Cargando…

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

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Bayha, Keith M., Ortell, Natalie, Ryan, Caitlin N., Griffitt, Kimberly J., Krasnec, Michelle, Sena, Johnny, Ramaraj, Thiruvarangan, Takeshita, Ryan, Mayer, Gregory D., Schilkey, Faye, Griffitt, Robert J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5413019/
https://www.ncbi.nlm.nih.gov/pubmed/28464028
http://dx.doi.org/10.1371/journal.pone.0176559
_version_ 1783233119568003072
author Bayha, Keith M.
Ortell, Natalie
Ryan, Caitlin N.
Griffitt, Kimberly J.
Krasnec, Michelle
Sena, Johnny
Ramaraj, Thiruvarangan
Takeshita, Ryan
Mayer, Gregory D.
Schilkey, Faye
Griffitt, Robert J.
author_facet Bayha, Keith M.
Ortell, Natalie
Ryan, Caitlin N.
Griffitt, Kimberly J.
Krasnec, Michelle
Sena, Johnny
Ramaraj, Thiruvarangan
Takeshita, Ryan
Mayer, Gregory D.
Schilkey, Faye
Griffitt, Robert J.
author_sort Bayha, Keith M.
collection PubMed
description 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.
format Online
Article
Text
id pubmed-5413019
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-54130192017-05-14 Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder Bayha, Keith M. Ortell, Natalie Ryan, Caitlin N. Griffitt, Kimberly J. Krasnec, Michelle Sena, Johnny Ramaraj, Thiruvarangan Takeshita, Ryan Mayer, Gregory D. Schilkey, Faye Griffitt, Robert J. PLoS One Research Article 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. Public Library of Science 2017-05-02 /pmc/articles/PMC5413019/ /pubmed/28464028 http://dx.doi.org/10.1371/journal.pone.0176559 Text en © 2017 Bayha et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Bayha, Keith M.
Ortell, Natalie
Ryan, Caitlin N.
Griffitt, Kimberly J.
Krasnec, Michelle
Sena, Johnny
Ramaraj, Thiruvarangan
Takeshita, Ryan
Mayer, Gregory D.
Schilkey, Faye
Griffitt, Robert J.
Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder
title Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder
title_full Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder
title_fullStr Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder
title_full_unstemmed Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder
title_short Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder
title_sort crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5413019/
https://www.ncbi.nlm.nih.gov/pubmed/28464028
http://dx.doi.org/10.1371/journal.pone.0176559
work_keys_str_mv AT bayhakeithm crudeoilimpairsimmunefunctionandincreasessusceptibilitytopathogenicbacteriainsouthernflounder
AT ortellnatalie crudeoilimpairsimmunefunctionandincreasessusceptibilitytopathogenicbacteriainsouthernflounder
AT ryancaitlinn crudeoilimpairsimmunefunctionandincreasessusceptibilitytopathogenicbacteriainsouthernflounder
AT griffittkimberlyj crudeoilimpairsimmunefunctionandincreasessusceptibilitytopathogenicbacteriainsouthernflounder
AT krasnecmichelle crudeoilimpairsimmunefunctionandincreasessusceptibilitytopathogenicbacteriainsouthernflounder
AT senajohnny crudeoilimpairsimmunefunctionandincreasessusceptibilitytopathogenicbacteriainsouthernflounder
AT ramarajthiruvarangan crudeoilimpairsimmunefunctionandincreasessusceptibilitytopathogenicbacteriainsouthernflounder
AT takeshitaryan crudeoilimpairsimmunefunctionandincreasessusceptibilitytopathogenicbacteriainsouthernflounder
AT mayergregoryd crudeoilimpairsimmunefunctionandincreasessusceptibilitytopathogenicbacteriainsouthernflounder
AT schilkeyfaye crudeoilimpairsimmunefunctionandincreasessusceptibilitytopathogenicbacteriainsouthernflounder
AT griffittrobertj crudeoilimpairsimmunefunctionandincreasessusceptibilitytopathogenicbacteriainsouthernflounder