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

Toxicity of Tributyltin to the European flat oyster Ostrea edulis: metabolomic responses indicate impacts to energy metabolism, biochemical composition and reproductive maturation
Toxicity of Tributyltin to the European flat oyster Ostrea edulis: metabolomic responses indicate impacts to energy metabolism, biochemical composition and reproductive maturation
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.
tributyltin, Toxicity, Metabolomics, Ostrea edulis, Endocrine disruptors
1932-6203
Zapata Restrepo, Lina
2276abeb-952d-4475-9620-bd0885291f64
Hauton, Christopher
7706f6ba-4497-42b2-8c6d-00df81676331
Hudson, Malcolm
1ae18506-6f2a-48af-8c72-83ab28679f55
Williams, Ian
c9d674ac-ee69-4937-ab43-17e716266e22
Hauton, David
49163059-9cbb-4759-8bf5-0b29c3cfb7e7
Zapata Restrepo, Lina
2276abeb-952d-4475-9620-bd0885291f64
Hauton, Christopher
7706f6ba-4497-42b2-8c6d-00df81676331
Hudson, Malcolm
1ae18506-6f2a-48af-8c72-83ab28679f55
Williams, Ian
c9d674ac-ee69-4937-ab43-17e716266e22
Hauton, David
49163059-9cbb-4759-8bf5-0b29c3cfb7e7

Zapata Restrepo, Lina, Hauton, Christopher, Hudson, Malcolm, Williams, Ian and Hauton, David (2023) Toxicity of Tributyltin to the European flat oyster Ostrea edulis: metabolomic responses indicate impacts to energy metabolism, biochemical composition and reproductive maturation. PLoS ONE, 18 (2), [e0280777]. (doi:10.1371/journal.pone.0280777).

Record type: Article

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.

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Toxicity of Tributyltin to the European flat oyster Ostrea edulis metabolomic responses indicate impacts to energy metabolism, biochemical composition and reproductive maturation - Author's Original
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Submitted date: 15 August 2022
Published date: 6 February 2023
Keywords: tributyltin, Toxicity, Metabolomics, Ostrea edulis, Endocrine disruptors

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Local EPrints ID: 473212
URI: http://eprints.soton.ac.uk/id/eprint/473212
ISSN: 1932-6203
PURE UUID: 2bbe45ce-409b-4819-b83b-5f74dc583ba2
ORCID for Christopher Hauton: ORCID iD orcid.org/0000-0002-2313-4226
ORCID for Ian Williams: ORCID iD orcid.org/0000-0002-0121-1219

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Date deposited: 12 Jan 2023 17:59
Last modified: 19 Aug 2025 04:01

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Contributors

Author: Lina Zapata Restrepo
Author: Malcolm Hudson
Author: Ian Williams ORCID iD
Author: David Hauton

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