NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica

Diaz, Julia M.; Plummer, Sydney; Hansel, Colleen M.; Andeer, Peter F.; Saito, Mak A.; McIlvin, Matthew R.

doi:10.1073/pnas.1821233116

Title: NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica

Journal Article · Thu Jul 25 00:00:00 UTC 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1821233116 · OSTI ID:1625032

Diaz, Julia M. ^[1]; Plummer, Sydney ^[2];

^[3]; Andeer, Peter F. ^[4]; Saito, Mak A. ^[3]; McIlvin, Matthew R. ^[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; DOE/OSTI
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

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1625032

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 33 Vol. 116; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Mn oxide formation by phototrophs: Spatial and temporal patterns, with evidence of an enzymatic superoxide-mediated pathway Chaput, Dominique L.; Fowler, Alexandré J.; Seo, Onyou Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-54403-8	journal	December 2019
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Mn oxide formation by phototrophs: Spatial and temporal patterns, with evidence of an enzymatic superoxide-mediated pathway Chaput, Dominique L.; Fowler, Alexandré J.; Seo, Onyou Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-54403-8	journal	December 2019
Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen Sutherland, Kevin M.; Wankel, Scott D.; Hansel, Colleen M. Proceedings of the National Academy of Sciences, Vol. 117, Issue 7 https://doi.org/10.1073/pnas.1912313117	journal	February 2020

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59 BASIC BIOLOGICAL SCIENCES
Science & Technology - Other Topics
biogeochemistry
oxidative stress
photosynthesis
reactive oxygen species

Title: NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica

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