Gill and liver transcriptomic responses of Achirus lineatus (Neopterygii: Achiridae) exposed to water-accommodated fraction (WAF) of light crude oil reveal an onset of hypoxia-like condition

Abstract

Crude oil is one of the most widespread pollutants released into the marine environment, and native species have provided useful information about the effect of crude oil pollution in marine ecosystems. We consider that the lined sole Achirus lineatus can be a useful monitor of the effect of crude oil in the Gulf of Mexico (GoM) because this flounder species has a wide distribution along the GoM, and its response to oil components is relevant. The objective of this study was to compare the transcriptomic changes in liver and gill of adults lined sole fish (Achirus lineatus) exposed to a sublethal acute concentration of water-accommodated fraction (WAF) of light crude oil for 48 h. RNA-Seq was performed to assess the transcriptional changes in both organs. A total of 1073 differentially expressed genes (DEGs) were detected in gills; 662 (61.69%) were upregulated, and 411 (38.30%) were downregulated whereas in liver, 515 DEGs; 306 (59.42%) were upregulated, and 209 (40.58%) were downregulated. Xenobiotic metabolism and redox metabolism, along with DNA repair mechanisms, were activated. The induction of hypoxia-regulated genes and the generalized regulation of multiple signaling pathways support the hypothesis that WAF exposition causes a hypoxia-like condition.

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Data availability

The datasets generated for this study can be found in the NCBI Sequence Read Archive (SRA) under the bioproject accession number PRJNA646280. BioSample accessions: SAMN15538527-SAMN15538534.

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Acknowledgements

We thank to Dr. Ernesto Pérez-Rueda (Instituto de Investigaciones en Matemáticas Aplicadas y en Sistemas IIMAS, Universidad Nacional Autónoma de México) and Dr. Mario Alberto Martínez-Núñez (UMDI-Sisal, Facultad de Ciencias, Universidad Nacional Autónoma de México) for their preliminary analysis of an earlier version of the transcriptome of A. lineatus. Special thanks to Mr. Richard Mena-Loría & Mrs. Irma Pérez-García for their help during maintenance of fish. The authors appreciate all the comments of the anonymous reviewers.

This research has been funded by the Mexican National Council for Science and Technology-Mexican Ministry of Energy-Hydrocarbon Fund, project 201441. This is a contribution of the Gulf of Mexico Research Consortium (CIGoM). We acknowledge PEMEX´s specific request to the Hydrocarbon Fund to address the environmental effects of oil spills in the Gulf of Mexico.

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Affiliations

Authors

Contributions

Experimental design: MAP, JAZB, RRC

Sample collection: JAPV

Experimental procedures: JAZB, MRG

Writing: JAZB, IMHV, MAP, FA, CEGP, APS, RRC

Data analysis: JAZB, DAOR, APS, IMHV

Formal analysis: JAZB, RRC

Editing: JAZB, RRC, MAP, CEGP, APS, FA

Supervising and founding resources: RRC

Corresponding author

Correspondence to Rossanna Rodríguez-Canul.

Ethics declarations

Ethics approval and consent to participate

The animal study was reviewed and approved by the Institutional Animal Care and Use Committee of the Center for Research and Advanced Studies (Centro de Investigación y de Estudios Avanzados del IPN) (CICUAL-CINVESTAV) (APPROVAL NUMBER: 2875). It complies with the applicable Mexican Official Norm (NOM-062-ZOO-1999), “Technical Specifications for the Care and Use of Laboratory Animals”, as well as all applicable federal and institutional regulations.

All authors agree to participate in the study.

Competing interests

The authors declare no competing interests.

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Responsible Editor: Bruno Nunes

Supplementary Figures

Supplementary Fig. 1
figure7

Top 20 families of proteins most regulated for each organ evaluated. A) Top 20 up and down-regulated protein families (Pfam) encoded for transcripts in gills. B) Top 20 up and down-regulated protein families (Pfam) encoded for transcripts in the liver

Supplementary Fig. 2
figure8

Correlation analysis between RNA-Seq and RT-qPCR gene expression of randomly selected DEGs. The Spearman correlation test confirm that both gene expressions analysis give similar results  (PNG 15 kb)

Supplementary Fig. 3
figure9

PAHs quantification  in the WAF stock solution. a PAHs concentrations of high and low molecular weight (HMW and LMW respectively) evaluated by condition (control group and WAF 50%). b The  EPA priority compound detected (*) and other PAHs quantified (PNG 99 kb)

Supplementary Fig. 4
figure10

PAHs quantified from the bile of A. lineatus. Some compounds were also detected in control conditions. We argue that this is due to the presence of hydrocarbons in the Yucatán coast derived from the oil industry activities in the GoM. ND, nondetected. Panel a shows the PAHs of high and low molecular weigh (HMW and LMW, respectively) evaluated by experimental conditions (control group and WAF 50%). Panel b shows the individual PAH compounds per fish (n = 4) in each experimental condition (red dot = WAF treatment fish bile, blue dot = control group fish bile, black dot = data mean, CV, coeficient of variation) (PNG 96 kb)

High resolution image (TIFF 1934 kb)

High resolution image (TIFF 548 kb)

High resolution image (TIF 199 kb)

High resolution image (TIF 258 kb)

Supplementary Table 1

Summary of de novo transcriptome statistics of Achirus lineatus (XLS 8780 kb)

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Zamora-Briseño, J.A., Améndola-Pimenta, M., Ortega-Rosas, D.A. et al. Gill and liver transcriptomic responses of Achirus lineatus (Neopterygii: Achiridae) exposed to water-accommodated fraction (WAF) of light crude oil reveal an onset of hypoxia-like condition. Environ Sci Pollut Res (2021). https://doi.org/10.1007/s11356-021-12909-7

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Keywords

  • Lined sole
  • Light crude oil
  • WAF acute exposure
  • Gulf of Mexico
  • Transcriptomic analysis
  • Hypoxia