Characterization of the biodegradation, bioremediation and detoxification capacity of a bacterial consortium able to degrade the fungicide thiabendazole

Abstract

Thiabendazole (TBZ) is a persistent fungicide used in the post-harvest treatment of fruits. Its application results in the production of contaminated effluents which should be treated before their environmental discharge. In the absence of efficient treatment methods in place, biological systems based on microbial inocula with specialized degrading capacities against TBZ could be a feasible treatment approach. Only recently the first bacterial consortium able to rapidly transform TBZ was isolated. This study aimed to characterize its biodegradation, bioremediation and detoxification potential. The capacity of the consortium to mineralize 14 C-benzyl-ring labelled TBZ was initially assessed. Subsequent tests evaluated its degradation capacity under various conditions (range of pH, temperatures and TBZ concentration levels) and relevant practical scenarios (simultaneous presence of other postharvest compounds) and its bioaugmentation potential in soils contaminated with increasing TBZ levels. Finally cytotoxicity assays explored its detoxification potential. The consortium effectively mineralized the benzoyl ring of the benzimidazole moiety of TBZ and degraded spillage level concentrations of the fungicide in aqueous cultures (750 mg L -1 ) and in soil (500 mg kg -1). It maintained its high degradation capacity in a wide range of pH (4.5-7.5) and temperatures (15-37°C) and in the presence of other pesticides (ortho-phenylphenol and diphenylamine). Toxicity assays using the human liver cancer cell line HepG2 showed a progressive decrease in cytotoxicity, concomitantly with the biodegradation of TBZ, pointing to a detoxification process. Overall, the bacterial consortium showed high potential for future implementation in bioremediation and biodepuration applications.

Nutritional inter-dependencies and a carbazole-dioxygenase are key elements of a bacterial consortium relying on a Sphingomonas for the degradation of the fungicide thiabendazole

“…Considering all our meta-omic analysis, non-target MS analysis, current and previous isotopic ( 13 C and 14 C) studies [14] we propose a transformation pathway of TBZ fully accomplished by Sphingomonas 3X21F (Table 1): TBZ is initially cleaved at the imidazole moiety of the benzimidazole ring by carbazole dioxygenase CarAaAcFdr; this produces an unknown dioxygenated transient intermediate which is meta -cleaved by CarBaBb and hydrolyzed by CarC to 1,3-thiazole-4-carboxamidine as a dead-end transformation product (in line with previous findings [14] and our non-target MS analysis), and catechol (directly or through the intermediate production of anthranilate). This is further transformed by Sphingomonas 3X21F (in line with the assimilation of the 13 C-phenyl moiety of TBZ in the SIP analysis and previous radiorespirometric assays [15]) probably to the ortho -cleavage pathway terminal products acetyl-CoA and succinate, entering the TCA cycle.…”

“…Bacterial specialists that have the capacity to degrade TBZ could be invaluable in bioaugmentation and biodepuration strategies to avert its environmental impact. In this context, we recently enriched from a heavily TBZ contaminated soil the first bacterial consortium capable of degrading and detoxifying TBZ while using it as the sole carbon source [14, 15]. The consortium, which was dominated by different α-, β- and γ-Proteobacteria , was stable in its composition and its degrading efficiency.…”

Extreme allelic heterogeneity at a Caenorhabditis elegans beta-tubulin locus explains natural resistance to benzimidazoles

“…Although depending on multiple factors like soil pH, the half time of carbendazim in soil can reach between 30 to 180 days [ 62 ]. Thiabendazole, another environmentally stable BZ, is intensively used in the post-harvest treatment of fruits and can reach half times of more than one year [ 61 ]. It was detected in biological waste samples in concentrations of up to 600 μg/kg [ 63 ].…”

Thiabendazole Fungicide Adsorption Onto Four Agricultural Soils Collected from the Loukkos Area of Northwestern Morocco

“…Thiabendazole is a compound derived from bеnzimidazole, primarily used in agriculture to control mould, blight and other fungi responsible for diseases in fruits and vegetables [12]. High amount of Thiabendazole used as a post-harvest fungicide results in water contamination as it has toxicity to animals causing liver and intestinal disorders [13].…”