Loss of mobile genomic islands in metal resistant, hydrogen-oxidizing Cupriavidus metallidurans

Abstract

The genome of the metal resistant, hydrogen-oxidizing bacterium Cupriavidus metallidurans strain CH34 contains horizontally acquired plasmids and genomic islands. Metal-resistance determinants on the two plasmids may exert genetic dominance over other related determinants. To investigate whether these recessive determinants can be activated in the absence of the dominant ones, the transcriptome of the highly zinc-sensitive deletion mutant Δe4 (Δ cadA ΔzntA ΔdmeF ΔfieF ) of the plasmid-free parent AE104 was characterized using gene arrays. As a consequence of some unexpected results, close examination by PCR and genomic re-resequencing of strains CH34, AE104, Δe4 and others revealed that the genomic islands CMGIs 2, 3, 4, D, E, but no other islands or recessive determinants, were deleted in some of these strains. Provided CH34 wild type was kept under alternating zinc and nickel selection pressure, no comparable deletions occurred. All current data suggest that genes were actually deleted and were not, as previously surmised, simply absent from the respective strain. As a consequence, a cured database was compiled from the newly generated and previously published gene array data. Analysis of data from this database indicated that some genes of recessive, no longer needed determinants were nevertheless expressed and up-regulated. Their products may interact with those of the dominant determinants to mediate a mosaic phenotype. The ability to contribute to such a mosaic phenotype may prevent deletion of the recessive determinant. The data suggest that the bacterium actively modifies its genome to deal with metal stress and the same time ensures metal homeostasis. Significance In their natural environment, bacteria continually acquire genes by horizontal gene transfer and newly acquired determinants may become dominant over related ones already present in the host genome. When a bacterium is taken into laboratory culture, it is isolated from the horizontal gene transfer network. It can no longer gain genes, but instead may lose them. This was indeed observed in Cupriavidus metallidurans for loss key metal-resistance determinants when no selection pressure was continuously kept. However, some recessive metal-resistance determinants were maintained in the genome. It is proposed that they might contribute some accessory genes to related dominant resistance determinants, for instance periplasmic metal-binding proteins or two-component regulatory systems. Alternatively, they may only remain in the genome because their DNA serves as a scaffold for the nucleoid. Using C. metallidurans as an example, this study sheds light on the fate and function of horizontally acquired genes in bacteria.