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EsxA (ESAT-6) and EsxB (CFP-10) are virulence factors exported by the ESX-1 system in mycobacterial pathogens. InMycobacterium marinum , an established model for ESX-1 secretion inMycobacterium tuberculosis , genes required for ESX-1 export reside at the extended region of difference 1 (RD1) locus. In this study, a novel locus required for ESX-1 export inM. marinum was identified outside the RD1 locus. AnM. marinum strain bearing a transposon-insertion between theMMAR _1663 andMMAR _1664 genes exhibited smooth-colony morphology, was deficient for ESX-1 export, was nonhemolytic, and was attenuated for virulence. Genetic complementation revealed a restoration of colony morphology and a partial restoration of virulence in cell culture models. Yet hemolysis and the export of ESX-1 substrates into the bacteriological mediumin vitro as measured by both immunoblotting and quantitative proteomics were not restored. We show that genetic complementation of the transposon insertion strain partially restored the translocation of EsxA and EsxB to the mycobacterial cell surface. Our findings indicate that the export of EsxA and EsxB to the cell surface, rather than secretion into the bacteriological medium, correlates with virulence inM. marinum . Together, these findings not only expand the known genetic loci required for ESX-1 secretion inM. marinum but also provide an explanation for the observed disparity betweenin vitro ESX-1 export and virulence.

A Novel ESX-1 Locus Reveals that Surface-Associated ESX-1 Substrates Mediate Virulence in Mycobacterium marinum