The organophosphate pesticide -OP- malathion inducing thyroidal disruptions and failures in the metamorphosis of the Senegalese sole, Solea senegalensis

Abstract

BackgroundOrganophosphate pesticides-OP-, like malathion, can alter the normal functioning of neuro-endocrine systems (e.g., hypothalamus-pituitary-thyroid-HPT- axis), and to interfere on the thyroidal homeostasis. Through direct interactions with thyroid receptors, an/or indirectly via up-stream signalling pathways, from the HPT axis (i.e., negative feedback regulation), malathion possess the ability to affect integrity of thyroidal follicular tissue, and it can also block or delay its hormonal functioning. This insecticide can alter the majority of the ontogenetic processes, inducing several deformities, and also provoking decreases in the growth and survival patterns. The present study has been performed to determine the sublethal effects of malathion during the first month of life of the Senegalese sole, Solea senegalensis, and it is mainly focused on the metamorphosis phase. Different transcript expression levels (i.e. thyroid receptors, matrix and bone -Gla-proteins) and immunohistochemical patterns (i.e. thyroid hormones, osteocalcin, cell proliferation) have been analysed during the most critical phases of the flatfish metamorphosis, that is, through differentiation of thyroid system and skeletal development, migration of the eye, and further adaptation to benthic behaviours.ResultsIn early life stages of the Senegalese sole, the exposure to the highest concentration of malathion (6.25 μg/L) affected to the growth patterns, showing the exposed individuals, a reduction around 60 and 92% of the total length and the dry weigth, respectively. In paralell, a significant reduction of the thyroid follicles (i.e., size and number) it was also been recorded, in a dose-dependent way. Abnormal phenotypes induced in the exposed larvae, did not complete the process of metamorphosis, and displayed several morphological abnormalities and developmental disorders, which were mainly associated with the eye migration process, and with thyroidal and skeletal disorders (i.e., transcriptional and protein changes of thyroid hormones and receptors, and of matrix and bone Gla proteins distribution), that conduced to an inadequate adaptation to the benthic life.ConclusionsIn the Senegalese sole, the majority of the ontogenetic alterations induced by the exposure to malathion were mainly associated to the metamorphosis period, which is a thyroid-driven proccess. In fact, most crucial and transitional ontogenic events, appeared notably disturbed, for e.g., thyroid gland differentiation and functioning, migration of eye, skeletal development and benthonic behaviors.

The Role of the Thyroid Axis in Fish

“…In goldfish, monocrotophos decrease TH levels, and up-regulate pituitary TSHβ and hepatic DIO1 and DIO3 expressions ( 397 ). In Senegalese sole, exposure to malathion affects growth patterns (eye migration, skeletal disorders), reduces thyroid follicle size, and induces decreased thyroid signaling (as seen by low TRβ mRNA levels) ( 398 ).…”

Pesticides With Potential Thyroid Hormone-Disrupting Effects: A Review of Recent Data

“…These alterations of physiology might impact survival rates leading to restocking failures through dwindling numbers of juveniles released into river estuaries (123). Ortiz-Delgado et al (124) investigated malathion exposure effects in the Senegalese sole, Solea senegalensis, a flatfish whose morphology, obtained gradually through metamorphosis, is THdependent. By exposing fish to malathion (another OPP), the authors demonstrated the sensitivity of this process to this pesticide that is still widely used in developing countries.…”

Exposure Impacts of Diquat dibromide herbicide formulation on amphibian larval development

“…Numerous anthropogenic substances originating from industrial, pharmaceutical, and agricultural activities (herbicides, fungicides, and insecticides etc) are found in the environment. These substances majorly end up in the aquatic ecosystem, which becomes the warehouse of their residues (Ortiz-Delgado et al, 2019). Many of these substances have the potential to modulate the thyroid functions through different pathways including hormone synthesis and release, hormone transportation through the blood, hormone metabolism as well as the final clearance (Diamanti-Kandarakis et al, 2009).…”