Oyster reproduction is affected by exposure to polystyrene microplastics

Rossana Sussarellu; Marc Suquet; Yoann Thomas; Christophe Lambert; Caroline Fabioux; Marie Eve Julie Pernet; Nelly Le Goïc; Virgile Quillien; Christian Mingant; Yanouk Epelboin; Charlotte Corporeau; Julien Guyomarch; Johan Robbens; Ika Paul-Pont; Philippe Soudant; Arnaud Huvet

doi:10.1073/pnas.1519019113

Edited by Marguerite A. Xenopoulos, Trent University, Durham, ON, Canada, and accepted by the Editorial Board December 22, 2015 (received for review September 25, 2015)

Significance

Plastics are a contaminant of emerging concern accumulating in marine ecosystems. Plastics tend to break down into small particles, called microplastics, which also enter the marine environment directly as fragments from a variety of sources, including cosmetics, clothing, and industrial processes. Given their ubiquitous nature and small dimensions, the ingestion and impact of microplastics on marine life are a cause for concern, notably for filter feeders. Oysters were exposed to polystyrene microparticles, which were shown to interfere with energy uptake and allocation, reproduction, and offspring performance. A drop in energy allocation played a major role in this reproductive impairment. This study provides ground-breaking data on microplastic impacts in an invertebrate model, helping to predict ecological impact in marine ecosystems.

Abstract

Plastics are persistent synthetic polymers that accumulate as waste in the marine environment. Microplastic (MP) particles are derived from the breakdown of larger debris or can enter the environment as microscopic fragments. Because filter-feeder organisms ingest MP while feeding, they are likely to be impacted by MP pollution. To assess the impact of polystyrene microspheres (micro-PS) on the physiology of the Pacific oyster, adult oysters were experimentally exposed to virgin micro-PS (2 and 6 µm in diameter; 0.023 mg·L⁻¹) for 2 mo during a reproductive cycle. Effects were investigated on ecophysiological parameters; cellular, transcriptomic, and proteomic responses; fecundity; and offspring development. Oysters preferentially ingested the 6-µm micro-PS over the 2-µm-diameter particles. Consumption of microalgae and absorption efficiency were significantly higher in exposed oysters, suggesting compensatory and physical effects on both digestive parameters. After 2 mo, exposed oysters had significant decreases in oocyte number (−38%), diameter (−5%), and sperm velocity (−23%). The D-larval yield and larval development of offspring derived from exposed parents decreased by 41% and 18%, respectively, compared with control offspring. Dynamic energy budget modeling, supported by transcriptomic profiles, suggested a significant shift of energy allocation from reproduction to structural growth, and elevated maintenance costs in exposed oysters, which is thought to be caused by interference with energy uptake. Molecular signatures of endocrine disruption were also revealed, but no endocrine disruptors were found in the biological samples. This study provides evidence that micro-PS cause feeding modifications and reproductive disruption in oysters, with significant impacts on offspring.

Footnotes

↵¹Present address: Department of Biogeochemistry and Ecotoxicology, Laboratory of Ecotoxicology, Institute Français de Recherche pour l'Exploitation de la Mer, 43110 Nantes, France.
↵²To whom correspondence should be addressed. Email: arnaud.huvet{at}ifremer.fr.

Author contributions: R.S., P.S., and A.H. designed research; R.S., M.S., C.L., C.F., M.E.J.P., N.L.G., V.Q., C.M., Y.E., C.C., J.G., P.S., and A.H. performed research; R.S., Y.T., and A.H. analyzed data; and R.S., M.S., Y.T., C.L., C.F., C.C., J.R., I.P.P., P.S., and A.H. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. M.A.X. is a guest editor invited by the Editorial Board.
Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession no. GSE71845).
See Commentary on page 2331.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1519019113/-/DCSupplemental.

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