Abstract

Exposure to crude oil or its individual constituents can have detrimental impacts on fish species, including impairment of the immune response. Increased observations of skin lesions in northern Gulf of Mexico fish during the 2010 Deepwater Horizon oil spill indicated the possibility of oil-induced immunocompromisation resulting in bacterial or viral infection. This study used a full factorial design of oil exposure and bacterial challenge to examine how oil exposure impairs southern flounder (Paralichthys lethostigma) immune function and increases susceptibility to the bacteria Vibrio anguillarum, a causative agent of vibriosis. Fish exposed to oil prior to bacterial challenge exhibited 94.4% mortality within 48 hours of bacterial exposure. Flounder challenged with V. anguillarum without prior oil exposure had <10% mortality. Exposure resulted in taxonomically distinct gill and intestine bacterial communities. Mortality strongly correlated with V. anguillarum levels, where it comprised a significantly higher percentage of the microbiome in Oil/Pathogen challenged fish and was nearly non-existent in the No Oil/Pathogen challenged fish bacterial community. Elevated V. anguillarum levels were a direct result of oil exposure-induced immunosuppression. Oil-exposure reduced expression of immunoglobulin M, the major systemic fish antibody, and resulted in an overall downregulation in transcriptome response, particularly in genes related to immune function, response to stimulus and hemostasis. Ultimately, sediment-borne oil exposure impairs immune function, leading to increased incidences of bacterial infections. This type of sediment-borne exposure may result in long-term marine ecosystem effects, as oil-bound sediment in the northern Gulf of Mexico will likely remain a contamination source for years to come.

Highlights

  • The explosion and collapse of the Deepwater Horizon oil platform on April 20, 2010 resulted in the second largest release of oil in history [1]

  • We examined the impacts of oil exposure on immune function and susceptibility to pathogenic bacteria in the southern flounder (Paralichthys lethostigma), a benthicassociated fish that supports an important sport fishery in the Gulf of Mexico [37]

  • The near complete mortality in Oil/Pathogen challenged fish within 48 hrs is linked to the interactions of two processes: the inability to fight off V. anguillarum infection and the inability to withstand the hemolytic effects of V. anguillarum by producing more red blood cells

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Summary

Introduction

The explosion and collapse of the Deepwater Horizon oil platform on April 20, 2010 resulted in the second largest release of oil in history [1]. With the release of an unprecedented amount of oil came efforts to examine observed and potential effects on the nGoM ecosystem. Multiple studies examined oil spill impacts on resident Gulf of Mexico benthic or benthopelagic invertebrates [12,13,14,15], planktonic invertebrates [16,17], fish [18,19,20,21,22,23] and marine mammals [24]. Of particular interest to this study are observations during the oil spill of increased incidences of external lesions or sores on nGoM fish species that are indicative of bacterial infections such as vibriosis [25]. Exposure has been tied to depressed immune function and increased susceptibility to pathogen infection in a wide range of fish species [27,28,29,30,31,32,33,34,35,36]

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