Omics-centric evidences of fipronil biodegradation by Rhodococcus sp. FIP_B3

• Published in: Environmental pollution (1987) 2025-01, Vol.364 (Pt 1), p.125320, Article 125320
• Main Authors: Jaiswal, Anjali, Pandey, Anand Kumar, Tripathi, Animesh, Dubey, Suresh Kumar
• Format: Article
• Language: English
• Subjects: Biodegradation, Environmental; Insecticides - metabolism; Metabolites; Muti-omics; Pesticide; Pseudo-first-order kinetics; Pyrazoles - metabolism; Rhodococcus - genetics; Rhodococcus - metabolism; Soil Pollutants - metabolism; Soil-microcosm
• ISSN: 0269-7491; 1873-6424; 1873-6424
• DOI: 10.1016/j.envpol.2024.125320

The widespread use of the pesticide fipronil in domestic and agriculture sectors has resulted in its accumulation across the environment. Its use to assure food security has inadvertently affected soil microbiome composition, fertility and, ultimately, human health. Degradation of residual fipronil present in the environment using specific microbial species is a promising strategy for its removal. The present study delves into the omics approach for fipronil biodegradation using the native bacterium Rhodococcus sp. FIP_B3. It has been observed that within 40 days, nearly 84% of the insecticide gets degraded. The biodegradation follows a pseudo-first-order kinetics (k = 0.0197/d with a half-life of ∼11 days). Whole genome analysis revealed Cytochrome P450 monooxygenase, peroxidase-related enzyme, haloalkane dehalogenase, 2-nitropropane dioxygenase, and aconitate hydratase are involved in the degradation process. Fipronil-sulfone, 5-amino-1-(2-chloro-4-(trifluoromethyl)phenyl)-4- ((trifluoromethyl)sulfonyl)-1H-pyrazole-3-carbonitrile, (E)-5-chloro-2-oxo-3- (trifluoromethyl)pent-4-enoic acid, 4,4,4-trifluoro-2-oxobutanoic acid, and 3,3,3- trifluoropropanoic acid were identified as the major metabolites that support the bacterial degradation of fipronil. In-silico molecular docking and molecular dynamic simulation-based analyses of degradation pathway intermediates with their respective enzymes have indicated stable interactions with significant binding energies (−5.9 to −9.7 kcal/mol). These results have provided the mechanistic cause of the elevated potential of Rhodococcus sp. FIP_B3 for fipronil degradation and will be advantageous in framing appropriate strategies for the bioremediation of fipronil-contaminated environment. [Display omitted] •Rhodococcus sp. FIP_B3 is an efficient bio-degrader of fipronil.•Microcosm study reported ∼84 % degradation with pseudo-first-order kinetics.•Peroxidase enzyme potentially mediates fipronil to fipronil sulfone degradation.•Proteome analysis evidenced differential expression of fipronil degradative enzymes.•Metabolome analysis detected intermediary products validating the proposed pathway.