Larval Red Drum (Sciaenops ocellatus) Sublethal Exposure to Weathered Deepwater Horizon Crude Oil: Developmental and Transcriptomic Consequences

Abstract

The Deepwater Horizon (DWH) incident resulted in extensive oiling of the pelagic zone and shoreline habitats of many commercially important fish species. Exposure to the water-accommodated fraction (WAF) of oil from the spill causes developmental toxicity through cardiac defects in pelagic fish species. However, few studies have evaluated the effects of the oil on near-shore estuarine fish species such as red drum (Sciaenops ocellatus). Following exposure to a certified weathered slick oil (4.74 μg/L ∑PAH) from the DWH event, significant sublethal impacts were observed ranging from impaired nervous system development [average 17 and 22% reductions in brain and eye area at 48 h postfertilization (hpf), respectively] to abnormal cardiac morphology (100% incidence at 24, 48, and 72 hpf) in red drum larvae. Consistent with the phenotypic responses, significantly differentially expressed transcripts, enriched gene ontology, and altered functions and canonical pathways predicted adverse outcomes in nervous and cardiovascular systems, with more pronounced changes at later larval stages. Our study demonstrated that the WAF of weathered slick oil of DWH caused morphological abnormalities predicted by a suite of advanced bioinformatic tools in early developing red drum and also provided the basis for a better understanding of molecular mechanisms of crude oil toxicity in fish.

Effects of Dissolved Organic Carbon, Ultraviolet Light and their Co‐Exposure on Deepwater Horizon crude oil acute toxicity to larval red drum (Sciaenops ocellatus)

“…Although similar photo‐enhanced toxicities were observed with our tests, a direct comparison cannot be made with the above‐mentioned studies because different UV photoperiods, total exposure times, and total UV dose were applied. However, it can be concluded and confirmed that red drum are among the most sensitive fishes to crude oil and photo‐enhanced crude oil toxicity tested to date (Alloy et al 2017; Xu et al 2017).…”

“…Specifically, water samples analyzed from Barataria Bay, Louisiana (USA), where red drum are known to spawn, revealed ∑PAH concentrations >200 μg/L at the beginning of May, which decreased over time to as high as 22 μg/L by the end of June (Whitehead et al 2012). Although only mortality was assessed as a measure for acute toxicity in the present study, it should be noted that crude oil induces other sublethal effects (e.g., cardiac and ocular function and development) to developing red drum at much lower concentrations (Khursigara et al 2017; Xu et al 2017; Magnuson et al 2018). Most likely these negative effects have later repercussions to the developing fish and subsequently jeopardize their survival in the natural environment.…”

“…Red drum ( Sciaenops ocellatus ) is an ecologically and economically important fish species of the Gulf of Mexico that is very sensitive to crude oil exposure, especially if exposed during the ELS (Alloy et al 2017; Xu et al 2017). They spawn along the Gulf coast and produce transparent, positively buoyant embryos that develop relatively quickly and hatch at approximately 1 d post fertilization (Wilson and Nieland 1994).…”

Transport, Fate and Impacts of the Deep Plume of Petroleum Hydrocarbons Formed During the Macondo Blowout

“…As such, sub-lethal oil exposure in later life stage fish has important ecological implications, which is further compounded by the fact that the impairments following acute exposure (24-48 h) can be observed at least 6 weeks later Mauduit et al, 2019), and in some cases on much longer time scales (Zhang et al, 2017). In addition to the typical cardiotoxic impairments, work on the DWH oil spill has highlighted a suite of emerging toxicity endpoints in fish, including: impaired eye development (Xu et al, 2017) with subsequent reductions in visual acuity (Magnuson et al, 2018); reduced brain size (Xu et al, 2017), evidence for impaired neural function (Xu et al, 2017and altered behavior (Johansen et al, 2017Rowsey et al, 2019); evidence for mitochondrial dysfunction (Johansen and Esbaugh, 2019;Kirby et al, 2019;Xu et al, 2017Xu et al, , 2019; altered control of embryonic buoyancy (Pasparakis et al, 2017); impaired cholesterol biosynthesis (McGruer et al, 2019); impaired immune function (Bayha et al, 2017;Jones et al, 2017;Rodgers et al, 2018); and impaired hypothalamus-pituitaryinterrenal axis function (Reddam et al, 2017).…”

De Novo Hepatic Transcriptome Assembly and Systems Level Analysis of Three Species of Dietary Fish, Sardinops sagax, Scomber japonicus, and Pleuronichthys verticalis

“…As a means to link bioavailability measurements for EDCs and fish response, a genomics approach offers a robust toolkit to associate the presence of these chemicals with genomic biomarkers. Advances in molecular methods, such as microarrays, quantitative PCR (q-PCR) and high-throughput sequencing (HTS) have substantially improved the sensitivity of analyses for assessing the biological effects of EDCs on animal physiology [ 23 , 25 , 26 , 27 , 28 , 29 , 30 ]. Recently developed genomics technologies have also facilitated assessment of the effects of xenobiotics in the environment on human health [ 31 ].…”