Comparative analysis of distinctive transcriptome profiles with biochemical evidence in bisphenol S- and benzo[a]pyrene-exposed liver tissues of the olive flounder Paralichthys olivaceus

RESEARCH ARTICLE Comparative analysis of distinctive transcriptome profiles with biochemical evidence in bisphenol S- and benzo[a]pyreneexposed liver tissues of the olive flounder Paralichthys olivaceus a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 Jee-Hyun Jung1,2*, Young-Sun Moon1, Bo-Mi Kim3, Young-Mi Lee4, Moonkoo Kim1,2, JaeSung Rhee5,6* 1 Oil and POPs Research Group, Korea Institute of Ocean Science and Technology, Geoje, South Korea, 2 Department of Marine Environmental Science, Korea University of Science and Technology, Daejeon, South Korea, 3 Unit of Polar Genomics, Korea Polar Research Institute, Incheon, South Korea, 4 Department of Life Science, College of Natural Sciences, Sangmyung University, Seoul, South Korea, 5 Department of Marine Science, College of Natural Sciences, Incheon National University, Incheon, South Korea, 6 Research Institute of Basic Sciences, Incheon National University, Incheon, South Korea * (JHJ); (JSR) OPEN ACCESS Citation: Jung J-H, Moon Y-S, Kim B-M, Lee Y-M, Kim M, Rhee J-S (2018) Comparative analysis of distinctive transcriptome profiles with biochemical evidence in bisphenol S- and benzo[a]pyreneexposed liver tissues of the olive flounder Paralichthys olivaceus. PLoS ONE 13(5): e0196425. https://doi.org/10.1371/journal. pone.0196425 Editor: Cheryl S. Rosenfeld, University of Missouri Columbia, UNITED STATES Received: January 3, 2018 Accepted: April 12, 2018 Published: May 1, 2018 Copyright: © 2018 Jung et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All the raw data are available in the Sequencing Read Archive (SRA) of NCBI under the BioProject number PRJNA421418, with the accession number SRP126397 (SRX3459054- SRX3459061). Abstract Flounder is a promising model species for environmental monitoring of coastal regions. To assess the usefulness of liver transcriptome profiling, juvenile olive flounder Paralichthys olivaceus were exposed to two pollutants, bisphenol S (BPS) and benzo[a]pyrene (BaP), which have different chemical characteristics and have distinct modes of metabolic action in teleost. Six hours after intraperitoneal injection with BPS (50 mg/kg bw) or BaP (20 mg/kg bw), liver transcriptomes were analyzed using the Illumina Hiseq 3000 platform. Interestingly, the transcriptome was highly sensitive and was distinctively expressed in response to each chemical. The primary effect of BPS was significantly increased transcription of egg process and vitellogenesis related genes, including vitellogenins (vtg1, vtg2), zona pellucida sperm-binding proteins (zp3, zp4), and estrogen receptors (erα, erβ), with increases in plasma 17β-estradiol (E2) and vitellogenin (VTG) concentrations. Following BaP treatment, detoxification- and biotransformation-related genes such as cyp1a1 and UDP-glucuronosyltransferase (ugt1a1) were significantly increased, with an increase in EROD activity. In both transcriptomes, mRNA expression of genes involved in antioxidant defense systems was increased, while genes involved in innate immunity were decreased upon BPS or BaP exposure with a decrease in complement activity. This study provides useful insight into the chemical-specific hepatic transcriptional response of P. olivaceus and suggests a basis for further studies examining biomarker application of liver transcriptomes for environmental pollution. Funding: This work was supported by a grant from the National Research Foundation of Korea (NRF2016R1A2B4009939) funded to Young-Mi Lee. The funders had no role in study design, data PLOS ONE | https://doi.org/10.1371/journal.pone.0196425 May 1, 2018 1 / 25 Chemical-specific transcriptome profiles of olive flounder collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Introduction Flatfish are bottom-dwelling fishes that spend most of their life cycle on the bottom of estuaries and coastal regions. Thus, flatfish are acutely or chronically exposed to a wide range of environmental pollutants derived from agricultural and industrial wastes, municipal sewage, and human activity [1]. Due to their benthic habitats and wide-ranging geographical distributions, flatfish could be potential indicators of water and sediment quality, using their molecular, biochemical, and physiological sensitivity. Numerous biomarkers have been continuously developed to understand the potential effects of environmental pollutants on flatfish in their role as sentinels [2–5]. The capacity of a biomarker to respond may be prolonged or restricted by complex molecular pathways with combinations of certain signal cascades, as numerous aquatic pollutants are released in different forms with distinct modes of action in waterbodies. Particularly, biochemical markers, including molecular responses, have been identified as powerful and cost-effective approaches to obtain information on the status of the environment and the effects of pollution on resident species, including flatfish [5–9]. However, the accessibility of genomic resources (e.g., whole genome and transcriptome) is limited in most marine fish, even though gene expression profiling has been widely applied to predict the potential toxicity of various chemical compounds and to elucidate the underlying molecular mechanisms. The olive flounder Paralichthys olivaceus (also known as the Japanese flounder or bastard halibut) used in this study is one of the most cosmopolitan aquaculture species in east and south Asia, including South Korea, Japan, and China. P. olivaceus is desirable for commercial culture and was subsequently introduced in many Asia countries for aquaculture production. In 2011, the catch of wild P. olivaceus was approximately 4,600 metric tons and its aquaculture production was over 40,000 metric tons [10]. One of the most important steps in developing a model species for environmental monitoring is the availability of genomic information. Genomic platforms have been successfully applied to understand diverse molecular and physiological characteristics of P. olivaceus [11–14]. The recently published whole genome sequence of P. olivaceus provides a unique advantage for genomic application among flatfish [15]. Despite these advantages, application of genomic information of P. olivaceus in marine environmental monitoring has received little attention to date. The primary objective of the present study was to test whether the transcriptome profiling of the olive flounder could be usefully applied for the monitoring of marine pollutants. Because the sensitivity of signal pathways is very different for chemicals, two distinct chemical pollutants were employed in this study. Bisphenol S (BPS) is a structural analog (...truncated)