Comparative genomic analysis of nine Sphingobium strains: Insights into their evolution and hexachlorocyclohexane (HCH) degradation pathways

Verma, Helianthous; Kumar, Roshan; Oldach, Phoebe; Sangwan, Naseer; Khurana, Jitendra P.; Gilbert, Jack A.; Lal, Rup

doi:10.1186/1471-2164-15-1014

Title: Comparative genomic analysis of nine Sphingobium strains: Insights into their evolution and hexachlorocyclohexane (HCH) degradation pathways

Journal Article · Sun Nov 23 00:00:00 EST 2014 · BMC Genomics

DOI:https://doi.org/10.1186/1471-2164-15-1014· OSTI ID:1223126

Verma, Helianthous ^[1]; Kumar, Roshan ^[1]; Oldach, Phoebe ^[1]; Sangwan, Naseer ^[1]; Khurana, Jitendra P. ^[2]; Gilbert, Jack A. ^[3]; Lal, Rup ^[1]

Univ. of Delhi, Delhi (India)
Univ. of Delhi, South Campus, New Delhi (India)
Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Chicago, Chicago, IL (United States)

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. In addition, 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. In 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.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1223126

Journal Information:: BMC Genomics, Vol. 15, Issue 1; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 57 works

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Data from: Comparative genomic analysis of nine Sphingobium strains: insights into their evolution and Hexachlorocyclohexane (HCH) degradation pathways Verma, Helianthous; Kumar, Roshan; Oldach, Phoebe Dryad-Supplementary information for journal article at DOI: 10.1186/1471-2164-15-1014, 11 files https://doi.org/10.5061/dryad.t4624	dataset	December 2014
Revealing large metagenomic regions through long DNA fragment hybridization capture Gasc, Cyrielle; Peyret, Pierre Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0251-0	journal	March 2017
Perspectives of lindane (γ-hexachlorocyclohexane) biodegradation from the environment: a review Kumar, Dharmender; Pannu, Rochika Bioresources and Bioprocessing, Vol. 5, Issue 1 https://doi.org/10.1186/s40643-018-0213-9	journal	June 2018
Hydrolase CehA and Monooxygenase CfdC Are Responsible for Carbofuran Degradation in Sphingomonas sp. Strain CDS-1 Yan, Xin; Jin, Wen; Wu, Guang Applied and Environmental Microbiology, Vol. 84, Issue 16 https://doi.org/10.1128/aem.00805-18	journal	June 2018
Evolution of Sphingomonad Gene Clusters Related to Pesticide Catabolism Revealed by Genome Sequence and Mobilomics of Sphingobium herbicidovorans MH Nielsen, Tue Kjærgaard; Rasmussen, Morten; Demanèche, Sandrine Genome Biology and Evolution, Vol. 9, Issue 9 https://doi.org/10.1093/gbe/evx185	journal	September 2017
Draft Genome Sequence of the Plant Growth-Promoting Sphingobium sp. Strain AEW4, Isolated from the Rhizosphere of the Beachgrass Ammophila breviligulata Wanees, Abanoub E.; Zaslow, Shari J.; Potter, Savannah J. Genome Announcements, Vol. 6, Issue 21 https://doi.org/10.1128/genomea.00410-18	journal	May 2018
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 Tabata, Michiro; Ohhata, Satoshi; Nikawadori, Yuki DNA Research, Vol. 23, Issue 6 https://doi.org/10.1093/dnares/dsw041	journal	August 2016
Evolutionary Genomics of an Ancient Prophage of the Order Sphingomonadales Viswanathan, Vandana; Narjala, Anushree; Ravichandran, Aravind Genome Biology and Evolution, Vol. 9, Issue 3 https://doi.org/10.1093/gbe/evx024	journal	March 2017
Genome Organization of Sphingobium indicum B90A: An Archetypal Hexachlorocyclohexane (HCH) Degrading Genotype Verma, Helianthous; Bajaj, Abhay; Kumar, Roshan Genome Biology and Evolution, Vol. 9, Issue 9 https://doi.org/10.1093/gbe/evx133	journal	July 2017
Draft Genome Sequence of Sphingobium yanoikuyae TJ, a Halotolerant Di- n -Butyl-Phthalate-Degrading Bacterium Jin, Decai; Zhu, Ying; Wang, Xinxin Genome Announcements, Vol. 4, Issue 3 https://doi.org/10.1128/genomea.00569-16	journal	June 2016
Adaptive Evolution of Sphingobium hydrophobicum C1T in Electronic Waste Contaminated River Sediment Song, Da; Chen, Xingjuan; Xu, Meiying Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02263	journal	October 2019
Metagenomic Analysis of a Complex Community Present in Pond Sediment Negi, Vivek; Lal, Rup Journal of Genomics, Vol. 5 https://doi.org/10.7150/jgen.16685	journal	January 2017

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Hexachlorocyclohexane (HCH)
Sphingobium
lin genes
Xenobiotic compounds