skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: 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 diatomThalassiosira oceanicaare described. Extracellular superoxide production inT. oceanicaexudates 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 putativemore » homologs toT. oceanicaGR 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.« less

Authors:
 [1];  [2]; ORCiD logo [3];  [4];  [3];  [3]
  1. 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
  2. Univ. of Georgia, Savannah, GA (United States). Skidaway Institute of Oceanography. Dept. of Marine Sciences
  3. Woods Hole Oceanographic Institution, Woods Hole, MA (United States). Dept. of Marine Chemistry and Geochemistry
  4. 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 Lab. (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. https://doi.org/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 diatomThalassiosira oceanicaare described. Extracellular superoxide production inT. oceanicaexudates 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 toT. oceanicaGR 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 = {2019},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Save / Share:

Works referenced in this record:

Exploiting algal NADPH oxidase for biophotovoltaic energy
journal, January 2015

  • Anderson, Alexander; Laohavisit, Anuphon; Blaby, Ian K.
  • Plant Biotechnology Journal, Vol. 14, Issue 1
  • DOI: 10.1111/pbi.12332

Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase
journal, February 1993

  • O'Donnell, V. B.; Tew, D. G.; Jones, O. T. G.
  • Biochemical Journal, Vol. 290, Issue 1
  • DOI: 10.1042/bj2900041

NADPH Oxidase: An Update
journal, March 1999


Species-Level Variability in Extracellular Production Rates of Reactive Oxygen Species by Diatoms
journal, March 2016


Mechanism of superoxide anion generation in the toxic red tide phytoplankton Chattonella marina: possible involvement of NAD(P)H oxidase
journal, December 2000

  • Kim, Daekyung; Nakamura, Atsushi; Okamoto, Tarou
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1524, Issue 2-3
  • DOI: 10.1016/S0304-4165(00)00161-6

Tight Regulation of Extracellular Superoxide Points to Its Vital Role in the Physiology of the Globally Relevant Roseobacter Clade
journal, March 2019


Reduction of nitro blue tetrazolium by CO2- and O2- radicals
journal, April 1980

  • Bielski, Benon H. J.; Shiue, Grace G.; Bajuk, Stanley
  • The Journal of Physical Chemistry, Vol. 84, Issue 8
  • DOI: 10.1021/j100445a006

Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes
journal, May 2013


Widespread Production of Extracellular Superoxide by Heterotrophic Bacteria
journal, May 2013


Photosynthesis does influence superoxide production in the ichthyotoxic alga Chattonella marina (Raphidophyceae)
journal, November 2002


Production of extracellular superoxide and hydrogen peroxide by five marine species of harmful bloom-forming algae
journal, November 2018

  • Diaz, Julia M.; Plummer, Sydney; Tomas, Carmelo
  • Journal of Plankton Research, Vol. 40, Issue 6
  • DOI: 10.1093/plankt/fby043

The influence of light on copper-limited growth of an oceanic diatom, Thalassiosira oceanica (Coscinodiscophyceae)
journal, August 2017

  • Kim, Jun-Woo; Price, Neil M.
  • Journal of Phycology, Vol. 53, Issue 5
  • DOI: 10.1111/jpy.12563

Thiol chemistry and specificity in redox signaling
journal, September 2008


Production of extracellular reactive oxygen species by phytoplankton: past and future directions
journal, September 2018


Quinone Reduction by the Na+-Translocating NADH Dehydrogenase Promotes Extracellular Superoxide Production in Vibrio cholerae
journal, February 2007

  • Lin, Po-Chi; Türk, Karin; Häse, Claudia C.
  • Journal of Bacteriology, Vol. 189, Issue 10
  • DOI: 10.1128/JB.01651-06

OXIDATIVE STRESS IN MARINE ENVIRONMENTS: Biochemistry and Physiological Ecology
journal, January 2006


Dynamics of extracellular superoxide production by Trichodesmium colonies from the Sargasso Sea: Controls on ROS production by Trichodesmium
journal, May 2016

  • Hansel, C. M.; Buchwald, C.; Diaz, J. M.
  • Limnology and Oceanography, Vol. 61, Issue 4
  • DOI: 10.1002/lno.10266

Do Metabolite Transport Processes Limit Photosynthesis?
journal, September 2010

  • Bräutigam, Andrea; Weber, Andreas P. M.
  • Plant Physiology, Vol. 155, Issue 1
  • DOI: 10.1104/pp.110.164970

Presence of the distinct systems responsible for superoxide anion and hydrogen peroxide generation in red tide phytoplankton Chattonella marina and Chattonella ovata
journal, January 2007

  • Kim, Daekyung; Nakashima, Takuji; Matsuyama, Yukihiko
  • Journal of Plankton Research, Vol. 29, Issue 3
  • DOI: 10.1093/plankt/fbm011

Regulation of electron transport in microalgae
journal, August 2011

  • Cardol, Pierre; Forti, Giorgio; Finazzi, Giovanni
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 8
  • DOI: 10.1016/j.bbabio.2010.12.004

Reactivity of HO 2 /O 2 Radicals in Aqueous Solution
journal, October 1985

  • Bielski, Benon H. J.; Cabelli, Diane E.; Arudi, Ravindra L.
  • Journal of Physical and Chemical Reference Data, Vol. 14, Issue 4
  • DOI: 10.1063/1.555739

Superoxide production by marine microalgae: I. Survey of 37 species from 6 classes
journal, April 2005


Rapid Hydrogen Peroxide release from the coral Stylophora pistillata during feeding and in response to chemical and physical stimuli
journal, February 2016

  • Armoza-Zvuloni, Rachel; Schneider, Avi; Sher, Daniel
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep21000

Extracellular SOD-Derived H2O2 Promotes VEGF Signaling in Caveolae/Lipid Rafts and Post-Ischemic Angiogenesis in Mice
journal, April 2010


The production of superoxide anion radicals in the reaction of reduced flavins and flavoproteins with molecular oxygen
journal, September 1969

  • Massey, V.; Strickland, S.; Mayhew, S. G.
  • Biochemical and Biophysical Research Communications, Vol. 36, Issue 6
  • DOI: 10.1016/0006-291X(69)90287-3

Uptake mechanisms for inorganic iron and ferric citrate in Trichodesmium erythraeum IMS101
journal, January 2014

  • Roe, Kelly L.; Barbeau, Katherine A.
  • Metallomics, Vol. 6, Issue 11
  • DOI: 10.1039/c4mt00026a

NOX family NADPH oxidases: Not just in mammals
journal, September 2007


Review
journal, January 2003


Redox Signaling Across Cell Membranes
journal, June 2009


Pathogen-Induced Defense and Innate Immunity in Macroalgae
journal, December 2007

  • Weinberger, Florian
  • The Biological Bulletin, Vol. 213, Issue 3
  • DOI: 10.2307/25066646

Candida albicans FRE8 encodes a member of the NADPH oxidase family that produces a burst of ROS during fungal morphogenesis
journal, December 2017


Photosynthetic electron flow affects H2O2 signaling by inactivation of catalase in Chlamydomonas reinhardtii
journal, September 2008


Superoxide generated by glutathione reductase initiates a vanadate-dependent free radical chain oxidation of NADH
journal, May 1992


Catalase- and Superoxide Dismutase-induced Morphological Changes and Growth Inhibition in the Red Tide Phytoplankton Chattonella marina
journal, January 1995

  • Oda, Tatsuya; Moritomi, Junko; Kawano, Ienobu
  • Bioscience, Biotechnology, and Biochemistry, Vol. 59, Issue 11
  • DOI: 10.1271/bbb.59.2044

Role of Superoxide as a Signaling Molecule
journal, June 2004


Extracellular production of superoxide by marine diatoms: Contrasting effects on iron redox chemistry and bioavailability
journal, July 2005

  • Kustka, Adam B.; Shaked, Yeala; Milligan, Allen J.
  • Limnology and Oceanography, Vol. 50, Issue 4
  • DOI: 10.4319/lo.2005.50.4.1172

Oxygen Consumption Associated with Ferric Reductase Activity and iron Uptake by Iron-Limited Cells of Chlorella Kessleri (Chlorophyceae)
journal, June 2001


The regulation of xanthophyll cycle activity and of non-photochemical fluorescence quenching by two alternative electron flows in the diatoms Phaeodactylum tricornutum and Cyclotella meneghiniana
journal, July 2009

  • Grouneva, Irina; Jakob, Torsten; Wilhelm, Christian
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 7
  • DOI: 10.1016/j.bbabio.2009.02.004

Redox- and Reactive Oxygen Species-Dependent Signaling into and out of the Photosynthesizing Chloroplast
journal, June 2016

  • Dietz, Karl-Josef; Turkan, Ismail; Krieger-Liszkay, Anja
  • Plant Physiology, Vol. 171, Issue 3
  • DOI: 10.1104/pp.16.00375

ROS-talk – how the apoplast, the chloroplast, and the nucleus get the message through
journal, January 2012

  • Shapiguzov, Alexey; Vainonen, Julia P.; Wrzaczek, Michael
  • Frontiers in Plant Science, Vol. 3
  • DOI: 10.3389/fpls.2012.00292

Extracellular Production and Degradation of Superoxide in the Coral Stylophora pistillata and Cultured Symbiodinium
journal, September 2010


THE WATER-WATER CYCLE IN CHLOROPLASTS: Scavenging of Active Oxygens and Dissipation of Excess Photons
journal, June 1999


Revaluating ocean warming impacts on global phytoplankton
journal, October 2015

  • Behrenfeld, Michael J.; O’Malley, Robert T.; Boss, Emmanuel S.
  • Nature Climate Change, Vol. 6, Issue 3
  • DOI: 10.1038/nclimate2838

Differential Patterns of Microbiota Recovery in Symbiotic and Aposymbiotic Corals following Antibiotic Disturbance
journal, April 2021


Superoxide production by marine microalgae: II. Towards understanding ecological consequences and possible functions
journal, March 2005


NADPH Oxidase: An Update
journal, March 1999


    Works referencing / citing this record:

    Mn oxide formation by phototrophs: Spatial and temporal patterns, with evidence of an enzymatic superoxide-mediated pathway
    journal, December 2019


    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
    • DOI: 10.1073/pnas.1912313117