The Trojan Horse of the microbiological arms race: Phage-encoded toxins as a defence against eukaryotic predators

Environmental Microbiology

Volumn 16, Issue 2, 2014, Pages 454-466

  Arnold, Jason W ^a   Koudelka, Gerald B ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACANTHAMOEBA; ACANTHAMOEBA CASTELLANII; BACTERIA (MICROORGANISMS); CORYNEBACTERIUM DIPHTHERIAE; EQUIDAE; EUKARYOTA; TETRAHYMENA;

CELL SURFACE RECEPTOR; DIPHTHERIA TOXIN; EXOTOXIN; SHIGA TOXIN;

ACANTHAMOEBA CASTELLANII; ANTIBIOSIS; ARTICLE; BACTERIOPHAGE; COCULTURE; CORYNEBACTERIUM DIPHTHERIAE; CULTURE MEDIUM; METABOLISM; MICROBIOLOGY; PHAGOCYTOSIS; PHYSIOLOGY;

ACANTHAMOEBA CASTELLANII; ANTIBIOSIS; BACTERIOPHAGES; COCULTURE TECHNIQUES; CORYNEBACTERIUM DIPHTHERIAE; CULTURE MEDIA; DIPHTHERIA TOXIN; EXOTOXINS; PHAGOCYTOSIS; RECEPTORS, CELL SURFACE; SHIGA TOXIN;

EID: 84893004381     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12232     Document Type: Article

References (57)

1. Agu, C.A., Klein, R., Schwab, S., König-Schuster, M., Kodajova, P., Ausserlechner, M., etal. (2006) The cytotoxic activity of the bacteriophage λ-holin protein reduces tumour growth rates in mammary cancer cell xenograft models. J Gene Med 8: 229-241.
2. Alsam, S., Jeong, S.R., Sissons, J., Dudley, R., Kim, K.S., and Khan, N.A. (2006) Escherichia coli interactions with Acanthamoeba: a symbiosis with environmental and clinical implications. J Med Microbiol 55: 689-694.
3. Axelsson-Olsson, D., Olofsson, J., Ellström, P., Waldenström, J., and Olsen, B. (2009) A simple method for long-term storage of Acanthamoeba species. Parasitol Res 104: 935-937.
4. Barker, J., Humphrey, T.J., and Brown, M.W.R. (1999) Survival of Escherichia coli 0157 in a soil protozoan: implications for disease. FEMS Microbiol Lett 173: 291-295.
5. Berninger, U., Finlay, B.J., and Kuuppo-Leinikk, P. (1991) Protozoan control of bacterial abundances in freshwater. Limnol Oceanogr 36: 139-147.
6. Bowers, B., and Olszewski, T.E. (1972) Pinocytosis in Acanthamoeba castellanii: kinetics and morphology. J Cell Biol 53: 681-694.
7. Brussow, H., Canchaya, C., and Hardt, W.-D. (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68: 560-602.
8. Brüssow, H. (2007) Bacteria between protists and phages: from antipredation strategies to the evolution of pathogenicity. Mol Microbiol 65: 583-589.
9. Casas, V., Miyake, J., Balsley, H., Roark, J., Telles, S., Leeds, S., etal. (2006) Widespread occurrence of phage-encoded exotoxin genes in terrestrial and aquatic environments in Southern California. FEMS Microbiol Lett 261: 141-149.
10. Chekabab, S.M., Daigle, F., Charette, S.J., Dozois, C.M., and Harel, J. (2013) Shiga toxins decrease enterohaemorrhagic Escherichia coli survival within Acanthamoeba castellanii. FEMS Microbiol Lett 344: 86-93.
11. Daniels, D., Schroeder, J.L., Szybalski, W., Sanger, F., Coulson, A.R., Hong, G.F., etal. (1983) Lambda II. New York, NY, USA: Cold Spring Harbor Laboratory.
12. Dong, M., Yeh, F., Tepp, W.H., Dean, C., Johnson, E.A., Janz, R., and Chapman, E.R. (2006) SV2 Is the protein receptor for Botulinum Neurotoxin A. Science 312: 592-596.
13. Drazin, R., Kandel, J., and Collier, R.J. (1971) Structure and activity of Diphtheria toxin: II. attack by trypsin at a specific site within the intact toxin molecule. J Biol Chem 246: 1504-1510.
14. Eidels, L., Proia, R.L., and Hart, D.A. (1983) Membrane receptors for bacterial toxins. Microbiol Rev 47: 596-620.
15. Faucher, S.P., Mueller, C.A., and Shuman, H.A. (2011) Legionella pneumophila transcriptome during intracellular multiplication in human macrophages. Front Microbiol 2: 60.
16. Gobert, A.P., Vareille, M., Glasser, A.L., Hindre, T., de Sablet, T., and Martin, C. (2007) Shiga toxin produced by enterohemorrhagic Escherichia coli inhibits PI3K/NF-kappa B signaling pathway in globotriaosylceramide-3-negative human intestinal epithelial cells. J Immunol 178: 8168-8174.
17. Holmes, R.K. (2000) Biology and molecular epidemiology of diphtheria toxin and the tox gene. J Infect Dis 181: S156-S167.
18. Howell, M.D., and Villemez, C.L. (1984) Toxicity of ricin, diphtheria toxin and alpha-Amanitin for Acanthamoeba castellanii (1983). J Parasitol 70: 918-923.
19. Jacewicz, M., Clausen, H., Nudelman, E., Donohue-Rolfe, A., and Keusch, G.T. (1986) Pathogenesis of shigella diarrhea. XI. Isolation of a shigella toxin-binding glycolipid from rabbit jejunum and HeLa cells and its identification as globotriaosylceramide. J Exp Med 163: 1391-1404.
20. Johannes, L., and Romer, W. (2010) Shiga toxins [mdash] from cell biology to biomedical applications. Nat Rev Micro 8: 105-116.
21. Jousset, A. (2012) Ecological and evolutive implications of bacterial defences against predators. Environ Microbiol 14: 1830-1843.
22. Keusch, J.J., Manzella, S.M., Nyame, K.A., Cummings, R.D., and Baenziger, J.U. (2000) Cloning of Gb3 synthase, the key enzyme in globo-series glycosphingolipid synthesis, predicts a family of alpha 1, 4-glycosyltransferases conserved in plants, insects, and mammals. J Biol Chem 275: 25315-25321.
23. Kiarash, A., Boyd, B., and Lingwood, C.A. (1994) Glycosphingolipid receptor function is modified by fatty acid content. Verotoxin 1 and verotoxin 2c preferentially recognize different globotriaosyl ceramide fatty acid homologues. J Biol Chem 269: 11138-11146.
24. Kilvington, S., and White, D. (1991) A simple method for the cryopreservation of free-living amoebae belonging to the genera Naegleria and Acanthamoeba. Eur J Protistol 27: 115-118.
25. Kim, J.-H., Matin, A., Shin, H.-J., Park, H., Yoo, K.-T., Yuan, X.-Z., etal. (2012) Functional roles of mannose-binding protein in the adhesion, cytotoxicity and phagocytosis of Acanthamoeba castellanii. Exp Parasitol 132: 287-292.
26. Lainhart, W., Stolfa, G., and Koudelka, G.B. (2009) Shiga toxin as a bacterial defense against a eukaryotic predator, Tetrahymena thermophila. J Bacteriol 191: 5116-5122.
27. Livny, J., and Friedman, D.I. (2004) Characterizing spontaneous induction of Stx encoding phages using a selectable reporter system. Mol Microbiol 51: 1691-1704.
28. Matz, C., and Kjelleberg, S. (2005) Off the hook - how bacteria survive protozoan grazing. Trends Microbiol 13: 302-307.
29. Minot, S., Sinha, R., Chen, J., Li, H., Keilbaugh, S.A., Wu, G.D., etal. (2011) The human gut virome: inter-individual variation and dynamic response to diet. Genome Res 21: 1616-1625.
30. Naglich, J.G., Metherall, J.E., Russell, D.W., and Eidels, L. (1992) Expression cloning of a diphtheria toxin receptor: identity with a heparin-binding EGF-like growth factor precursor. Cell 69: 1051-1061.
31. Pappenheimer, A.M., Jr (1977) Diphtheria toxin. Annu Rev Biochem 46: 69-94.
32. Ptashne, M. (1986) A Genetic Switch. Palo Alto, CA, USA: Blackwell Press.
33. Ramegowda, B., and Tesh, V.L. (1996) Differentiation-associated toxin receptor modulation, cytokine production, and sensitivity to Shiga-like toxins in human monocytes and monocytic cell lines. Infect Immun 64: 1173-1180.
34. Rappuoli, R., Michel, J.L., and Murphy, J.R. (1983) Integration of corynebacteriophages beta tox+, omega tox+, and gamma tox- into two attachment sites on the Corynebacterium diphtheriae chromosome. J Bacteriol 153: 1202-1210.
35. Samuel, J.E., Perera, L.P., Ward, S., O'Brien, A.D., Ginsburg, V., and Krivan, H.C. (1990) Comparison of the glycolipid receptor specificities of Shiga-like toxin type II and Shiga-like toxin type II variants. Infect Immun 58: 611-618.
36. Sandvig, K., and van Deurs, B. (2000) Entry of ricin and Shiga toxin into cells: molecular mechanisms and medical perspectives. EMBO J 19: 5943-5950.
37. Sandvig, K., Grimmer, S., Lauvrak, S.U., Torgersen, M.L., Skretting, G., van Deurs, B., and Iversen, T.G. (2002) Pathways followed by ricin and Shiga toxin into cells. Histochem Cell Biol 117: 131-141.
38. Sandvig, K., Bergan, J., Dyve, A.-B., Skotland, T., and Torgersen, M.L. (2010) Endocytosis and retrograde transport of Shiga toxin. Toxicon 56: 1181-1185.
39. Segal, G., and Shuman, H.A. (1999) Legionella pneumophila utilizes the same genes to multiply within Acanthamoeba castellanii and human macrophages. Infect Immun 67: 2117-2124.
40. Segal, G., Purcell, M., and Shuman, H.A. (1998) Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc Natl Acad Sci USA 95: 1669-1674.
41. van Setten, P.A., Monnens, L.A., Verstraten, R.G., van den Heuvel, L.P., and van Hinsbergh, V.W. (1996) Effects of verocytotoxin-1 on nonadherent human monocytes: binding characteristics, protein synthesis, and induction of cytokine release. Blood 88: 174-183.
42. Sherr, B.F., and Sherr, E.B. (1984) Role of heterotrophic protozoa in carbon and energy flow in aquatic ecosystems. In Current Perspectives in Microbial Ecology. Klug, M.J., and Reddy, C.A. (eds). Washington, DC, USA: American Society for Microbiology, pp. 412-423.
43. Shimizu, T., Ohta, Y., and Noda, M. (2009) Shiga toxin 2 is specifically released from bacterial cells by two different mechanisms. Infect Immun 77: 2813-2823.
44. Shkilnyj, P., and Koudelka, G.B. (2007) Effect of salt shock on the stability of l imm434 Lysogens. J Bacteriol 189: 3115-3123.
45. Siddiqui, R., and Khan, N.A. (2012a) Acanthamoeba is an evolutionary ancestor of macrophages: a myth or reality. Exp Parasitol 130: 95-97.
46. Siddiqui, R., and Khan, N. (2012b) Biology and pathogenesis of Acanthamoeba. Parasit Vectors 5: 6.
47. Silverman, J.A., Mindell, J.A., Finkelstein, A., Shen, W.H., and Collier, R.J. (1994) Mutational analysis of the helical hairpin region of diphtheria toxin transmembrane domain. J Biol Chem 269: 22524-22532.
48. Steinert, M., Birkness, K., White, E., Fields, B., and Quinn, F. (1998) Mycobacterium avium bacilli grow saprozoically in coculture with Acanthamoeba polyphaga and survive within cyst walls. Appl Environ Microbiol 64: 2256-2261.
49. Stolfa, G., and Koudelka, G.B. (2013) Entry and killing of Tetrahymena thermophila by bacterially produced Shiga toxin. mBio 4: e00416-12.
50. Tesh, V.L., Ramegowda, B., and Samuel, J.E. (1994) Purified Shiga-like toxins induce expression of proinflammatory cytokines from murine peritoneal macrophages. Infect Immun 62: 5085-5094.
51. Tseng, T.-T., Tyler, B., and Setubal, J. (2009) Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. BMC Microbiol 9: S2.
52. Tyler, J.S., Mills, M.J., and Friedman, D.I. (2004) The operator and early promoter region of the Shiga toxin type 2-encoding bacteriophage 933W and control of toxin expression. J Bacteriol 186: 7670-7679.
53. Wagner, P.L., Neely, M.N., Zhang, X., Acheson, D.W., Waldor, M.K., and Friedman, D.I. (2001) Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J Bacteriol 183: 2081-2085.
54. Wagner, P.L., Livny, J., Neely, M.N., Acheson, D.W., Friedman, D.I., and Waldor, M.K. (2002) Bacteriophage control of Shiga toxin 1 production and release by Escherichia coli. Mol Microbiol 44: 957-970.
55. Weinbauer, M.G. (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28: 127-181.
56. Wen, S.X., Teel, L.D., Judge, N.A., and O'Brien, A.D. (2006) Genetic toxoids of Shiga toxin types 1 and 2 protect mice against homologous but not heterologous toxin challenge. Vaccine 24: 1142-1148.
57. Yan, L., Cerny, R.L., and Cirillo, J.D. (2004) Evidence that hsp90 Is involved in the altered interactions of Acanthamoeba castellanii variants with bacteria. Eukaryot Cell 3: 567-578.