TY - JOUR
T1 - Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder
AU - Bayha, Keith M.
AU - Ortell, Natalie
AU - Ryan, Caitlin N.
AU - Griffitt, Kimberly J.
AU - Krasnec, Michelle
AU - Sena, Johnny
AU - Ramaraj, Thiruvarangan
AU - Takeshita, Ryan
AU - Mayer, Gregory D.
AU - Schilkey, Faye
AU - Griffitt, Robert J.
N1 - Funding Information:
The authors wish to thank D Simning, J Johnson and B Baily from the Tox Lab at GCRL for technical assistance with fish culture, data collection and sampling during experimentation, and data entry and organization. All funding for this study was provided by the State of Louisiana as part of the Deepwater Horizon Natural Resource Damage Assessment awarded to the University of Southern Mississippi (master contract number S161-1814).
Funding Information:
Michelle Krasnec and Ryan Takeshita are employees of Stratus Consulting (now Abt Associates). All funding for this study was provided by the State of Louisiana through Stratus Consulting (master contract number S161-1814) as part of the Deepwater Horizon Natural Resource Damage Assessment to the University of Southern Mississippi. There are no patents, products in development or marketed products to declare. This does not alter our adherence to all the PLOS ONE policies on sharing data and materials.
Publisher Copyright:
© 2017 Bayha et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PY - 2017/5
Y1 - 2017/5
N2 - 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. Oilexposure 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, sedimentborne 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.
AB - 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. Oilexposure 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, sedimentborne 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.
UR - http://www.scopus.com/inward/record.url?scp=85019010799&partnerID=8YFLogxK
U2 - 10.1371/journal.pone.0176559
DO - 10.1371/journal.pone.0176559
M3 - Article
C2 - 28464028
AN - SCOPUS:85019010799
VL - 12
JO - PLoS ONE
JF - PLoS ONE
SN - 1932-6203
IS - 5
M1 - e0176559
ER -