Molecular fingerprint of gilthead seabream physiology in response to pollutant mixtures in the wild

The increase in trace element concentrations in the aquatic environment due to anthropogenic activities, urges the need for their monitoring and potential toxicity, persistence, bioaccumulation, and biomagnification at different trophic levels. Gilthead seabream is a species of commercial importance in the Mediterranean Sea, both for the aquaculture and fisheries sectors, however very little is known about their trace element contamination accumulation and the resulting effect on their health status. In the present study, 135 juveniles were collected from seven coastal lagoons known to be essential nursery areas for this species. We measured seventeen different inorganic contaminants at the individual level in fish muscle (namely Al, As, Be, Bi, Cd, Cr, Cu, Hg, Li, Ni, Pb, Rb, Sb, Sr, Ti, Tl and Zn). Our results revealed the accumulation of multiple trace elements in individuals and distinct contamination signatures between lagoons which might lead to contrasted quality as nurseries for juveniles of numerous ecologically and economically relevant fish species in addition to seabreams. We further evaluated the potential adverse effect of these complex contamination mixtures on the liver (the main organ implicated in the metabolism of xenobiotics) and red muscle (a highly metabolic organ) using a proteomic approach. Alterations in cellular organization pathways and protein transport were detected in both tissues (albeit they were not similarly regulated). Chromosome organization and telomere maintenance in the liver appeared to be affected by contaminant mixture which could increase mortality, age-related disease risk and shorter lifetime expectancy for these juveniles. Red muscle proteome also demonstrated an upregulation of pathways involved in metabolism in response to contamination which raises the issue of potential energy allocation trade-offs between the organisms’ main functions such as reproduction and growth. This study provides new insights into the cellular and molecular responses of seabreams to environmental pollution and proposed biomarkers of health effects of trace elements that could serve as a starting point for larger-scale biomonitoring programs.