Enzymatic degradation of organophosphorus insecticides decreases toxicity in planarians and enhances survival

Abstract

Organophosphorus insecticides (OPs) are toxic compounds used for agricultural purposes and responsible for severe types of contamination worldwide. OPs may also induce chronic deleterious effects and developmental disruption. Finding remediation strategies is a major concern to diminish their impact on environment and human health. Enzymes have emerged as a promising eco-friendly route for decontaminating OPs. The enzyme SsoPox from the archaea Sulfolobus solfataricus has been particularly studied, considering both its tremendous stability and phosphotriesterase activity. However, the toxicity of the degradation products generated through enzyme hydrolysis has been poorly investigated. To address both neurotoxicity and developmental perturbation, freshwater planarians from Platyhelminthes were considered to evaluate the impact of OP and degradation product exposure. Planarians have a large proportion of stem cells that give them an unconventional capacity for regeneration. OPs were found to be highly toxic to planarians and enzyme decontamination drastically enhanced survival rate. Although not completely innocuous, the degradation products were found to be less toxic than insecticides and reduced poisoning effects by increasing NOEC values by up to eight-fold. SsoPox also limited detrimental consequences on planarian mobility and enabled them to recover a non-exposed type regeneration process suggesting that enzymatic decontamination is a promising alternative to bioremediation.

Enzymatic decontamination of paraoxon-ethyl limits long-term effects in planarians

“…Conversely to G1, enzyme treatment did not fully protect cholinesterase activities at G2 suggesting a long-term sensitization to paraoxon-ethyl over regenerating worms. These results were consistent with previous in vitro observations reporting AChE activity reduction down to 40% after paraoxon-ethyl exposure at sublethal concentration 26 . Interestingly, although cholinesterase expression was mainly detected in the anterior moiety of the worms, no difference was observed between cholinesterase activities from anterior and posterior fragment after paraoxon-ethyl exposure.…”

“…identifying and localizing expression of S. mediterranea cholinesterases. Planarians were previously shown to harbor cholinesterases sharing common ancestors with human enzymes 26,36 . Nevertheless, the number of planarian cholinesterases and their respective roles are poorly understood.…”

“…To evaluate the benefits of enzymatic decontamination of paraoxon-ethyl, planarian cholinesterase expressions were evaluated after treatment by SsoPox-αsD6. This variant was previously described to efficiently degrade a broad spectrum of organophosphorus insecticides including paraoxon-ethyl with a catalytic efficiency of 2.95 ± 1.55 × 10 4 M −1 .s −1 allowing a fast and complete decontamination and the corresponding degradation products were characterized 26,34 . The enzyme appeared to protect planarian cholinesterase expression in most cases (Fig.…”

“…Recently, SsoPox was rationally engineered and led to the isolation of variant SsoPox-αsD6 with proficient capacity to degrade a broad panel of OP [30][31][32][33][34] . The in vivo decontamination efficiency of SsoPox-αsD6 was previously demonstrated by protecting planarians from severe exposure to OP 26,35 .…”

“…Recently, a new aquatic animal model has emerged for the evaluation of toxicity of exogenous compounds: the planarian, a flatworm belonging to Platyhelminthes phylum. This worm, harboring a mammalian-like cholinergic nervous system, is an excellent animal model to study, not only toxicity, but also developmental disruptions, thanks to a huge proportion of stem cells that confers an extraordinary capacity for regeneration [24][25][26][27] . Such an animal model is highly attractive to study both the toxicity of insecticides and evaluate the efficiency of decontamination methods.…”