Transcriptomic evaluation of the American oyster, Crassostrea virginica, deployed during the Deepwater Horizon oil spill: Evidence of an active hydrocarbon response pathway

Abstract

Estuarine organisms were impacted by the Deepwater Horizon oil spill which released ∼5 million barrels of crude oil into the Gulf of Mexico in the spring and summer of 2010. Crassostrea virginica, the American oyster, is a keystone species in these coastal estuaries and is routinely used for environmental monitoring purposes. However, very little is known about their cellular and molecular responses to hydrocarbon exposure. In response to the spill, a monitoring program was initiated by deploying hatchery-reared oysters at three sites along the Alabama and Mississippi coast (Grand Bay, MS, Fort Morgan, AL, and Orange Beach, AL). Oysters were deployed for 2-month periods at five different time points from May 2010 to May 2011. Gill and digestive gland tissues were harvested for gene expression analysis and determination of aliphatic and polycyclic aromatic hydrocarbon (PAH) concentrations. To facilitate identification of stress response genes that may be involved in the hydrocarbon response, a nearly complete transcriptome was assembled using Roche 454 and Illumina high-throughput sequencing from RNA samples obtained from the gill and digestive gland tissues of deployed oysters. This effort resulted in the assembly and annotation of 27,227 transcripts comprised of a large assortment of stress response genes, including members of the aryl hydrocarbon receptor (AHR) pathway, Phase I and II biotransformation enzymes, antioxidant enzymes and xenobiotic transporters. From this assembly several potential biomarkers of hydrocarbon exposure were chosen for expression profiling, including the AHR, two cytochrome P450 1A genes (CYP1A-like 1 and CYP1A-like 2), Cu/Zn superoxide dismutase (CuZnSOD), glutathione S-transferase theta (GST theta) and multidrug resistance protein 3 (MRP3). Higher expression levels of GST theta and MRP3 were observed in gill tissues from all three sites during the summer to early fall 2010 deployments. Linear regression analysis indicated a statistically significant relationship between total PAH levels in digestive gland tissue samples with CYP1A-like 2, CuZnSOD, GST theta and MRP3 induction. These observations provide evidence of a potentially conserved AHR pathway in invertebrates and yield new insight into the development of novel biomarkers for use in environmental monitoring activities.

Soaking up the oil: Biological impacts of dispersants and crude oil on the sponge Halichondria panicea

“…Energy intensive house-keeping functions such as DNA replication are down-regulated while genes involved in general detoxification pathways and stress response are up-regulated. This response is consistent with other studies on sponges (Guzman and Conaco, 2016) and other aquatic organisms (Leveelahti et al, 2011;Jenny et al, 2016) exposed to chemical and thermal stressors or nutrient deprivation (Fan et al, 2020).…”

“…Cellular response to hydrocarbon exposure is often mediated through the aryl hydrocarbon receptor (AHR) pathway (Puga et al, 2002;Jenny et al, 2016). Target of the AHR pathway include both Phase I and Phase II detoxification genes and may also cause changes to the cell cycle (Puga et al, 2002).…”

“…In marine environments, hydrocarbons, released in large quantities during an oil spill, can cause diverse biological impacts including changes to gene expression (Jenny et al, 2016), oxidative stress, decreases in immune function (Hannam et al, 2010) and disruption of development/survival of early life history stages of organisms (Stefansson et al, 2016).…”

Biomarker responses and biotransformation capacity in Arctic and temperate benthic species exposed to polycyclic aromatic hydrocarbons

“…Phase I biotransformation of PAHs is mostly mediated by CYP1A enzymes in vertebrates, whereas other CYP enzymes than the CYP1 subfamily seem to be involved in PAH biotransformation in marine invertebrates (Livingstone 1993). Only a few studies showed the existence of the aryl hydrocarbon receptor (AHR) transcription factor in marine invertebrates and suggested that the expression of Phase I enzymes through AHR in response to hydrocarbon exposure might be tissue-specific in bivalves (Skarphéðinsdóttir et al 2003;Jenny et al 2016). Additionally, relatively large differences in dominating Phase II biotransformation pathways between invertebrates could yield different PAH metabolite patterns.…”

Pesticide mixture toxicity assessment through in situ and laboratory approaches using embryo-larval stages of the pacific oyster (Magallana gigas)

“…Moreover, an ASTM (American Society for Testing and Materials) guideline for field bivalve testing exists (ASTM, 2013). However, these monitoring studies use transplanted adult (rarely juvenile) oysters (Cao and Wang, 2016;Clara Rebouças Do Amaral et al, 2005;Hédouin et al, 2011;Jenny et al, 2016;Lee and Birch, 2016) or mussels (Benedicto et al, 2011;Brooks et al, 2012;Cappello et al, 2015;Devier et al, 2005;Haynes et al, 1995;Lehtonen et al, 2016).…”