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Insights into Ongoing Evolution of the Hexachlorocyclohexane Catabolic Pathway from Comparative Genomics of Ten Sphingomonadaceae Strains.

ABSTRACT: Hexachlorocyclohexane (HCH), a synthetic organochloride, was first used as a broad-acre insecticide in the 1940s, and many HCH-degrading bacterial strains have been isolated from around the globe during the last 20 years. To date, the same degradation pathway (the lin pathway) has been implicated in all strains characterized, although the pathway has only been characterized intensively in two strains and for only a single HCH isomer. To further elucidate the evolution of the lin pathway, we have biochemically and genetically characterized three HCH-degrading strains from the Czech Republic and compared the genomes of these and seven other HCH-degrading bacterial strains. The three new strains each yielded a distinct set of metabolites during their degradation of HCH isomers. Variable assembly of the pathway is a common feature across the 10 genomes, eight of which (including all three Czech strains) were either missing key lin genes or containing duplicate copies of upstream lin genes (linA-F). The analysis also confirmed the important role of horizontal transfer mediated by insertion sequence IS6100 in the acquisition of the pathway, with a stronger association of IS6100 to the lin genes in the new strains. In one strain, a linA variant was identified that likely caused a novel degradation phenotype involving a shift in isomer preference. This study identifies a number of strains that are in the early stages of lin pathway acquisition and shows that the state of the pathway can explain the degradation patterns observed.

SUBMITTER: Pearce SL

PROVIDER: S-EPMC4478539 | biostudies-literature | 2015 Jun

REPOSITORIES: biostudies-literature

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Insights into Ongoing Evolution of the Hexachlorocyclohexane Catabolic Pathway from Comparative Genomics of Ten Sphingomonadaceae Strains.

Pearce Stephen L SL Oakeshott John G JG Pandey Gunjan G

G3 (Bethesda, Md.) 20150407 6

Hexachlorocyclohexane (HCH), a synthetic organochloride, was first used as a broad-acre insecticide in the 1940s, and many HCH-degrading bacterial strains have been isolated from around the globe during the last 20 years. To date, the same degradation pathway (the lin pathway) has been implicated in all strains characterized, although the pathway has only been characterized intensively in two strains and for only a single HCH isomer. To further elucidate the evolution of the lin pathway, we have ...[more]

PMID: 25850427

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Project description:BACKGROUND: Sphingobium spp. are efficient degraders of a wide range of chlorinated and aromatic hydrocarbons. In particular, strains which harbour the lin pathway genes mediating the degradation of hexachlorocyclohexane (HCH) isomers are of interest due to the widespread persistence of this contaminant. Here, we examined the evolution and diversification of the lin pathway under the selective pressure of HCH, by comparing the draft genomes of six newly-sequenced Sphingobium spp. (strains LL03, DS20, IP26, HDIPO4, P25 and RL3) isolated from HCH dumpsites, with three existing genomes (S. indicum B90A, S. japonicum UT26S and Sphingobium sp. SYK6). RESULTS: Efficient HCH degraders phylogenetically clustered in a closely related group comprising of UT26S, B90A, HDIPO4 and IP26, where HDIPO4 and IP26 were classified as subspecies with ANI value >98%. Less than 10% of the total gene content was shared among all nine strains, but among the eight HCH-associated strains, that is all except SYK6, the shared gene content jumped to nearly 25%. Genes associated with nitrogen stress response and two-component systems were found to be enriched. The strains also housed many xenobiotic degradation pathways other than HCH, despite the absence of these xenobiotics from isolation sources. Additionally, these strains, although non-motile, but posses flagellar assembly genes. While strains HDIPO4 and IP26 contained the complete set of lin genes, DS20 was entirely devoid of lin genes (except linKLMN) whereas, LL03, P25 and RL3 were identified as lin deficient strains, as they housed incomplete lin pathways. Further, in HDIPO4, linA was found as a hybrid of two natural variants i.e., linA1 and linA2 known for their different enantioselectivity. CONCLUSION: The bacteria isolated from HCH dumpsites provide a natural testing ground to study variations in the lin system and their effects on degradation efficacy. Further, the diversity in the lin gene sequences and copy number, their arrangement with respect to IS6100 and evidence for potential plasmid content elucidate possible evolutionary acquisition mechanisms for this pathway. This study further opens the horizon for selection of bacterial strains for inclusion in an HCH bioremediation consortium and suggests that HDIPO4, IP26 and B90A would be appropriate candidates for inclusion.

Dataset Information

Insights into Ongoing Evolution of the Hexachlorocyclohexane Catabolic Pathway from Comparative Genomics of Ten Sphingomonadaceae Strains.

Publications

Insights into Ongoing Evolution of the Hexachlorocyclohexane Catabolic Pathway from Comparative Genomics of Ten Sphingomonadaceae Strains.

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