Skip to main content
SpringerLink
Log in

Differential Gene Expression Induced by Acute Exposure to Water Accommodated Fraction (WAF) and Chemically Enhanced WAF (CEWAF) of Light Crude Oil and Nokomis 3-F4 in Limulus polyphemus Larvae

  • Published:
Bulletin of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

In 2018 we evaluated at 48 h and 96 h, the gene expression profile of larvae of Limulus polyphemus exposed to 10% and 100% of water-accommodated fraction (WAF) of light crude oil (API 35), and 10% and 100% of a chemically enhanced WAF (CEWAF) with the dispersant Nokomis 3-F4® in a static-acute (96 h) bioassay. Alkanes and PAHs concentrations were higher in CEWAF than in WAF stock solutions. Under the proved conditions, the expression profile of genes associated to detoxification processes (glutathione S-transferase and glutathione peroxidase), stress (heat shock protein), innate immunity (tumor necrosis factor receptor-associated factor 4 traf4), cell death (apoptosis inhibitor 5) and DNA repairing (E3 ubiquitin protein ligase), showed a deregulation at 48 h followed by an upregulation at 96 h, with exception of glutathione peroxidase, heat shock protein and innate immunity that remained low in CEWAF. In conclusion, by using genes that have been proposed as biomarkers to pollutants exposure, L. polyphemus larvae showed an early activation of genes related to the immune system, antioxidant, heat shock and NER.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aas E, Baussant T, Balk L et al (2000) PAH metabolites in bile, cytochrome P4501A and DNA adducts as environmental risk parameters for chronic oil exposure: a laboratory experiment with Atlantic cod. Aquat Toxicol 51:241–258

    CAS  Google Scholar 

  • Adams J, Sweezey M, Hodson PV (2014) Oil and oil dispersant do not cause synergistic toxicity to fish embryos. Environ Toxicol Chem 33:107–114

    CAS  Google Scholar 

  • Adeyemo OK, Kroll KJ, Denslow ND (2015) Developmental abnormalities and differential expression of genes induced in oil and dispersant exposed Menidia beryllina embryos. Aquat Toxicol 168:60–71

    CAS  Google Scholar 

  • Bakker AK, Dutton J, Sclafani M, Santangelo N (2017) Accumulation of nonessential trace elements (Ag, As, Cd, Cr, Hg and Pb) in Atlantic horseshoe crab (Limulus polyphemus) early life stages. Sci Total Environ 596:69–78

    Google Scholar 

  • Barron MG, Ka’aihue L (2003) Critical evaluation of CROSERF test methods for oil dispersant toxicity testing under subarctic conditions. Mar Pollut Bull 46:1191–1199

    CAS  Google Scholar 

  • Boehm PD, Neff JM, Page DS (2007) Assessment of polycyclic aromatic hydrocarbon exposure in the waters of Prince William Sound after the Exxon Valdez oil spill: 1989–2005. Mar Pollut Bull 54:339–356

    CAS  Google Scholar 

  • Botton ML (2000) Toxicity of cadmium and mercury to horseshoe crab (Limulus polyphemus) embryos and larvae. Bull Environ Contam Toxicol 64:137–143

    CAS  Google Scholar 

  • Botton ML, Hodge M, Gonzalez TI (1998) High tolerance to tributyltin in embryos and larvae of the horseshoe Crab, Limulus polyphemus. Estuaries 21:340

    CAS  Google Scholar 

  • Botton ML, Loveland RE, Tiwari A (2003) Distribution, abundance, and survivorship of young-of-the-year in a commercially exploited population of horseshoe crabs Limulus polyphemus. Mar Ecol Prog Ser 265:175–184

    Google Scholar 

  • Botton ML, Tankersley RA, Loveland RE (2010) Developmental ecology of the American horseshoe crab Limulus polyphemus. Curr Zool 56:550–562

    Google Scholar 

  • Brown-Peterson NJ, Krasnec MO, Lay CR et al (2017) Responses of juvenile southern flounder exposed to Deepwater Horizon oil-contaminated sediments. Environ Toxicol Chem 36:1067–1076

    CAS  Google Scholar 

  • Chaudhari M, Jayaraj R, Santhosh SR, Rao PVL (2009) Oxidative damage and gene expression profile of antioxidant enzymes after T-2 toxin exposure in mice. J Biochem Mol Toxicol 23:212–221

    CAS  Google Scholar 

  • Chen H, Zha J, Yuan L, Wang Z (2015) Effects of fluoxetine on behavior, antioxidant enzyme systems, and multixenobiotic resistance in the Asian clam Corbicula fluminea. Chemosphere 119:856–862

    CAS  Google Scholar 

  • Cheung CCC, Zheng GJ, Lam PKS, Richardson BJ (2002) Relationships between tissue concentrations of chlorinated hydrocarbons (polychlorinated biphenyls and chlorinated pesticides) and antioxidative responses of marine mussels, Perna viridis. Mar Pollut Bull 45:181–191

    CAS  Google Scholar 

  • Cubillos-Rojas M, Schneider T, Hadjebi O et al (2016) The HERC2 ubiquitin ligase is essential for embryonic development and regulates motor coordination. Oncotarget 7:56083–56106

    Google Scholar 

  • de Soysa TY, Ulrich A, Friedrich T et al (2012) Macondo crude oil from the Deepwater Horizon oil spill disrupts specific developmental processes during zebrafish embryogenesis. BMC Biol 10:40

    Google Scholar 

  • Dong M, Zhu L, Shao B et al (2013) The effects of endosulfan on cytochrome P450 enzymes and glutathione S-transferases in zebrafish (Danio rerio) livers. Ecotoxicol Environ Saf 92:1–9

    CAS  Google Scholar 

  • Esbaugh AJ, Mager EM, Stieglitz JD et al (2016) The effects of weathering and chemical dispersion on Deepwater Horizon crude oil toxicity to mahi-mahi (Coryphaena hippurus) early life stages. Sci Total Environ 543:644–651

    CAS  Google Scholar 

  • Funch P, Wang T, Pertoldi C, Middelbo ANEB (2016) Low oxygen levels slow embryonic development of Limulus polyphemus. Biol Bull 231:113–119

    CAS  Google Scholar 

  • George-Ares A, Clark JR (2000) Aquatic toxicity of two Corexit® dispersants. Chemosphere 40:897–906

    CAS  Google Scholar 

  • González-Penagos CE, Zamora-Briseño JA, Cerqueda-García D, Améndola-Pimenta M, Pérez-Vega JA, Hernández-Nuñez E, Rodríguez-Canul R (2020) Alterations in the gut microbiota of zebrafish (Danio rerio) in response to water-soluble crude oil components and its mixture with a chemical dispersant. Front Public Health 8. https://doi.org/10.3389/fpubh.2020.584953

  • Hallare AV, Kosmehl T, Schulze T et al (2005) Assessing contamination levels of Laguna Lake sediments (Philippines) using a contact assay with zebrafish (Danio rerio) embryos. Sci Total Environ 347:254–271

    CAS  Google Scholar 

  • Hemmer MJ, Barron MG, Greene RM (2011) Comparative toxicity of eight oil dispersants, Louisiana sweet crude oil (LSC), and chemically dispersed LSC to two aquatic test species. Environ Toxicol Chem 30:2244–2252

    CAS  Google Scholar 

  • Hicken CE, Linbo TL, Baldwin DH et al (2011) Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish. Proc Natl Acad Sci USA 108:7086–7090

    CAS  Google Scholar 

  • Hutcheson MS, Pedersen D, Anastas ND et al (1996) Beyond TPH: health-based evaluation of petroleum hydrocarbon exposures. Regul Toxicol Pharmacol 24:85–101

    CAS  Google Scholar 

  • Jones ER, Martyniuk CJ, Morris JM et al (2017) Exposure to Deepwater Horizon oil and Corexit 9500 at low concentrations induces transcriptional changes and alters immune transcriptional pathways in sheepshead minnows. Comp Biochem Physiol Part D Genomics Proteomics 23:8–16

    CAS  Google Scholar 

  • Judson RS, Martin MT, Reif DM et al (2010) Analysis of eight oil spill dispersants using rapid, in vitro tests for endocrine and other biological activity. Environ Sci Technol 44:5979–5985

    CAS  Google Scholar 

  • Kang TH, Reardon JT, Sancar A (2011) Regulation of nucleotide excision repair activity by transcriptional and post-transcriptional control of the XPA protein. Nucleic Acids Res 39:3176–3187

    CAS  Google Scholar 

  • Kedinger V, Rio MC (2007) TRAF4, the unique family member. In: Wu H (ed) TNF receptor associated factors (TRAFs). Advances in experimental medicine and biology, vol 597. Springer, New York, pp 60–71

    Google Scholar 

  • Keith LH (2014) The source of U.S. EPA’s sixteen PAH priority pollutants. Polycycl Aromat Compd 35:147–160

    Google Scholar 

  • Kwan BKY, Chan AKY, Cheung SG, Shin PKS (2015) Responses of growth and hemolymph quality in juvenile Chinese horseshoe crab Tachypleus tridentatus (Xiphosura) to sublethaltributyltin and cadmium. Ecotoxicology 24:1880–1895

    CAS  Google Scholar 

  • Kwan BKY, Un VKY, Cheung SG, Shin PKS (2018) Horseshoe crabs as potential sentinel species for coastal health: juvenile hemolymph quality and relationship to habitat conditions. Mar Freshw Res 69:894–905

    Google Scholar 

  • Lee KW, Shim WJ, Yim UH, Kang JH (2013) Acute and chronic toxicity study of the water accommodated fraction (WAF), chemically enhanced WAF (CEWAF) of crude oil and dispersant in the rock pool copepod Tigriopus japonicus. Chemosphere 92:1161–1168

    CAS  Google Scholar 

  • Logan CA, Somero GN (2011) Effects of thermal acclimation on transcriptional responses to acute heat stress in the eurythermal fish Gillichthys mirabilis (Cooper). Am J Physiol Integr Comp Physiol 300:R1373–R1383

    CAS  Google Scholar 

  • Madison BN, Hodson PV, Langlois VS (2015) Diluted bitumen causes deformities and molecular responses indicative of oxidative stress in Japanese medaka embryos. Aquat Toxicol 165:222–230

    CAS  Google Scholar 

  • Martin JD, Adams J, Hollebone B et al (2014) Chronic toxicity of heavy fuel oils to fish embryos using multiple exposure scenarios. Environ Toxicol Chem 33:677–687

    CAS  Google Scholar 

  • Norma Oficial Mexicana (1999) Especificaciones técnicas para la producción, cuidado y uso de los animales de laboratorio. [NOM-062-ZOO-1999]. Diario Oficial de la Federación, México. DOF: 22/08/2001

  • Novitsky TJ (1984) Discovery to commercialization: the blood of the horseshoe crab. Oceanus 27:13–18

    Google Scholar 

  • Okai Y, Sato E, Higashi-Okai K, Inoue M (2004) Enhancing effect of the endocrine disruptor para-nonylphenol on the generation of reactive oxygen species in human blood neutrophils. Environ Health Perspect 112:553–556

    CAS  Google Scholar 

  • Oruc E, Sevgiler Y, Uner N (2004) Tissue-specific oxidative stress responses in fish exposed to 2,4-D and azinphosmethyl. Comp Biochem Physiol Part C Toxicol Pharmacol 137:43–51

    Google Scholar 

  • Pampanin DM, Brooks SJ, Grøsvik BE et al (2017) DNA adducts in marine fish as biological marker of genotoxicity in environmental monitoring: the way forward. Mar Environ Res 124:49–62

    Google Scholar 

  • Peiffer J, Grova N, Hidalgo S et al (2016) Behavioral toxicity and physiological changes from repeated exposure to fluorene administered orally or intraperitoneally to adult male Wistar rats: a dose–response study. Neurotoxicology 53:321–333

    CAS  Google Scholar 

  • Perrichon P, Le Menach K, Akcha F et al (2016) Toxicity assessment of water-accommodated fractions from two different oils using a zebrafish (Danio rerio) embryo-larval bioassay with a multilevel approach. Sci Total Environ 568:952–966

    CAS  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36

    Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R foundation for statistical computing. AR Core Team, Vienna

  • Rhee J-S, Raisuddin S, Lee K-W et al (2009) Heat shock protein (Hsp) gene responses of the intertidal copepod Tigriopus japonicus to environmental toxicants. Comp Biochem Physiol Part C Toxicol Pharmacol 149:104–112

    Google Scholar 

  • Rico-Martínez R, Snell TW, Shearer TL (2013) Synergistic toxicity of Macondo crude oil and dispersant Corexit 9500A ® to the Brachionus plicatilis species complex (Rotifera). Environ Pollut 173:5–10

    Google Scholar 

  • Saco-Álvarez L, Bellas J, Nieto Ó et al (2008) Toxicity and phototoxicity of water-accommodated fraction obtained from Prestige fuel oil and Marine fuel oil evaluated by marine bioassays. Sci Total Environ 394:275–282

    Google Scholar 

  • Samanta SK, Singh OV, Jain RK (2002) Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol 20:243–248. https://doi.org/10.1016/S0167-7799(02)01943-1

    Article  CAS  Google Scholar 

  • Sammarco PW, Kolian SR, Warby RA et al (2013) Distribution and concentrations of petroleum hydrocarbons associated with the BP/Deepwater Horizon Oil Spill, Gulf of Mexico. Mar Pollut Bull 73:129–143

    CAS  Google Scholar 

  • San-Segundo L, Guimarães L, Fernández Torija C et al (2016) Alterations in gene expression levels provide early indicators of chemical stress during Xenopus laevis embryo development: a case study with perfluorooctane sulfonate (PFOS). Ecotoxicol Environ Saf 127:51–60

    CAS  Google Scholar 

  • Singer MM, Aurand D, Bragin GE et al (2000) Standardization of the preparation and quantitation of water-accommodated fractions of petroleum for toxicity testing. Mar Pollut Bull 40:1007–1016

    CAS  Google Scholar 

  • Smith D, Brockmann HJ, Beekey M, King T, Millard M, Zaldívar-Rae J (2017) Conservation status of the American horseshoe crab, (Limulus polyphemus): a regional assessment. Rev Fish Biol Fish 27:135–175

    Google Scholar 

  • Sun H, Wang W, Li J, Yang Z (2014) Growth, oxidative stress responses, and gene transcription of juvenile bighead carp (Hypophthalmichthys nobilis) under chronic exposure of ammonia. Environ Toxicol Chem 33:1726–1731

    CAS  Google Scholar 

  • Tairova Z, Frantzen M, Mosbech A et al (2019) Effects of water accommodated fraction of physically and chemically dispersed heavy fuel oil on beach spawning capelin (Mallotus villosus). Mar Environ Res 147:62–71

    CAS  Google Scholar 

  • Tiedke J, Cubuk C, Burmester T (2013) Environmental acidification triggers oxidative stress and enhances globin expression in zebrafish gills. Biochem Biophys Res Commun 441:624–629

    CAS  Google Scholar 

  • Untergasser A, Nijveen H, Rao X et al (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74

    Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Google Scholar 

  • Ward JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58:236–244

    Google Scholar 

  • Wise J, Wise JP (2011) A review of the toxicity of chemical dispersants. Rev Environ Health 26:281–300

    CAS  Google Scholar 

  • Wu W, Sato K, Koike A et al (2010) HERC2 is an E3 ligase that targets BRCA1 for degradation. Cancer Res 70:6384–6392

    CAS  Google Scholar 

  • Wu D, Wang Z, Hollebone B et al (2012) Comparative toxicity of four chemically dispersed and undispersed crude oils to rainbow trout embryos. Environ Toxicol Chem 31:754–765

    CAS  Google Scholar 

  • Xie P (2013) TRAF molecules in cell signaling and in human diseases. J Mol Signal 8:7

Download references

Acknowledgements

This research has been funded by the Mexican National Council for Science and Technology (CONACyT) − Mexican Ministry of Energy − Hydrocarbon Fund, Project 201441, and CONACyT Project PDCPN 2015-1097. 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. JCAD was supported with a scholarship from PDCPN 2015-1097 Project.

Author information

Authors and Affiliations

  1. Centro de Investigación y de Estudios Avanzados del IPN (CINVESTAV-IPN) - Unidad Mérida, Carretera Antigua a Progreso Km. 6, CP 97310, Mérida, Yucatán, Mexico

    Monica Améndola-Pimenta, Carlos Eduardo González-Penagos, Jesús Alejandro Zamora-Briseño, Juan Pablo Ek-Huchim & Rossanna Rodríguez-Canul

  2. Tecnológico Nacional de México - Instituto Tecnológico de Tizimín, Final Aeropuerto Cupul s/n, CP 97700, Tizimín, Yucatán, Mexico

    Jorge Carlos Alcocer-Domínguez & Juan José Sandoval-Gio

Authors
  1. Monica Améndola-Pimenta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorge Carlos Alcocer-Domínguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan José Sandoval-Gio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carlos Eduardo González-Penagos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jesús Alejandro Zamora-Briseño
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Juan Pablo Ek-Huchim
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rossanna Rodríguez-Canul
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rossanna Rodríguez-Canul.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (TIF 727 kb)

Supplementary file2 (XLSX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Améndola-Pimenta, M., Alcocer-Domínguez, J.C., Sandoval-Gio, J.J. et al. Differential Gene Expression Induced by Acute Exposure to Water Accommodated Fraction (WAF) and Chemically Enhanced WAF (CEWAF) of Light Crude Oil and Nokomis 3-F4 in Limulus polyphemus Larvae. Bull Environ Contam Toxicol 108, 99–106 (2022). https://doi.org/10.1007/s00128-021-03272-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00128-021-03272-x

Keywords

Search

Navigation