Multicellular Bacteria Deploy the Type VI Secretion System to Preemptively Strike Neighboring Cells

PLoS Pathogens

Volumn 9, Issue 9, 2013, Pages

  Alteri, Christopher J ^a   Himpsl, Stephanie D ^a   Pickens, Shannon R ^a   Lindner, Jonathon R ^a   Zora, Jonathan S ^a   Miller, Jessa E ^a   Arno, Peter D ^a   Straight, Samuel W ^a   Mobley, Harry L T ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; RNA DIRECTED DNA POLYMERASE; THIOREDOXIN;

ARTICLE; BACTERICIDAL ACTIVITY; CELL CONTACT; CELL DEATH; CELL DENSITY; CELL VIABILITY; CELLULAR IMMUNITY; COLONY FORMING UNIT; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENETIC COMPLEMENTATION; NONHUMAN; PHASE CONTRAST MICROSCOPY; PHENOTYPE; PHYLOGENETIC TREE; POLYMERASE CHAIN REACTION; PROTEUS MIRABILIS; SEQUENCE ALIGNMENT; TRANSPOSON; TYPE VI SECRETION SYSTEM;

BACTERIAL SECRETION SYSTEMS; DNA TRANSPOSABLE ELEMENTS; MICROBIAL INTERACTIONS; MUTAGENESIS; PROTEUS MIRABILIS;

EID: 84884680533     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003608     Document Type: Article

References (47)

1. Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, et al. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312: 1526-1530.
2. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, et al. (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103: 1528-1533.
3. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ, (2007) 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 104: 15508-15513.
4. Ma AT, Mekalanos JJ, (2010) In vivo actin cross-linking induced by Vibrio cholerae type VI secretion system is associated with intestinal inflammation. Proc Natl Acad Sci U S A 107: 4365-4370.
5. Hood RD, Singh P, Hsu F, Guvener T, Carl MA, et al. (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7: 25-37.
6. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, et al. (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475: 343-U392.
7. Riley MA, Wertz JE, (2002) Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol 56: 117-137.
8. Cotter P, (2011) Microbiology: Molecular syringes scratch the surface. Nature 475: 301-303.
9. Dienes L, (1946) Reproductive processes in Proteus cultures. Proc Soc Exp Biol Med 63: 265-270.
10. Dienes L, (1947) Further observations on the reproduction of bacilli from large bodies in Proteus cultures. Proc Soc Exp Biol Med 66: 97.
11. Senior BW, (1977) Dienes Phenomenon- Identification of Determinants of Compatibility. Journal of General Microbiology 102: 235-244.
12. Pfaller MA, Mujeeb I, Hollis RJ, Jones RN, Doern GV, (2000) Evaluation of the discriminatory powers of the dienes test and ribotyping as typing methods for Proteus mirabilis. J Clin Microbiol 38: 1077-1080.
13. De Louvois J, (1969) Serotyping and the Dienes reaction on Proteus mirabilis from hospital infections. J Clin Pathol 22: 263-268.
14. Budding AE, Ingham CJ, Bitter W, Vandenbroucke-Grauls CM, Schneeberger PM, (2009) The Dienes phenomenon: competition and territoriality in Swarming Proteus mirabilis. J Bacteriol 191: 3892-3900.
15. Gibbs KA, Urbanowski ML, Greenberg EP, (2008) Genetic determinants of self identity and social recognition in bacteria. Science 321: 256-259.
16. Gibbs KA, Greenberg EP, (2011) Territoriality in Proteus: advertisement and aggression. Chem Rev 111: 188-194.
17. Gibbs KA, Wenren LM, Greenberg EP, (2011) Identity Gene Expression in Proteus mirabilis. J Bacteriol 193: 3286-3292.
18. Mobley HL, Belas R, (1995) Swarming and pathogenicity of Proteus mirabilis in the urinary tract. Trends Microbiol 3: 280-284.
19. Allison C, Hughes C, (1991) Bacterial swarming: an example of prokaryotic differentiation and multicellular behaviour. Sci Prog 75: 403-422.
20. Basler M, Ho BT, Mekalanos JJ, (2013) Tit-for-Tat: Type VI Secretion System Counterattack during Bacterial Cell-Cell Interactions. Cell 152: 884-894.
21. Basler M, Mekalanos JJ, (2012) Type 6 secretion dynamics within and between bacterial cells. Science 337: 815.
22. Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ, (2012) Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483: 182-U178.
23. Dong TG, Ho BT, Yoder-Himes DR, Mekalanos JJ, (2013) Identification of T6SS-dependent effector and immunity proteins by Tn-seq in Vibrio cholerae. Proc Natl Acad Sci U S A 110: 2623-2628.
24. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM, et al. (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci U S A 106: 4154-4159.
25. Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I, (2009) 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 10: 104.
26. Rossmann MG, Mesyanzhinov VV, Arisaka F, Leiman PG, (2004) The bacteriophage T4 DNA injection machine. Curr Opin Struct Biol 14: 171-180.
27. Tewari R, Bailes E, Bunting KA, Coates JC, (2010) Armadillo-repeat protein functions: questions for little creatures. Trends Cell Biol 20: 470-481.
28. Pawson T, Nash P, (2003) Assembly of cell regulatory systems through protein interaction domains. Science 300: 445-452.
29. Lane MC, Alteri CJ, Smith SN, Mobley HLT, (2007) Expression of flagella is coincident with uropathogenic Escherichia coli ascension to the upper urinary tract. Proc Natl Acad Sci U S A 104: 16669-16674.
30. Aoki SK, Pamma R, Hernday AD, Bickham JE, Braaten BA, et al. (2005) Contact-dependent inhibition of growth in Escherichia coli. Science 309: 1245-1248.
31. Poole SJ, Diner EJ, Aoki SK, Braaten BA, de Roodenbeke CT, et al. (2011) Identification of Functional Toxin/Immunity Genes Linked to Contact-Dependent Growth Inhibition (CDI) and Rearrangement Hotspot (Rhs) Systems. Plos Genetics 7: e1002217.
32. Aoki SK, Diner EJ, de Roodenbeke CT, Burgess BR, Poole SJ, et al. (2010) A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 468: 439-442.
33. Erickson M, Newman D, Helm RA, Dino A, Calcutt M, et al. (2009) Competition among isolates of Salmonella enterica ssp enterica serovar Typhimurium: role of prophage/phage in archived cultures. FEMS Microbiol Lett 294: 37-44.
34. Bettelheim KA, Carlile MJ, (1976) Colony Incompatibility in Bacteria. Nature 264: 757-758.
35. Munson EL, Pfaller MA, Doern GV, (2002) Modification of dienes mutual inhibition test for epidemiological characterization of Pseudomonas aeruginosa isolates. J Clin Microbiol 40: 4285-4288.
36. De Maayer P, Venter SN, Kamber T, Duffy B, Coutinho TA, et al. (2011) 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 12: 576.
37. Russell AB, Singh P, Brittnacher M, Bui NK, Hood RD, et al. (2012) A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 11: 538-549.
38. Dong TG, Mekalanos JJ, (2012) Characterization of the RpoN regulon reveals differential regulation of T6SS and new flagellar operons in Vibrio cholerae O37 strain V52. Nucleic Acids Research 40: 7766-7775.
39. West SA, Gardner A, (2010) Altruism, spite, and greenbeards. Science 327: 1341-1344.
40. Hamilton WD, (1964) The genetical evolution of social behaviour. I. J Theor Biol 7: 1-16.
41. Jones BD, Mobley HL, (1987) Genetic and biochemical diversity of ureases of Proteus, Providencia, and Morganella species isolated from urinary tract infection. Infect Immun 55: 2198-2203.
42. Himpsl SD, Lockatell CV, Hebel JR, Johnson DE, Mobley HL, (2008) Identification of virulence determinants in uropathogenic Proteus mirabilis using signature-tagged mutagenesis. J Med Microbiol 57: 1068-1078.
43. Alteri CJ, Smith SN, Mobley HLT, (2009) Fitness of Escherichia coli during Urinary Tract Infection Requires Gluconeogenesis and the TCA Cycle. PLoS Pathog 5: e1000448.
44. Bevis BJ, Glick BS, (2002) Rapidly maturing variants of the Discosoma red fluorescent protein (DsRed). Nat Biotechnol 20: 83-87.
45. Kanehisa M, Goto S, (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Research 28: 27-30.
46. Thompson JD, Higgins DG, Gibson TJ, (1994) Clustal-W- Improving the Sensitivity of Progressive Multiple Sequence Alignment through Sequence Weighting, Position-Specific Gap Penalties and Weight Matrix Choice. Nucleic Acids Research 22: 4673-4680.
47. Warren JW, Tenney JH, Hoopes JM, Muncie HL, Anthony WC, (1982) A prospective microbiologic study of bacteriuria in patients with chronic indwelling urethral catheters. J Infect Dis 146: 719-723.