Nitric oxide production and antioxidant function during viral infection of the coccolithophore Emiliania huxleyi

Abstract Emiliania huxleyi is a globally important marine phytoplankton that is routinely infected by viruses. Understanding the controls on the growth and demise of E. huxleyi blooms is essential for predicting the biogeochemical fate of their organic carbon and nutrients. In this study, we show th...

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Published in:The ISME Journal
Main Authors: Schieler, Brittany M, Soni, Megha V, Brown, Christopher M, Coolen, Marco J L, Fredricks, Helen, Van Mooy, Benjamin A S, Hirsh, Donald J, Bidle, Kay D
Other Authors: NSF | GEO | Division of Ocean Sciences, Gordon and Betty Moore Foundation
Format: Article in Journal/Newspaper
Language:English
Published: Oxford University Press (OUP) 2019
Subjects:
Online Access:http://dx.doi.org/10.1038/s41396-018-0325-4
http://www.nature.com/articles/s41396-018-0325-4
http://www.nature.com/articles/s41396-018-0325-4.pdf
https://academic.oup.com/ismej/article-pdf/13/4/1019/55551324/41396_2018_article_325.pdf
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spelling croxfordunivpr:10.1038/s41396-018-0325-4 2024-03-17T08:59:16+00:00 Nitric oxide production and antioxidant function during viral infection of the coccolithophore Emiliania huxleyi Schieler, Brittany M Soni, Megha V Brown, Christopher M Coolen, Marco J L Fredricks, Helen Van Mooy, Benjamin A S Hirsh, Donald J Bidle, Kay D NSF | GEO | Division of Ocean Sciences Gordon and Betty Moore Foundation NSF | GEO | Division of Ocean Sciences Gordon and Betty Moore Foundation 2019 http://dx.doi.org/10.1038/s41396-018-0325-4 http://www.nature.com/articles/s41396-018-0325-4 http://www.nature.com/articles/s41396-018-0325-4.pdf https://academic.oup.com/ismej/article-pdf/13/4/1019/55551324/41396_2018_article_325.pdf en eng Oxford University Press (OUP) https://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0 https://creativecommons.org/licenses/by/4.0 The ISME Journal volume 13, issue 4, page 1019-1031 ISSN 1751-7362 1751-7370 Ecology, Evolution, Behavior and Systematics Microbiology journal-article 2019 croxfordunivpr https://doi.org/10.1038/s41396-018-0325-4 2024-02-20T00:10:10Z Abstract Emiliania huxleyi is a globally important marine phytoplankton that is routinely infected by viruses. Understanding the controls on the growth and demise of E. huxleyi blooms is essential for predicting the biogeochemical fate of their organic carbon and nutrients. In this study, we show that the production of nitric oxide (NO), a gaseous, membrane-permeable free radical, is a hallmark of early-stage lytic infection in E. huxleyi by Coccolithoviruses, both in culture and in natural populations in the North Atlantic. Enhanced NO production was detected both intra- and extra-cellularly in laboratory cultures, and treatment of cells with an NO scavenger significantly reduced viral production. Pre-treatment of exponentially growing E. huxleyi cultures with the NO donor S-nitroso-N-acetylpenicillamine (SNAP) prior to challenge with hydrogen peroxide (H2O2) led to greater cell survival, suggesting that NO may have a cellular antioxidant function. Indeed, cell lysates generated from cultures treated with SNAP and undergoing infection displayed enhanced ability to detoxify H2O2. Lastly, we show that fluorescent indicators of cellular ROS, NO, and death, in combination with classic DNA- and lipid-based biomarkers of infection, can function as real-time diagnostic tools to identify and contextualize viral infection in natural E. huxleyi blooms. Article in Journal/Newspaper North Atlantic Oxford University Press The ISME Journal 13 4 1019 1031
institution Open Polar
collection Oxford University Press
op_collection_id croxfordunivpr
language English
topic Ecology, Evolution, Behavior and Systematics
Microbiology
spellingShingle Ecology, Evolution, Behavior and Systematics
Microbiology
Schieler, Brittany M
Soni, Megha V
Brown, Christopher M
Coolen, Marco J L
Fredricks, Helen
Van Mooy, Benjamin A S
Hirsh, Donald J
Bidle, Kay D
Nitric oxide production and antioxidant function during viral infection of the coccolithophore Emiliania huxleyi
topic_facet Ecology, Evolution, Behavior and Systematics
Microbiology
description Abstract Emiliania huxleyi is a globally important marine phytoplankton that is routinely infected by viruses. Understanding the controls on the growth and demise of E. huxleyi blooms is essential for predicting the biogeochemical fate of their organic carbon and nutrients. In this study, we show that the production of nitric oxide (NO), a gaseous, membrane-permeable free radical, is a hallmark of early-stage lytic infection in E. huxleyi by Coccolithoviruses, both in culture and in natural populations in the North Atlantic. Enhanced NO production was detected both intra- and extra-cellularly in laboratory cultures, and treatment of cells with an NO scavenger significantly reduced viral production. Pre-treatment of exponentially growing E. huxleyi cultures with the NO donor S-nitroso-N-acetylpenicillamine (SNAP) prior to challenge with hydrogen peroxide (H2O2) led to greater cell survival, suggesting that NO may have a cellular antioxidant function. Indeed, cell lysates generated from cultures treated with SNAP and undergoing infection displayed enhanced ability to detoxify H2O2. Lastly, we show that fluorescent indicators of cellular ROS, NO, and death, in combination with classic DNA- and lipid-based biomarkers of infection, can function as real-time diagnostic tools to identify and contextualize viral infection in natural E. huxleyi blooms.
author2 NSF | GEO | Division of Ocean Sciences
Gordon and Betty Moore Foundation
NSF | GEO | Division of Ocean Sciences
Gordon and Betty Moore Foundation
format Article in Journal/Newspaper
author Schieler, Brittany M
Soni, Megha V
Brown, Christopher M
Coolen, Marco J L
Fredricks, Helen
Van Mooy, Benjamin A S
Hirsh, Donald J
Bidle, Kay D
author_facet Schieler, Brittany M
Soni, Megha V
Brown, Christopher M
Coolen, Marco J L
Fredricks, Helen
Van Mooy, Benjamin A S
Hirsh, Donald J
Bidle, Kay D
author_sort Schieler, Brittany M
title Nitric oxide production and antioxidant function during viral infection of the coccolithophore Emiliania huxleyi
title_short Nitric oxide production and antioxidant function during viral infection of the coccolithophore Emiliania huxleyi
title_full Nitric oxide production and antioxidant function during viral infection of the coccolithophore Emiliania huxleyi
title_fullStr Nitric oxide production and antioxidant function during viral infection of the coccolithophore Emiliania huxleyi
title_full_unstemmed Nitric oxide production and antioxidant function during viral infection of the coccolithophore Emiliania huxleyi
title_sort nitric oxide production and antioxidant function during viral infection of the coccolithophore emiliania huxleyi
publisher Oxford University Press (OUP)
publishDate 2019
url http://dx.doi.org/10.1038/s41396-018-0325-4
http://www.nature.com/articles/s41396-018-0325-4
http://www.nature.com/articles/s41396-018-0325-4.pdf
https://academic.oup.com/ismej/article-pdf/13/4/1019/55551324/41396_2018_article_325.pdf
genre North Atlantic
genre_facet North Atlantic
op_source The ISME Journal
volume 13, issue 4, page 1019-1031
ISSN 1751-7362 1751-7370
op_rights https://creativecommons.org/licenses/by/4.0/
https://creativecommons.org/licenses/by/4.0
https://creativecommons.org/licenses/by/4.0
op_doi https://doi.org/10.1038/s41396-018-0325-4
container_title The ISME Journal
container_volume 13
container_issue 4
container_start_page 1019
op_container_end_page 1031
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