Unveiling the impact of bisphenol A on date mussels: Insights into oxidative stress, hormonal imbalance, gonadal atresia, and immune resilience

Abstract

Sedentary organisms, such as mussels, may be susceptible to environmental estrogenic compounds, including bisphenol A (BPA). This study aimed to evaluate the interplay between BPA exposure and the immune response, hormonal imbalance, tissue damage (specifically in the digestive glands, labial palps, and male gonads), gonadal atresia, and antioxidant mechanisms in the marine mussel, Lithophaga lithophaga. Over a period of 28 days, mussels were exposed to BPA concentrations of 0, 0.25, 1, 2, and 5 μg/L. The exposure resulted in notable morphological alterations in the hemocytes of L. lithophaga, characterized by irregularities in the outer cell membranes of granulocytes and hyalinocytes, with some cells exhibiting filopodia formation. Granulocytes displayed an increased number of granules and vacuoles, while the nuclei of hyalinocytes appeared shrunken. The condition index, along with levels of testosterone and 17β-estradiol, significantly decreased with increasing BPA concentration, except for the 1 and 2 μg/L treatments. BPA exposure led to a marked increase in malondialdehyde (MDA) levels and a reduction in reduced glutathione (GSH) across all tissues at every concentration tested. The activity of antioxidant enzymes varied among the gonads, digestive glands, and labial palps. Notably, there was a significant increase in superoxide dismutase (SOD) activity in the gonads of mussels exposed to 2 μg/L of BPA, as well as in the digestive glands and labial palps of those exposed to 1 μg/L, suggesting a potential alteration in redox homeostasis. Additionally, structural changes in the digestive tubules of BPA-exposed mussels were observed. The observed pathological symptoms were characteristic of an inflammatory response, including hemocyte diapedesis and infiltration, the formation of syncytia, and the sloughing of epithelial tissue, indicated by an increased ratio of mean luminal radius to mean epithelial thickness in a dose-dependent manner. In the BPA-exposed group, testicular follicles exhibited atrophy, deformation, and a reduction in both size and number per area, appearing nearly empty and lacking spermatids and spermatozoa, alongside hypertrophy and hyperplasia of auxiliary cells. Scanning electron microscopy further revealed structural abnormalities in the heads and flagella of spermatids from the BPA-exposed group. Thus, this study demonstrates the risk of long-term exposure to BPA in immune response, tissue, and biochemical responses of date mussel L. lithophaga. The gonad was the most affected tissues followed by the digestive gland and labial palps.