NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica
Abstract
Reactive oxygen species (ROS) like superoxide drive rapid transformations of carbon and metals in aquatic systems and play dynamic roles in biological health, signaling, and defense across a diversity of cell types. In phytoplankton, however, the ecophysiological role(s) of extracellular superoxide production has remained elusive. Here, the mechanism and function of extracellular superoxide production by the marine diatom Thalassiosira oceanica are described. Extracellular superoxide production in T. oceanica exudates was coupled to the oxidation of NADPH. A putative NADPH-oxidizing flavoenzyme with predicted transmembrane domains and high sequence similarity to glutathione reductase (GR) was implicated in this process. GR was also linked to extracellular superoxide production by whole cells via quenching by the flavoenzyme inhibitor diphenylene iodonium (DPI) and oxidized glutathione, the preferred electron acceptor of GR. Extracellular superoxide production followed a typical photosynthesis-irradiance curve and increased by 30% above the saturation irradiance of photosynthesis, while DPI significantly impaired the efficiency of photosystem II under a wide range of light levels. Together, these results suggest that extracellular superoxide production is a byproduct of a transplasma membrane electron transport system that serves to balance the cellular redox state through the recycling of photosynthetic NADPH. This photoprotective function may be widespread, consistent withmore »
- Authors:
-
[3];
- Univ. of Georgia, Savannah, GA (United States). Skidaway Institute of Oceanography. Dept. of Marine Sciences; Woods Hole Oceanographic Institution, Woods Hole, MA (United States). Dept. of Marine Chemistry and Geochemistry
- Univ. of Georgia, Savannah, GA (United States). Skidaway Institute of Oceanography. Dept. of Marine Sciences
- Woods Hole Oceanographic Institution, Woods Hole, MA (United States). Dept. of Marine Chemistry and Geochemistry
- Woods Hole Oceanographic Institution, Woods Hole, MA (United States). Dept. of Marine Chemistry and Geochemistry; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1625032
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 116; Journal Issue: 33; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics; reactive oxygen species; photosynthesis; oxidative stress; biogeochemistry
Citation Formats
Diaz, Julia M., Plummer, Sydney, Hansel, Colleen M., Andeer, Peter F., Saito, Mak A., and McIlvin, Matthew R. NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica. United States: N. p., 2019.
Web. doi:10.1073/pnas.1821233116.
Diaz, Julia M., Plummer, Sydney, Hansel, Colleen M., Andeer, Peter F., Saito, Mak A., & McIlvin, Matthew R. NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica. United States. https://doi.org/10.1073/pnas.1821233116
Diaz, Julia M., Plummer, Sydney, Hansel, Colleen M., Andeer, Peter F., Saito, Mak A., and McIlvin, Matthew R. Thu .
"NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica". United States. https://doi.org/10.1073/pnas.1821233116. https://www.osti.gov/servlets/purl/1625032.
@article{osti_1625032,
title = {NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica},
author = {Diaz, Julia M. and Plummer, Sydney and Hansel, Colleen M. and Andeer, Peter F. and Saito, Mak A. and McIlvin, Matthew R.},
abstractNote = {Reactive oxygen species (ROS) like superoxide drive rapid transformations of carbon and metals in aquatic systems and play dynamic roles in biological health, signaling, and defense across a diversity of cell types. In phytoplankton, however, the ecophysiological role(s) of extracellular superoxide production has remained elusive. Here, the mechanism and function of extracellular superoxide production by the marine diatom Thalassiosira oceanica are described. Extracellular superoxide production in T. oceanica exudates was coupled to the oxidation of NADPH. A putative NADPH-oxidizing flavoenzyme with predicted transmembrane domains and high sequence similarity to glutathione reductase (GR) was implicated in this process. GR was also linked to extracellular superoxide production by whole cells via quenching by the flavoenzyme inhibitor diphenylene iodonium (DPI) and oxidized glutathione, the preferred electron acceptor of GR. Extracellular superoxide production followed a typical photosynthesis-irradiance curve and increased by 30% above the saturation irradiance of photosynthesis, while DPI significantly impaired the efficiency of photosystem II under a wide range of light levels. Together, these results suggest that extracellular superoxide production is a byproduct of a transplasma membrane electron transport system that serves to balance the cellular redox state through the recycling of photosynthetic NADPH. This photoprotective function may be widespread, consistent with the presence of putative homologs to T. oceanica GR in other representative marine phytoplankton and ocean metagenomes. Given predicted climate-driven shifts in global surface ocean light regimes and phytoplankton community-level photoacclimation, these results provide implications for future ocean redox balance, ecological functioning, and coupled biogeochemical transformations of carbon and metals.},
doi = {10.1073/pnas.1821233116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 33,
volume = 116,
place = {United States},
year = {Thu Jul 25 00:00:00 EDT 2019},
month = {Thu Jul 25 00:00:00 EDT 2019}
}
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Works referencing / citing this record:
Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen
journal, February 2020
- Sutherland, Kevin M.; Wankel, Scott D.; Hansel, Colleen M.
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 7
Mn oxide formation by phototrophs: Spatial and temporal patterns, with evidence of an enzymatic superoxide-mediated pathway
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Mn oxide formation by phototrophs: Spatial and temporal patterns, with evidence of an enzymatic superoxide-mediated pathway
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Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen
journal, February 2020
- Sutherland, Kevin M.; Wankel, Scott D.; Hansel, Colleen M.
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 7