Toxicity of tributyltin to the European flat oyster Ostrea edulis: Metabolomic responses indicate impacts to energy metabolism, biochemical composition and reproductive maturation

PLoS One. 2023 Feb 6;18(2):e0280777. doi: 10.1371/journal.pone.0280777. eCollection 2023.

Abstract

Tri-Butyl Tin (TBT) remains as a legacy pollutant in the benthic environments. Although the toxic impacts and endocrine disruption caused by TBT to gastropod molluscs have been established, the changes in energy reserves allocated to maintenance, growth, reproduction and survival of European oysters Ostrea edulis, a target species of concerted benthic habitat restoration projects, have not been explored. This study was designed to evaluate the effect of TBT chloride (TBTCl) on potential ions and relevant metabolomic pathways and its association with changes in physiological, biochemical and reproductive parameters in O. edulis exposed to environmental relevant concentrations of TBTCl. Oysters were exposed to TBTCl 20 ng/L (n = 30), 200 ng/L (n = 30) and 2000 ng/L (n = 30) for nine weeks. At the end of the exposure, gametogenic stage, sex, energy reserve content and metabolomic profiling analysis were conducted to elucidate the metabolic alterations that occur in individuals exposed to those compounds. Metabolite analysis showed significant changes in the digestive gland biochemistry in oysters exposed to TBTCl, decreasing tissue ATP concentrations through a combination of the disruption of the TCA cycle and other important molecular pathways involved in homeostasis, mitochondrial metabolism and antioxidant response. TBTCl exposure increased mortality and caused changes in the gametogenesis with cycle arrest in stages G0 and G1. Sex determination was affected by TBTCl exposure, increasing the proportion of oysters identified as males in O. edulis treated at 20ng/l TBTCl, and with an increased proportion of inactive stages in oysters treated with 2000 ng/l TBTCl. The presence and persistence of environmental pollutants, such as TBT, could represent an additional threat to the declining O. edulis populations and related taxa around the world, by increasing mortality, changing reproductive maturation, and disrupting metabolism. Our findings identify the need to consider additional factors (e.g. legacy pollution) when identifying coastal locations for shellfish restoration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Ecosystem
  • Energy Metabolism
  • Humans
  • Male
  • Ostrea* / physiology
  • Trialkyltin Compounds* / toxicity

Substances

  • tributyltin
  • Trialkyltin Compounds

Grants and funding

This work and Zapata-Restrepo were supported by The University of Southampton Faculty of Engineering and the Environment Graduate School and the Colombia Government scholarship (Administrative Department of Science, Techonlogy and Innovation (Departamento Administrativo de Ciencia, Tecnología e Innovación - COLCIENCIAS), PhD scholarship, call 646 (2014). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript