infections in patients of the STI clinic, Amsterdam, the Netherlands, 2012-2015: a retrospective cohort study. Sex Transm Infect 2017; 93:467–471
    [Google Scholar]
  18. Eyre DW, Sanderson ND, Lord E, Regisford-Reimmer N, Chau K et al. Gonorrhoea treatment failure caused by a Neisseria gonorrhoeae strain with combined ceftriaxone and high-level azithromycin resistance, England, February 2018. Euro Surveill. 2018
    [Google Scholar]
  19. Eyre DW, Town K, Street T, Barker L, Sanderson N et al. Detection in the United Kingdom of the Neisseria gonorrhoeae FC428 clone, with ceftriaxone resistance and intermediate resistance to azithromycin, October to December 2018. Euro Surveill 2019
    [Google Scholar]
  20. Facius D, Fussenegger M, Meyer TF. Sequential action of factors involved in natural competence for transformation of Neisseria gonorrhoeae . FEMS Microbiol Lett 1996; 137:159–164 [CrossRef][PubMed]
    [Google Scholar]
  21. Snyder LA, Saunders NJ. The majority of genes in the pathogenic Neisseria species are present in non-pathogenic Neisseria lactamica, including those designated as 'virulence genes'. BMC Genomics 2006; 7:128
    [Google Scholar]
  22. Bennett JS, Bratcher HB, Brehony C, Harrison OB, Maiden MCJ. The Genus Neisseria . In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. (editors) The Prokaryotes: Alphaproteobacteria and Betaproteobacteria 2014 pp 881–900
    [Google Scholar]
  23. Maiden MC. Population genomics: diversity and virulence in the Neisseria . Curr Opin Microbiol 2008; 11:467–471
    [Google Scholar]
  24. Maiden MC, Harrison OB. Population and functional genomics of Neisseria revealed with gene-by-gene approaches. J Clin Microbiol 2016; 54:1949–1955
    [Google Scholar]
  25. Higashi DL, Biais N, Weyand NJ, Agellon A, Sisko JL et al. elongata produces type IV pili that mediate interspecies gene transfer with N. gonorrhoeae . PLoS One 2011; 6:e21373
    [Google Scholar]
  26. Bennett JS, Jolley KA, Earle SG, Corton C, Bentley SD et al. A genomic approach to bacterial taxonomy: an examination and proposed reclassification of species within the genus Neisseria . Microbiology 2012; 158:1570–1580
    [Google Scholar]
  27. Dillard JP, Seifert HS. A variable genetic island specific for Neisseria gonorrhoeae is involved in providing DNA for natural transformation and is found more often in disseminated infection isolates. Mol Microbiol 2001; 41:263–277
    [Google Scholar]
  28. Ramsey ME, Woodhams KL, Dillard JP. The Gonococcal Genetic Island and Type IV Secretion in the Pathogenic Neisseria . Front Microbiol 2011; 2:61
    [Google Scholar]
  29. Kellogg DS, Peacock WL, Deacon WE, Brown L, Pirkle DI. Neisseria gonorrhoeae. I. virulence genetically linked to clonal variation. J Bacteriol 1963; 85:1274–1279 [CrossRef][PubMed]
    [Google Scholar]
  30. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477
    [Google Scholar]
  31. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069
    [Google Scholar]
  32. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75
    [Google Scholar]
  33. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The seed and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 2014; 42:D206–214
    [Google Scholar]
  34. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S et al. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 2015; 5:8365 [CrossRef][PubMed]
    [Google Scholar]
  35. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624
    [Google Scholar]
  36. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P et al. Artemis: sequence visualization and annotation. Bioinformatics 2000; 16:944–945
    [Google Scholar]
  37. Snyder L. Sequence read Archive SRP078299; 2016
  38. Snyder L. Sequence read Archive SRP078300; 2016
  39. Snyder L. Sequence read Archive SRP078301; 2016
  40. Snyder L. Sequence read Archive SRP078302; 2016
  41. Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C et al. Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 2012; 158:1005–1015
    [Google Scholar]
  42. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410
    [Google Scholar]
  43. Zhang F, Zhao S, Ren C, Zhu Y, Zhou H et al. CRISPRminer is a knowledge base for exploring CRISPR-Cas systems in microbe and phage interactions. Commun Biol 2018; 1:180
    [Google Scholar]
  44. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder : a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 2007; 35:W52–57
    [Google Scholar]
  45. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Scalable generation of high-quality protein multiple sequence alignments using Clustal omega. Mol Syst Biol 2011; 7:539
    [Google Scholar]
  46. Li J, Yao Y, HH X, 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
    [Google Scholar]
  47. 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:
    [Google Scholar]
  48. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies, Mol. Biol. Evol 2006; 23:254–267
    [Google Scholar]
  49. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010; 5:e11147
    [Google Scholar]
  50. Topaz N, Retchless AC, Chang H-Y, Hu F, Wang X. Genbank NZ_CP031251; 2018
  51. Goldberg B, Campos J, Tallon L, Sadzewicz L, Sengamalay N et al. Genbank NZ_CP020452; 2017
  52. Streich RO, Curtis MA, Bradshaw DJ, Pratten J, Wade WG. Genbank NZ_CP039886; 2019
  53. Doyle S. Genbank NZ_LS483369; 2018
  54. Tettelin H, Saunders NJ, Heidelberg J, Jeffries AC, Nelson KE et al. Genbank NC_003112.2; 2012
  55. Bentley SD, Vernikos GS, Snyder LA, Churcher C, Arrowsmith C et al. Genbank NC_008767.1; 2012
  56. Bernardini G, Renzone G, Comanducci M, Mini R, Arena S et al. Genbank NC_003116.1; 2012
  57. Lewis LA, Gillaspy AF, McLaughlin RE, Gipson M, Ducey TF et al. Genbank NC_002946.2; 2012
  58. Chung GT, Yoo JS, Oh HB, Lee YS, Cha SH et al. Genbank NC_011035.1; 2011
  59. Bennett JS, Bentley SD, Vernikos GS, Quail MA, Cherevach I et al. Genbank NC_014752.1; 2012
  60. Streich RO, Curtis MA, Bradshaw DJ, Pratten J, Wade WG. Genbank NZ_CP039887; 2019
  61. Weinstock G, Sodergren E, Clifton S, Fulton L, Fulton B et al. Genbank NZ_ACEO00000000; 2010
  62. Nichols M, Topaz N, Wang X, Wang X, Boxrud D. Genbank C2012011976; 2018
  63. Nichols M, Topaz N, Wang X, Wang X, Boxrud D. Genbank C2011004960; 2018
  64. Nichols M, Topaz N, Wang X, Wang X, Boxrud D. Genbank C2009010520; 2018
  65. Nichols M, Topaz N, Wang X, Wang X, Boxrud D. Genbank C2011020198; 2018
  66. Nichols M, Topaz N, Wang X, Wang X, Boxrud D. Genbank C2005001510; 2018
  67. Nichols M, Topaz N, Wang X, Wang X, Boxrud D. Genbank C2014021188; 2018
  68. Nichols M, Topaz N, Wang X, Wang X, Boxrud D. Genbank C2011020199; 2018
  69. Nichols M, Topaz N, Wang X, Wang X, Boxrud D. Genbank C2011033015; 2018
  70. Nichols M, Topaz N, Wang X, Wang X, Boxrud D. GenBank C2008002238; 2018
  71. Nichols M, Topaz N, Wang X, Wang X, Boxrud D. Genbank C2011009653; 2018
  72. Nichols M, Topaz N, Wang X, Wang X, Boxrud D. Genbank C2007002879; 2018
  73. Nichols M, Topaz N, Wang X, Wang X, Boxrud D. Genbank C2008001664; 2018
  74. Yazdankhah SP, Caugant DA. Neisseria meningitidis: an overview of the carriage state. J Med Microbiol 2004; 53:821–832
    [Google Scholar]
  75. Vandamme P, Holmes B, Bercovier H, Coenye T. Classification of Centers for Disease Control Group Eugonic Fermenter (EF)-4a and EF-4b as Neisseria animaloris sp. nov. and Neisseria zoodegmatis sp. nov., respectively. Int J Syst Evol Microbiol 2006; 56:1801–1805
    [Google Scholar]
  76. Barbé G, Babolat M, Boeufgras JM, Monget D, Freney J. Evaluation of API NH, a new 2-hour system for identification of Neisseria and Haemophilus species and Moraxella catarrhalis in a routine clinical laboratory. J Clin Microbiol 1994; 32:187–189
    [Google Scholar]
  77. Knapp JS. Hook EW 3rd. Prevalence and persistence of Neisseria cinerea and other Neisseria spp. in adults. J Clin Microbiol 1988; 26:896–900
    [Google Scholar]
  78. Spencer-Smith R, Roberts S, Gurung N, Snyder LAS. DNA uptake sequences in Neisseria gonorrhoeae as intrinsic transcriptional terminators and markers of horizontal gene transfer. Microb Genom 2016; 2:e000069
    [Google Scholar]
  79. Spratt BG, Bowler LD, Zhang QY, Zhou J, Smith JM. Role of interspecies transfer of chromosomal genes in the evolution of penicillin resistance in pathogenic and commensal Neisseria species. J Mol Evol 1992; 34:115–125
    [Google Scholar]
  80. Davidsen T, Rødland EA, Lagesen K, Seeberg E, Rognes T et al. Biased distribution of DNA uptake sequences towards genome maintenance genes. Nucleic Acids Res 2004; 32:1050-–10508
    [Google Scholar]
  81. Berry JL, Cehovin A, McDowell MA, Lea SM, Pelicic V. Functional analysis of the interdependence between DNA uptake sequence and its cognate ComP receptor during natural transformation in Neisseria species. PLoS Genet 2013; 9:e1004014
    [Google Scholar]
  82. Frye SA, Nilsen M, Tønjum T, Ambur OH. Dialects of the DNA uptake sequence in Neisseriaceae . PLoS Genet 2013; 9:e1003458
    [Google Scholar]
  83. Lery LM, 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
    [Google Scholar]
  84. Harrison OB, Schoen C, Retchless AC, Wang X, Jolley KA et al. Neisseria genomics: current status and future perspectives. Pathog Dis 2017; 75:
    [Google Scholar]
  85. Hollingshead S, Tang CM. An Overview of Neisseria meningitidis . Methods Mol Biol 1969; 2019:1–16
    [Google Scholar]
  86. Quillin SJ, Seifert HS. Neisseria gonorrhoeae host adaptation and pathogenesis. Nat Rev Microbiol 2018; 16:226–240
    [Google Scholar]
  87. Ribet D, Cossart P. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect 2015; 17:173–183
    [Google Scholar]
  88. Hung MC, Christodoulides M. The biology of Neisseria adhesins. Biology 2013; 2:1054–1109
    [Google Scholar]
  89. Hagman KE, Pan W, Spratt BG, Balthazar JT, Judd RC et al. Resistance of Neisseria gonorrhoeae to antimicrobial hydrophobic agents is modulated by the mtrRCDE efflux system. Microbiology 1995; 141:611–622
    [Google Scholar]
  90. Shafer WM, Veal WL, Lee EH, Zarantonelli L, Balthazar JT et al. Genetic organization and regulation of antimicrobial efflux systems possessed by Neisseria gonorrhoeae and Neisseria meningitidis . J Mol Microbiol Biotechnol 2001; 3:219–224
    [Google Scholar]
  91. Lee EH, Shafer WM. The farAB-encoded efflux pump mediates resistance of gonococci to long-chained antibacterial fatty acids. Mol Microbiol 1999; 33:839–845
    [Google Scholar]
  92. Plant L, Jonsson AB. Contacting the host: insights and implications of pathogenic Neisseria cell interactions. Scand J Infect Dis 2003; 35:608–613
    [Google Scholar]
  93. Wistreich GA, Baker RF. The presence of fimbriae (pili) in three species of Neisseria . J Gen Microbiol 1971; 65:167–173
    [Google Scholar]
  94. Wörmann ME, Horien CL, Johnson E, Liu G, Aho E et al. Neisseria cinerea isolates can adhere to human epithelial cells by type IV pilus-independent mechanisms. Microbiology 2016; 162:487–502
    [Google Scholar]
  95. Rahman M, Källström H, Normark S, Jonsson AB. PilC of pathogenic Neisseria is associated with the bacterial cell surface. Mol Microbiol 1997; 25:11–25
    [Google Scholar]
  96. Fussenegger M, Rudel T, Barten R, Ryll R, Meyer TF. Transformation competence and type-4 pilus biogenesis in Neisseria gonorrhoeae-a review. Gene 1997; 192:125–134
    [Google Scholar]
  97. Hamrick TS, Dempsey JA, Cohen MS, Cannon JG. Antigenic variation of gonococcal pilin expression in vivo: analysis of the strain FA1090 pilin repertoire and identification of the pilS gene copies recombining with pilE during experimental human infection. Microbiology 2001; 147:839–849
    [Google Scholar]
  98. Kahler CM, Martin LE, Tzeng YL, Miller YK, Sharkey K et al. Polymorphisms in pilin glycosylation locus of Neisseria meningitidis expressing class II pili. Infect Immun 2001; 69:3597–3604
    [Google Scholar]
  99. Bennett JS, Bentley SD, Vernikos GS, Quail MA, Cherevach I et al. Independent evolution of the core and accessory gene sets in the genus Neisseria: insights gained from the genome of Neisseria lactamica isolate 020-06. BMC Genomics 2010; 11:652
    [Google Scholar]
  100. Harrison OB, Claus H, Jiang Y, Bennett JS, Bratcher HB et al. Description and nomenclature of Neisseria meningitidis capsule locus. Emerg Infect Dis 2013; 19:566–573
    [Google Scholar]
  101. Bartley SN, Mowlaboccus S, Mullally CA, Stubbs KA, Vrielink A et al. Acquisition of the capsule locus by horizontal gene transfer in Neisseria meningitidis is often accompanied by the loss of UDP-GalNAc synthesis. Sci Rep 2017; 7:44442
    [Google Scholar]
  102. Swartley JS, Marfin AA, Edupuganti S, Liu LJ, Cieslak P et al. Capsule switching of Neisseria meningitidis . Proc Natl Acad Sci U S A 1997; 94:271–276
    [Google Scholar]
  103. Mustapha MM, Lemos APS, Griffith MP, Evans DR, Marx R et al. Two cases of newly characterized Neisseria species, Brazil. Emerg Infect Dis 2020; 26:366–369
    [Google Scholar]
  104. Serruto D, Bottomley MJ, Ram S, Giuliani MM, Rappuoli R. The new multicomponent vaccine against meningococcal serogroup B, 4CMenB: immunological, functional and structural characterization of the antigens. Vaccine 2012; 30:B87–97
    [Google Scholar]
  105. Gorringe AR, Pajón R. Bexsero: a multicomponent vaccine for prevention of meningococcal disease. Hum Vaccin Immunother 2012; 8:174–183
    [Google Scholar]
  106. Tzeng YL, Thomas J, Stephens DS. Regulation of capsule in Neisseria meningitidis . Crit Rev Microbiol 2016; 42:759–772
    [Google Scholar]
  107. Capecchi B, Adu-Bobie J, Di Marcello F, Ciucchi L, Masignani V et al. Neisseria meningitidis NadA is a new invasin which promotes bacterial adhesion to and penetration into human epithelial cells. Mol Microbiol 2005; 55:687–698
    [Google Scholar]
  108. Lucidarme J, Gilchrist S, Newbold LS, Gray SJ, Kaczmarski EB et al. Genetic distribution of noncapsular meningococcal group B vaccine antigens in Neisseria lactamica . Clin Vaccine Immunol 2013; 20:1360–1369
    [Google Scholar]
  109. Gibbs CP, Meyer TF. Genome plasticity in Neisseria gonorrhoeae . FEMS Microbiol Lett 1996; 145:173–179
    [Google Scholar]
  110. Snyder LA, Jarvis SA, Saunders NJ. Complete and variant forms of the 'gonococcal genetic island' in Neisseria meningitidis . Microbiology 2005; 151:4005–4013
    [Google Scholar]
  111. Woodhams KL, Benet ZL, Blonsky SE, Hackett KT, Dillard JP. Prevalence and detailed mapping of the gonococcal genetic island in Neisseria meningitidis . J Bacteriol 2012; 194:2275–2285
    [Google Scholar]
  112. Li YG, Christie PJ. The Agrobacterium VirB/VirD4 T4SS: mechanism and architecture defined through in vivo mutagenesis and chimeric systems. Curr Top Microbiol Immunol 2018; 418:233–260
    [Google Scholar]
  113. Hébert L, Moumen B, Pons N, Duquesne F, Breuil MF et al. Genomic characterization of the Taylorella genus. PLoS ONE 2012; 7:
    [Google Scholar]
  114. Jeltsch A. Maintenance of species identity and controlling speciation of bacteria: a new function for restriction/modification systems?. Gene 2003; 317:13–16
    [Google Scholar]
  115. Palmer KL, Godfrey P, Griggs A, Kos VN, Zucker J et al. Comparative genomics of enterococci: variation in Enterococcus faecalis, clade structure in E. faecium, and defining characteristics of E. gallinarum and E. casseliflavus . MBio 2012; 3:e00318-11
    [Google Scholar]
  116. Zhang Y. The CRISPR-Cas9 system in Neisseria spp. Pathog Dis 2017; 75:
    [Google Scholar]
  117. Stern A, Keren L, Wurtzel O, Amitai G, Sorek R. Self-targeting by CRISPR: gene regulation or autoimmunity?. Trends Genet 2010; 26:335–340
    [Google Scholar]
  118. Garneau JE, D, Villion M, Romero DA, Barrangou R et al. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 2010; 468:67–71
    [Google Scholar]
  119. Heussler GE, O'Toole GA. Friendly fire: biological functions and consequences of chromosomal targeting by CRISPR-Cas systems. J Bacteriol 2016; 198:1481–-6
    [Google Scholar]
  120. Shabbir MA, Hao H, Shabbir MZ, Hussain HI, Iqbal Z et al. Survival and evolution of CRISPR-Cas system in prokaryotes and its applications. Front Immunol. 2016; 7:eCollection 2016375
    [Google Scholar]
  121. Basler M. Type VI secretion system: secretion by a contractile nanomachine. Philos Trans R Soc Lond B Biol Sci 2015; 370:pii: 20150021
    [Google Scholar]
  122. 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
    [Google Scholar]
  123. Filloux A. The rise of the type VI secretion system. F1000Prime Rep 2013; 5:52
    [Google Scholar]
  124. 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; 7:1635–1643
    [Google Scholar]
  125. Cianfanelli FR, Monlezun L, Aim CSJ. Load, fire: the type VI secretion system, a bacterial Nanoweapon. Trends Microbiol 2016; 24:51–62
    [Google Scholar]
  126. Thomas J, Watve SS, Ratcliff WC, Hammer BK. Horizontal gene transfer of functional type VI killing genes by natural transformation. MBio 2017; 8:e00654–17
    [Google Scholar]
  127. Lin J, Zhang W, Cheng J, Yang X, Zhu K et al. Shen X. A Pseudomonas T6SS effector recruits PQS-containing outer membrane vesicles for iron acquisition. Nat Commun 2017; 8:14888
    [Google Scholar]
  128. Unterweger D, Kostiuk B, Pukatzki S. Adaptor proteins of type VI secretion system effectors. Trends Microbiol 2017; 25:8–10
    [Google Scholar]
  129. 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; 11:1085 [CrossRef]
    [Google Scholar]
  130. Pramanik A, Könninger U, Selvam A, Braun V. Secretion and activation of the Serratia marcescens hemolysin by structurally defined ShlB mutants. Int J Med Microbiol 2014; 304:351–359 [CrossRef]
    [Google Scholar]
  131. Schiebel E, Schwarz H, Braun V. Subcellular location and unique secretion of the hemolysin of Serratia marcescens . J Biol Chem 1989; 264:16311–16320[PubMed]
    [Google Scholar]
  132. Choby JE, Skaar EP. Heme synthesis and acquisition in bacterial pathogens. J Mol Biol 2016; 428:3408–3428 [CrossRef][PubMed]
    [Google Scholar]
  133. Schryvers AB, Stojiljkovic I. Iron acquisition systems in the pathogenic Neisseria . Mol Microbiol 1999; 32:1117–1123 [CrossRef][PubMed]
    [Google Scholar]
  134. Sekine Y, Tanzawa T, Tanaka Y, Ishimori K, Uchida T. Cytoplasmic heme-binding protein (HutX) from Vibrio cholerae is an intracellular heme transport protein for the heme-degrading enzyme, HutZ. Biochemistry 2016; 55:884–893 [CrossRef][PubMed]
    [Google Scholar]
  135. Wang T, Si M, Song Y, Zhu W, Gao F et al. Type VI secretion system transports Zn2+ to combat multiple stresses and host immunity. PLoS Pathog 2015; 11:e1005020 [CrossRef][PubMed]
    [Google Scholar]
  136. Marinaro M, Di Tommaso A, Uzzau S, Fasano A, De Magistris MT. Zonula occludens toxin is a powerful mucosal adjuvant for intranasally delivered antigens. Infect Immun 1999; 67:1287–1291 [CrossRef][PubMed]
    [Google Scholar]
  137. Kaakoush NO, Man SM, Lamb S, Raftery MJ, Wilkins MR et al. The secretome of Campylobacter concisus . Febs J 2010; 277:1606–1617 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000423
Loading
/content/journal/mgen/10.1099/mgen.0.000423
Loading

Data & Media loading...

Most cited this month 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