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...
Published in: | The ISME Journal |
---|---|
Main Authors: | , , , , , , , |
Other Authors: | , |
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 |
id |
croxfordunivpr:10.1038/s41396-018-0325-4 |
---|---|
record_format |
openpolar |
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 |
_version_ |
1793769686189473792 |