Potential Role for Fish in Transmission of
            <i>Mycobacterium ulcerans</i>
            Disease (Buruli Ulcer): an Environmental Study

Eddyani, Miriam; Ofori‐Adjei, David; Teugels, Guy G.; Weirdt, David De; Boakye, Daniel; Meyers, Wayne M.; Portaels, Françoise

doi:10.1128/aem.70.9.5679-5681.2004

Cited by 92 publications

(70 citation statements)

References 11 publications

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“…MIRU loci might be hot spots for transcriptional errors, leading to a faster adaptation to environmental changes than that caused by random mutations. M. ulcerans is well adapted to a variety of natural reservoirs, such as aquatic insects (21,29) and other aquatic organisms such as fish or snails (8,28). This might be due to the protective mininiche that is created by mycolactone (22).…”

Section: Discussionmentioning

confidence: 99%

GenotypingMycobacterium ulceransandMycobacterium marinumby Using Mycobacterial Interspersed Repetitive Units

et al. 2005

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A novel category of variable tandem repeats (VNTR) called mycobacterial interspersed repetitive units (MIRUs) has been identified for Mycobacterium ulcerans (n ‫؍‬ 39), M. marinum (n ‫؍‬ 27), and one related organism. Fifteen MIRU loci were identified in the genome of M. marinum and were used to genotype M. ulcerans, M. marinum, and an M. marinum-like organism that is considered a possible missing link between M. marinum and M. ulcerans. Seven MIRU loci were polymorphic, and locus-specific PCRs for four of these loci differentiated seven M. ulcerans genotypes, four M. marinum genotypes, and a unique genotype for the missing link organism. The seven M. ulcerans genotypes were related to six different geographic origins of isolates. All isolates from West and Central Africa, including old and recent isolates, belonged to the same genotype, emphasizing the great spatiotemporal homogeneity among African isolates. Unlike the M. ulcerans genotypes, the four M. marinum genotypes could not be clearly related to the geographic origins of the isolates. According to MIRU-VNTR typing, all M. ulcerans and M. marinum isolates of American origin were closely related, suggesting a common American ancestor for these two pathogenic species on the American continents. MIRU typing has significant potential value for discriminating between reoccurrence and reinfection for M. ulcerans disease.Mycobacterium ulcerans causes Buruli ulcer (BU), a disease that represents, after tuberculosis and leprosy, the third most common mycobacterial disease in humans (23,27). BU has been observed in many tropical areas, but most patients have come from Central and West Africa and Australia (5,11,27). Epidemiologically, the disease is associated with riverine and swampy terrains (27). BU is a devastating disease characterized by necrotizing, ulcerative lesions of subcutaneous tissues and the overlying skin. The main specific genomic characteristics of M. ulcerans are the IS2404 element (34) and a 174-kb plasmid(s) that houses the genes for mycolactone, a polyketide toxin (39). M. marinum causes infections in humans and in fish (7,31). Large outbreaks of infection due to M. marinum have been described in association with swimming pools (swimming pool granuloma) (42) and fish tanks (fish tank granuloma) (13,14,17,19). M. ulcerans and M. marinum, once cultured, are readily identified by conventional mycobacterial characterization methods (46). Various DNA-based techniques have been used to type mycobacteria (6,33,35). Such studies have demonstrated a close taxonomic relationship between M. ulcerans and M. marinum, although M. ulcerans harbors IS2404 and M. marinum does not (34). Recently, however, IS2404 was found in an unusual mycobacterial isolate with phenotypic properties closely related to those of M. marinum (4).Previous studies showed limited genotypic diversity in M. ulcerans, especially among isolates from a given geographic region. PCR-restriction profile analyses of 16S rRNAs showed four different genotypic profiles of M. ulcerans, i.e., the ...

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Section: Discussionmentioning

confidence: 99%

GenotypingMycobacterium ulceransandMycobacterium marinumby Using Mycobacterial Interspersed Repetitive Units

et al. 2005

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“…Those studies have relied solely on detection of IS2404 as evidence for M. ulcerans, based on a report showing that IS2404 was absent from 48 species of mycobacteria obtained from a laboratory collection (27). IS2404 PCR has been used to demonstrate the presence of M. ulcerans DNA in fish (10), frogs, many species of insects, snails, and a large range of aquatic samples from Africa (19,22 (31,35). In the past few years investigators have suggested that M. marinum isolates from humans are genetically different than isolates from poikilothermic species.…”

Section: Discussionmentioning

confidence: 99%

Globally Distributed Mycobacterial Fish Pathogens Produce a Novel Plasmid-Encoded Toxic Macrolide, Mycolactone F

et al. 2006

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Mycobacterium ulcerans and Mycobacterium marinum are closely related pathogens which share an aquatic environment. The pathogenesis of these organisms in humans is limited by their inability to grow above 35°C. M. marinum causes systemic disease in fish but produces localized skin infections in humans. M. ulcerans causes Buruli ulcer, a severe human skin lesion. At the molecular level, M. ulcerans is distinguished from M. marinum by the presence of a virulence plasmid which encodes a macrolide toxin, mycolactone, as well as by hundreds of insertion sequences, particularly IS2404. There has been a global increase in reports of fish mycobacteriosis. An unusual clade of M. marinum has been reported from fish in the Red and Mediterranean Seas and a new mycobacterial species, Mycobacterium pseudoshottsii, has been cultured from fish in the Chesapeake Bay, United States. We have discovered that both groups of fish pathogens produce a unique mycolactone toxin, mycolactone F. Mycolactone F is the smallest mycolactone (molecular weight, 700) yet identified. The core lactone structure of mycolactone F is identical to that of M. ulcerans mycolactones, but a unique side chain structure is present. Mycolactone F produces apoptosis and necrosis on cultured cells but is less potent than M. ulcerans mycolactones. Both groups of fish pathogens contain IS2404. In contrast to M. ulcerans and conventional M. marinum, mycolactone F-producing mycobacteria are incapable of growth at above 30°C. This fact is likely to limit their virulence for humans. However, such isolates may provide a reservoir for horizontal transfer of the mycolactone plasmid in aquatic environments.Mycobacterium marinum is a globally distributed pathogen of marine and freshwater fish which also causes skin infections in humans (7, 9). M. marinum is phenotypically distinguished from other mycobacteria by its low optimal growth temperature, light-induced carotenoid production, and relatively rapid growth rate compared to other slow-growing Mycobacterium species. There is considerable heterogeneity among M. marinum isolates, and several subgroups have been described (28,(33)(34)(35).Mycobacteriosis was first diagnosed in fish from the Red Sea in 1990 (5). The infection was initially found in cultured sea bass (Dicentrarchus labrax) in Eilat and has since been found in over 20 different fish species and a hawksbill sea turtle. The Red Sea isolates differed phenotypically from other M. marinum strains by being scotochromogenic (having constitutive pigment production). Whereas most M. marinum strains form colonies on mycobacterial media within 8 days, initial growth was not obtained from these isolates for at least 2 weeks. Similar isolates have also been found in the Mediterranean Sea in Greece and Italy. Molecular characterization of the Israeli isolates from fish confirmed their identity as M. marinum, but analysis of the 16S rRNA gene showed that the isolates formed clades within the species (33, 34). Molecular comparison of the fish isolates with human isolates of...

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“…There is a strong association between the occurrence of M. ulcerans infection in humans and slow-flowing or stagnant water bodies (Marsollier et al, 2007;Portaels et al, 1999;Roberts & Hirst, 1997;Ross et al, 1997;Stinear et al, 2000a). Aquatic snails (Marsollier et al, 2004), fish (Eddyani et al, 2004) and water bugs (Marsollier et al, 2002) are currently being discussed as passive and active hosts, respectively. However, the exact mode of transmission of Buruli ulcer has remained a mystery, partly because no genetic fingerprinting tool is available for micro-epidemiological analysis of infection chains.…”

Section: Introductionmentioning

confidence: 99%

Analysis of the Mycobacterium ulcerans genome sequence reveals new loci for variable number tandem repeats (VNTR) typing

et al. 2007

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Screening of the genome sequence of the Mycobacterium ulcerans strain Agy99 from Ghana with tandem repeats finder software revealed 34 novel non-degenerate tandem repeats containing loci suitable for variable number tandem repeats (VNTR) typing. All loci revealed polymorphism within M. ulcerans isolates of geographically diverse origins. The results confirm the evolutionary scenario suggested by multi-locus sequence typing in which a progenitor of all M. ulcerans lineages emerged from the environmental species Mycobacterium marinum and subsequently diverged into several geographical lineages. For further attempts to develop a VNTR-based genetic fingerprinting tool for M. ulcerans, it is suggested that the focus should rather be on M. marinum than on the African M. ulcerans Agy99 genome sequence as a starting point.

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Potential Role for Fish in Transmission of Mycobacterium ulcerans Disease (Buruli Ulcer): an Environmental Study

Cited by 92 publications

References 11 publications

GenotypingMycobacterium ulceransandMycobacterium marinumby Using Mycobacterial Interspersed Repetitive Units

GenotypingMycobacterium ulceransandMycobacterium marinumby Using Mycobacterial Interspersed Repetitive Units

Globally Distributed Mycobacterial Fish Pathogens Produce a Novel Plasmid-Encoded Toxic Macrolide, Mycolactone F

Analysis of the Mycobacterium ulcerans genome sequence reveals new loci for variable number tandem repeats (VNTR) typing

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