Amoebae as Potential Environmental Hosts for Mycobacterium ulcerans and Other Mycobacteria, but Doubtful Actors in Buruli Ulcer Epidemiology

PLoS Neglected Tropical Diseases

Volumn 6, Issue 8, 2012, Pages

  Gryseels, Sophie ^a   Amissah, Diana ^b   Durnez, Lies ^c   Vandelannoote, Koen ^c   Leirs, Herwig ^a,d   de Jonckheere, Johan ^e,f   Silva, Manuel T ^g   Portaels, Françoise ^c   Ablordey, Anthony ^b   Eddyani, Miriam ^c  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b University of Ghana   (Ghana)

^c INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^d Danish Pest Infestation Laboratory   (Denmark)

^e DE DUVE INSTITUTE   (Belgium)

^f SCIENTIFIC INSTITUTE OF PUBLIC HEALTH   (Belgium)

^g UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BIOCHEMICAL MARKER; IS2404; IS2406; POLYKETIDE SYNTHASE; UNCLASSIFIED DRUG;

ACANTHAMOEBA POLYPHAGA; ARTICLE; BACTERIAL TRANSMISSION; BACTERIAL VIABILITY; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATION; BIOFILM; BURULI ULCER; CONTROLLED STUDY; DETRITUS; HOST; MYCOBACTERIUM ULCERANS; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; WATER ANALYSIS;

AMOEBA; BURULI ULCER; DISEASE RESERVOIRS; DNA TRANSPOSABLE ELEMENTS; DNA, BACTERIAL; ENVIRONMENTAL MICROBIOLOGY; GHANA; HUMANS; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM; PHAGOCYTOSIS; SEQUENCE ANALYSIS, DNA;

EID: 84865973333     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001764     Document Type: Article

References (63)

1. Falkinham JO, (2002) Nontuberculous mycobacteria in the environment. Clin Chest Med 23: 529-551.
2. WHO World Health Organization "Buruli ulcer: Number of new cases of Buruli ulcer reported (per year). Available: http://apps.who.int/neglected_diseases/ntddata/buruli/buruli.html. Accessed 2012 Jul 15.
3. Merritt RW, Walker ED, Small PLC, Wallace JR, Johnson PDR, et al. (2010) Ecology and transmission of Buruli ulcer disease: a systematic review. PloS Negl Trop Dis 4: e911.
4. Stinear TP, Seemann T, Pidot S, Frigui W, Reysset G, et al. (2007) Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer. Genome Res 17: 192-200.
5. Miltner EC, Bermudez LE, (2000) Mycobacterium avium grown in Acanthamoeba castellanii is protected from the effects of antimicrobials. Antimicrob Agents Chemother 44: 1990-1994.
6. van Ingen J, Boeree MJ, van Soolingen D, Iseman MD, Heifets LB, et al. (2012) Are phylogenetic position, virulence, drug susceptibility and in vivo response to treatment in mycobacteria interrelated? Infect Genet Evol 12: 832-837.
7. Fyfe JAM, Lavender CJ, Handasyde KA, Legione AR, O'Brien CR, et al. (2010) A major role for mammals in the ecology of Mycobacterium ulcerans. PloS Negl Trop Dis 4: e791.
8. Portaels F, Chemlal K, Elsen P, Johnson PD, Hayman JA, et al. (2001) Mycobacterium ulcerans in wild animals. Rev Sci Tech OIE 20: 252-264.
9. Marsollier L, Aubry J, Coutanceau E, André J-PS, Small PL, et al. (2005) Colonization of the salivary glands of Naucoris cimicoides by Mycobacterium ulcerans requires host plasmatocytes and a macrolide toxin, mycolactone. Cell Microbiol 7: 935-943.
10. Marsollier L, Robert R, Aubry J, Andre J-S, Kouakou H, et al. (2002) Aquatic insects as a vector for Mycobacterium ulcerans. Appl Environ Microbiol 68: 4623-4628.
11. Marsollier L, André J-PS, Frigui W, Reysset G, Milon G, et al. (2007) Early trafficking events of Mycobacterium ulcerans within Naucoris cimicoides. Cell Microbiol 9: 347-355.
12. Mosi L, Williamson H, Wallace JR, Merritt RW, Small PLC, (2008) Persistent association of Mycobacterium ulcerans with West African predaceous insects of the family Belostomatidae. Appl Environ Microbiol 74: 7036-7042.
13. Benbow ME, Williamson H, Kimbirauskas R, Mcintosh MD, Kolar R, et al. (2008) Aquatic invertebrates as unlikely vectors of Buruli Ulcer disease. Emerging Infect Dis 14: 1247-1254.
14. Marion E, Eyangoh S, Yeramian E, Doannio J, Landier J, et al. (2010) Seasonal and regional dynamics of M. ulcerans transmission in environmental context: deciphering the role of water bugs as hosts and vectors. PloS Negl Trop Dis 4: e731.
15. Portaels F, Meyers WM, Ablordey A, Castro AG, Chemlal K, et al. (2008) First cultivation and characterization of Mycobacterium ulcerans from the environment. PloS Negl Trop Dis 2: e178.
16. Eddyani M, De Jonckheere JF, Durnez L, Suykerbuyk P, Leirs H, et al. (2008) Occurrence of free-living amoebae in communities of low and high endemicity for Buruli ulcer in southern Benin. Appl Environ Microbiol 74: 6547-6553.
17. Wilson MD, Boakye DA, Mosi L, Asiedu K, (2011) In the case of transmission of Mycobacterium ulcerans in Buruli ulcer disease Acanthamoeba species stand accused. Ghana Medical Journal 45: 1-4.
18. Marsollier L, Stinear T, Aubry J, Paul J, Andre S, et al. (2004) Aquatic plants stimulate the growth of and biofilm formation by Mycobacterium ulcerans in axenic culture and harbor these bacteria in the environment. Appl Environ Microbiol 70: 1097-1103.
19. Greub G, Raoult D, (2004) Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 17: 413-433.
20. Adékambi T, Ben Salah S, Khlif M, Raoult D, Drancourt M, (2006) Survival of environmental mycobacteria in Acanthamoeba polyphaga. Appl Environ Microbiol 72: 5974-5981.
21. Strahl ED, Gillaspy GE, Falkinham JO, (2001) Fluorescent acid-fast microscopy for measuring phagocytosis of Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrofulaceum by Tetrahymena pyriformi and their intracellular growth. Appl Environ Microbiol 67: 4432-4439.
22. Stuart AE, (1977) Phagocytic engulfment and cell adhesiveness as cellular surface phenomena. J Clin Pathol 30: 592.
23. Cosma CL, Sherman DR, Ramakrishnan L, (2003) The secret lives of the pathogenic mycobacteria. Annu Rev Microbiol 57: 641-676.
24. Thomas V, Bouchez T, Nicolas V, Robert S, Loret JF, et al. (2004) Amoebae in domestic water systems: resistance to disinfection treatments and implication in Legionella persistence. J Appl Microbiol 97: 950-963.
25. Thomas V, McDonnell G, (2007) Relationship between mycobacteria and amoebae: ecological and epidemiological concerns. Lett Appl Microbiol 45: 349-357.
26. Salah IB, Ghigo E, Drancourt M, (2009) Free-living amoebae, a training field for macrophage resistance of mycobacteria. European Society of Clinical Microbiology and Infectious Diseases 15: 894-905.
27. Cianciotto NP, Fields BS, (1992) Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc Natl Acad Sci USA 89: 5188-5191.
28. Cirillo JD, Cirillo SL, Yan L, Bermudez LE, Falkow S, et al. (1999) Intracellular growth in Acanthamoeba castellanii affects monocyte entry mechanisms and enhances virulence of Legionella pneumophila. Infect Immun 67: 4427-4434.
29. Cirillo JD, Falkow S, Tompkins LS, Bermudez LE, (1997) Interaction of Mycobacterium avium with environmental amoebae enhances virulence. Infect Immun 65: 3759-3767.
30. Silva MT, Portaels F, Pedrosa J, (2009) Pathogenetic mechanisms of the intracellular parasite Mycobacterium ulcerans leading to Buruli ulcer. Lancet Infect Dis 9: 699-710.
31. Krishna-Prasad BN, Gupta SK, (1978) Preliminary report on the engulfment and retention of mycobacteria by trophozoites of exenically grown Acanthamoeba castellanii Douglas, 1930. Curr Sci 47: 245-247.
32. Silva MT, (1990) Pitfalls in the ultrastructural analysis of mycobacteria, including Mycobacterium leprae. Trop Med Parasitol 41: 339-340.
33. Boom R, Sol CJ, Salimans MM, Jansen CL, Wertheim-van Dillen PM, et al. (1990) Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28: 495-503.
34. Durnez L, Stragier P, Roebben K, Ablordey A, Leirs H, et al. (2009) A comparison of DNA extraction procedures for the detection of Mycobacterium ulcerans, the causative agent of Buruli ulcer, in clinical and environmental specimens. J Microbiol Methods 76: 152-158.
35. Menashe O, Kaganskaya E, Baasov T, Yaron S, (2008) Aminoglycosides affect intracellular Salmonella enterica serovars typhimurium and virchow. Antimicrob Agents Chemother 52: 920-926.
36. Portaels F, De Muynck A, Sylla MP, (1988) Selective isolation of mycobacteria from soil: a statistical analysis approach. J Gen Microbiol 134: 849-855.
37. Portaels F, Fonteyene PA, de Beenhouwer H, de Rijk P, Guédénon A, et al. (1996) Variability in 3′ end of 16S rRNA sequence of Mycobacterium ulcerans is related to geographic origin of isolates. J Clin Microbiol 34: 962-965.
38. Page FC, (1976) An illustrated key to freshwater and soil amoebae. Ambleside, UK: Freshwater Biological Association.
39. De Jonckheere JF, Brown S, (2005) The identification of vahlkampfiid amoebae by ITS sequencing. Protist 156: 89-96.
40. De Jonckheere JF, (1998) Sequence variation in the ribosomal internal transcribed spacers, including the 5.8S rDNA, of Naegleria spp. Protist 149: 221-228.
41. Schroeder JM, Booton GC, Hay J, Niszl IA, Seal DV, et al. (2001) Use of subgenic 18S ribosomal DNA PCR and sequencing for genus and genotype identification of Acanthamoebae from humans with keratitis and from sewage sludge. J Clin Microbiol 39: 1903-1911.
42. Löytynoja A, Goldman N, (2005) An algorithm for progressive multiple alignment of sequences with insertions. Proc Natl Acad Sci USA 102: 10557-10562.
43. Yip MJ, Porter JL, Fyfe JaM, Lavender CJ, Portaels F, et al. (2007) Evolution of Mycobacterium ulcerans and other mycolactone-producing mycobacteria from a common Mycobacterium marinum progenitor. J Bacteriol 189: 2021-2029.
44. Fyfe JAM, Lavender CJ, Johnson PDR, Globan M, Sievers A, et al. (2007) Development and application of two multiplex real-time PCR assays for the detection of Mycobacterium ulcerans in clinical and environmental samples. Appl Environ Microbiol 73: 4733-4740.
45. R Development Core Team (2009) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, Vienna, Austria.
46. Lunn DJ, Thomas A, Best N, Spiegelhalter D, (2000) WinBUGS - A Bayesian modelling framework: Concepts, structure, and extensibility. St Com 10: 325-337.
47. Steinert M, Birkness K, White E, Fields B, Quinn F, (1998) Mycobacterium avium bacilli grow saprozoically in coculture with Acanthamoeba polyphaga and survive within cyst walls. Appl Environ Microbiol 64: 2256-2261.
48. Silva MT, Macedo PM, (1984) Ultrastructural characterization of normal and damaged membranes of Mycobacterium leprae and of cultivable mycobacteria. J Gen Microbiol 130: 369-380.
49. Draper P, Rees RJW, (1970) Electron-transparent zone of mycobacteria may be a defence mechanism. Nature 228: 860-&.
50. Astarie-Dequeker C, N'Diaye EN, Le Cabec V, Rittig MG, Prandi J, et al. (1999) The mannose receptor mediates uptake of pathogenic and nonpathogenic mycobacteria and bypasses bactericidal responses in human macrophages. Infect Immun 67: 469-477.
51. Torrado E, Fraga AG, Castro AG, Stragier P, Meyers WM, et al. (2007) Evidence for an intramacrophage growth phase of Mycobacterium ulcerans. Infect Immun 75: 977-987.
52. Gao LY, Guo S, McLaughlin B, Morisaki H, Engel JN, et al. (2004) A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 53: 1677-1693.
53. Grosset J, (2003) Mycobacterium tuberculosis in the extracellular compartment: an underestimated adversary. Antimicrob Agents Chemother 47: 833-836.
54. Cloud JL, Meyer JJ, Pounder JI, Jost KC, Sweeney A, et al. (2006) Mycobacterium arupense sp. nov., a non-chromogenic bacterium isolated from clinical specimens. Int J Syst Evol Microbiol 56: 1413-1418.
55. Schinsky MF, McNeil MM, Whitney AM, Steigerwalt AG, Lasker BA, et al. (2000) Mycobacterium septicum sp. nov., a new rapidly growing species associated with catheter-related bacteraemia. Int J Syst Evol Microbiol 50 Pt 2: 575-581.
56. Wallace RJJ, Brown-Elliott BA, Wilson RW, Mann L, Hall L, et al. (2004) Clinical and Laboratory Features of Mycobacterium porcinum. J Clin Microbiol 42: 5689-5697.
57. Portaels F, (1995) Epidemiology of mycobacterial diseases. In: Mycobacterial diseases of the skin Clinics in Dermatology. Schuster M, editor. New York: Elsevier Sciences. pp. 207-222.
58. Bermudez L, Petrofsky M, Goodman J, (1997) Exposure to low oxygen tension and increased osmolarity enhance the ability of Mycobacterium avium to enter intestinal epithelial (HT-29) cells. Infect Immun 65: 3768-3773.
59. Singh RD, Khullar M, Ganguly NK, (2000) Role of anaerobiosis in virulence of Salmonella typhimuirium. Mol Cell Biochem 215: 39-46-46.
60. Eddyani M, Debacker M, Martin A, Aguiar J, Johnson CR, et al. (2008) Primary culture of Mycobacterium ulcerans from human tissue specimens after storage in semisolid transport medium. J Clin Microbiol 46: 69-72.
61. La Scola B, Mezi L, Weiller PJ, Raoult D, (2001) Isolation of Legionella anisa using an amoebic coculture procedure. J Clin Microbiol 39: 365-366.
62. Pagnier I, Raoult D, La Scola B, (2008) Isolation and identification of amoeba-resisting bacteria from water in human environment by using an Acanthamoeba polyphaga co-culture procedure. Environ Microbiol 10: 1135-1144.
63. Vandelannoote K, Durnez L, Amissah D, Gryseels S, Dodoo A, et al. (2010) Application of real-time PCR in Ghana, a Buruli ulcer-endemic country, confirms the presence of Mycobacterium ulcerans in the environment. FEMS Microbiol Lett 304: 191-194.