Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder

PLoS One. 2017 May 2;12(5):e0176559. doi: 10.1371/journal.pone.0176559. eCollection 2017.

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.

MeSH terms

  • Animals
  • Fish Diseases / immunology
  • Fish Diseases / microbiology*
  • Flounder / immunology
  • Flounder / microbiology*
  • Immunity / drug effects
  • Petroleum / adverse effects*
  • Vibrio
  • Vibrio Infections / immunology
  • Vibrio Infections / veterinary

Substances

  • Petroleum

Grant support

All funding for this study was provided by the State of Louisiana through Stratus Consulting (master contract S161-1814) as part of the Deepwater Horizon Natural Resource Damage Assessment to the University of Southern Mississippi. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Michelle Krasnec and Ryan Takeshita are employees of Stratus Consulting (now Abt Associates). Stratus Consulting (now Abt Associates) provided support in the form of salaries for authors MK and RT, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.