Comparison of the complete genome sequences of four γ-hexachlorocyclohexane-degrading bacterial strains: insights into the evolution of bacteria able to degrade a recalcitrant man-made pesticide

Abstract

γ-Hexachlorocyclohexane (γ-HCH) is a recalcitrant man-made chlorinated pesticide. Here, the complete genome sequences of four γ-HCH-degrading sphingomonad strains, which are most unlikely to have been derived from one ancestral γ-HCH degrader, were compared. Together with several experimental data, we showed that (i) all the four strains carry almost identical linA to linE genes for the conversion of γ-HCH to maleylacetate (designated “specific” lin genes), (ii) considerably different genes are used for the metabolism of maleylacetate in one of the four strains, and (iii) the linKLMN genes for the putative ABC transporter necessary for γ-HCH utilization exhibit structural divergence, which reflects the phylogenetic relationship of their hosts. Replicon organization and location of the lin genes in the four genomes are significantly different with one another, and that most of the specific lin genes are located on multiple sphingomonad-unique plasmids. Copies of IS6100, the most abundant insertion sequence in the four strains, are often located in close proximity to the specific lin genes. Analysis of the footprints of target duplication upon IS6100 transposition and the experimental detection of IS6100 transposition strongly suggested that the IS6100 transposition has caused dynamic genome rearrangements and the diversification of lin-flanking regions in the four strains.

How enzyme promiscuity and horizontal gene transfer contribute to metabolic innovation

“…The PCP degradation pathway from S. chlorophenolicum and γ‐HCH degradation pathway from S. japonicum UT26 converge at β‐ketoadipate . PCP and γ‐HCH are metabolized to β‐ketoadipate (cyan box), a common intermediate in aromatic compound degradation.…”

“…However, PcpC and LinD share < 25% identity and did not diverge from a recent common ancestor . Like PCP degradation genes, γ‐HCH degradation genes were acquired by HGT, and most are associated with mobile genetic elements . The distribution of lin genes among γ‐HCH‐degrading species is complicated.…”

“…The distribution of lin genes among γ‐HCH‐degrading species is complicated. Higher conservation of lin genes relative to the rest of the genome supports the independent HGT of some genes or the whole pathway to each strain . Some strains do not possess all genes in the γ‐HCH degradation pathway, but whether this is due to gene loss (possibly during strain propagation), catalysis of missing steps by other enzymes, or complementation of missing steps by other strains in a microbial community is unknown .…”

“…Together, the evolution of the PCP and γ‐HCH degradation pathways demonstrates the role of HGT in patching together new pathways and integration of enzymes derived from HGT into central metabolism. However, low sequence similarity to enzymes with known functions has prevented identification of the ancestral functions of most PCP and γ‐HCH‐degrading enzymes, making it difficult trace the coevolution of structure and function of enzymes in these pathways .…”

Expression of an alcohol dehydrogenase gene in a heterotrophic bacterium induces carbon dioxide-dependent high-yield growth under oligotrophic conditions

“…Identical or almost identical adhX orthologues were found in other sphingomonad strains, and most of them were located on plasmids (Table S2), suggesting that the adhX-dependent HYGO phenotype is one of the important adaptation strategies to oligotrophic environments among sphingomonads. Sphingomonas-related strains (sphingomonads) are one of the most important bacterial groups for the degradation of recalcitrant hydrophobic compounds [36][37][38][39][40][41][42][43]. Growth under oligotrophic conditions seems to be beneficial for the evolutionary acquisition of new metabolic functions.…”