Amoebae as potential environmental hosts for Mycobacterium ulcerans and other mycobacteria, but doubtful actors in Buruli ulcer epidemiology

PLoS Negl Trop Dis. 2012;6(8):e1764. doi: 10.1371/journal.pntd.0001764. Epub 2012 Aug 7.

Abstract

Background: The reservoir and mode of transmission of Mycobacterium ulcerans, the causative agent of Buruli ulcer, remain unknown. Ecological, genetic and epidemiological information nonetheless suggests that M. ulcerans may reside in aquatic protozoa.

Methodology/principal findings: We experimentally infected Acanthamoeba polyphaga with M. ulcerans and found that the bacilli were phagocytised, not digested and remained viable for the duration of the experiment. Furthermore, we collected 13 water, 90 biofilm and 45 detritus samples in both Buruli ulcer endemic and non-endemic communities in Ghana, from which we cultivated amoeboid protozoa and mycobacteria. M. ulcerans was not isolated, but other mycobacteria were as frequently isolated from intracellular as from extracellular sources, suggesting that they commonly infect amoebae in nature. We screened the samples as well as the amoeba cultures for the M. ulcerans markers IS2404, IS2606 and KR-B. IS2404 was detected in 2% of the environmental samples and in 4% of the amoeba cultures. The IS2404 positive amoeba cultures included up to 5 different protozoan species, and originated both from Buruli ulcer endemic and non-endemic communities.

Conclusions/significance: This is the first report of experimental infection of amoebae with M. ulcerans and of the detection of the marker IS2404 in amoeba cultures isolated from the environment. We conclude that amoeba are potential natural hosts for M. ulcerans, yet remain sceptical about their implication in the transmission of M. ulcerans to humans and their importance in the epidemiology of Buruli ulcer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amoeba / microbiology*
  • Buruli Ulcer / epidemiology*
  • Buruli Ulcer / microbiology*
  • Buruli Ulcer / transmission
  • DNA Transposable Elements
  • DNA, Bacterial / chemistry
  • DNA, Bacterial / genetics
  • Disease Reservoirs*
  • Environmental Microbiology
  • Ghana
  • Humans
  • Microbial Viability
  • Molecular Sequence Data
  • Mycobacterium / isolation & purification*
  • Phagocytosis
  • Sequence Analysis, DNA

Substances

  • DNA Transposable Elements
  • DNA, Bacterial

Associated data

  • GENBANK/JX119197
  • GENBANK/JX119198
  • GENBANK/JX119199
  • GENBANK/JX119200
  • GENBANK/JX119201
  • GENBANK/JX119202
  • GENBANK/JX119203
  • GENBANK/JX119204
  • GENBANK/JX119205
  • GENBANK/JX119206
  • GENBANK/JX119207
  • GENBANK/JX119208
  • GENBANK/JX119209
  • GENBANK/JX119210

Grants and funding

This study was supported by the Flemish Interuniversity Council – University Development Cooperation (VLIR-UOS) and by the Stop Buruli Initiative funded by the UBS Optimus Foundation (Zurich, Switzerland). S. Gryseels is currently an FWO PhD fellow (FWO grant nr 1.1.671.10.N.00). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.