Dynamic regulation of extracellular superoxide production by the coccolithophore Emiliania huxleyi (CCMP 374)

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Date
2019-07-12
Authors
Plummer, Sydney
Taylor, Alexander E.
Harvey, Elizabeth L.
Hansel, Colleen M.
Diaz, Julia M.
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DOI
10.3389/fmicb.2019.01546
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Keywords
Reactive oxygen species
Superoxide
Emiliania huxleyi
Photophysiology
Oxidative stress
Redox homeostasis
Biogeochemical cycling
Abstract
In marine waters, ubiquitous reactive oxygen species (ROS) drive biogeochemical cycling of metals and carbon. Marine phytoplankton produce the ROS superoxide (O2−) extracellularly and can be a dominant source of O2− in natural aquatic systems. However, the cellular regulation, biological functioning, and broader ecological impacts of extracellular O2− production by marine phytoplankton remain mysterious. Here, we explored the regulation and potential roles of extracellular O2− production by a noncalcifying strain of the cosmopolitan coccolithophorid Emiliania huxleyi, a key species of marine phytoplankton that has not been examined for extracellular O2− production previously. Cell-normalized extracellular O2− production was the highest under presumably low-stress conditions during active proliferation and inversely related to cell density during exponential growth phase. Removal of extracellular O2− through addition of the O2− scavenger superoxide dismutase (SOD), however, increased growth rates, growth yields, cell biovolume, and photosynthetic efficiency (Fv/Fm) indicating an overall physiological improvement. Thus, the presence of extracellular O2− does not directly stimulate E. huxleyi proliferation, as previously suggested for other phytoplankton, bacteria, fungi, and protists. Extracellular O2− production decreased in the dark, suggesting a connection with photosynthetic processes. Taken together, the tight regulation of this stress independent production of extracellular O2− by E. huxleyi suggests that it could be involved in fundamental photophysiological processes.
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© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Plummeer, S., Taylor, A. E., Harvey, E. L., Hansel, C. M., & Diaz, J. M. Dynamic regulation of extracellular superoxide production by the coccolithophore Emiliania huxleyi (CCMP 374). Frontiers in Microbiology, 10, (2019): 1546, doi: 10.3389/fmicb.2019.01546.
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Plummeer, S., Taylor, A. E., Harvey, E. L., Hansel, C. M., & Diaz, J. M. (2019). Dynamic regulation of extracellular superoxide production by the coccolithophore Emiliania huxleyi (CCMP 374). Frontiers in Microbiology, 10, 1546.
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