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JB Accepts, published online ahead of print on 15 December 2006
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J. Bacteriol. doi:10.1128/JB.01442-06
Copyright (c) 2006, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

Evolution of Mycobacterium ulcerans and other mycolactone-producing mycobacteria from a common Mycobacterium marinum progenitor

Marcus J. Yip, Jessica L. Porter, Janet A. M. Fyfe, Caroline J. Lavender, Françoise Portaels, Martha Rhodes, Howard Kator, Angelo Colorni, Grant A. Jenkin, and Tim Stinear*

Department of Microbiology, Monash University, Wellington Rd, Clayton 3800, Australia; Victorian Infectious Diseases Reference Laboratory, 10 Wreckyn St, North Melbourne 3051, Australia; Institute of Tropical Medicine, Antwerp 2000, Belgium; Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA 23062, USA; Israel Oceanographic and Limnological Research Ltd, National Centre for Mariculture, Eilat 88112, Israel

* To whom correspondence should be addressed. Email: tim.stinear{at}med.monash.edu.au.


  Abstract

It had been assumed that production of the cytotoxic polyketide, mycolactone, was strictly associated with Mycobacterium ulcerans, the causative agent of Buruli ulcer. However, a recent study has uncovered a broader distribution of mycolactone-producing mycobacteria (MPM) that includes mycobacteria cultured from diseased fish and frogs in the USA and from diseased fish in the Red and Mediterranean seas. All these mycobacteria contain versions of the M. ulcerans pMUM plasmid, produce mycolactones and show a high degree of genetic relatedness to both M. ulcerans and Mycobacterium marinum. Here we show by multiple genetic methods, including multilocus sequence analysis and DNA-DNA hybridisation, that all MPM have evolved from a common M. marinum progenitor to form a genetically cohesive group among a more diverse assemblage of M. marinum strains. Like M. ulcerans, the fish and frog MPM show multiple copies of the insertion sequence IS2404. Comparisons of pMUM and chromosomal gene sequences demonstrate that plasmid acquisition and the subsequent ability to produce mycolactone was probably the key driver of speciation. Ongoing evolution amongst MPM has since produced at least two genetically distinct ecotypes that can be broadly divided into those typically causing disease in ectotherms (but also having a high zoonotic potential) and those causing disease in endotherms such as humans.


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