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  • 1
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    Constraints on superoxide mediated formation of manganese oxides (2014)
    Frontiers Media
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    Publication Date: 2022-05-25
    Description: © The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Microbiology 4 (2013): 262, doi:10.3389/fmicb.2013.00262.
    Description: Manganese (Mn) oxides are among the most reactive sorbents and oxidants within the environment, where they play a central role in the cycling of nutrients, metals, and carbon. Recent discoveries have identified superoxide (O−2) both of biogenic and abiogenic origin as an effective oxidant of Mn(II) leading to the formation of Mn oxides. Here we examined the conditions under which abiotically produced superoxide led to oxidative precipitation of Mn and the solid-phases produced. Oxidized Mn, as both aqueous Mn(III) and Mn(III/IV) oxides, was only observed in the presence of active catalase, indicating that hydrogen peroxide (H2O2), a product of the reaction of O−2 with Mn(II), inhibits the oxidation process presumably through the reduction of Mn(III). Citrate and pyrophosphate increased the yield of oxidized Mn but decreased the amount of Mn oxide produced via formation of Mn(III)-ligand complexes. While complexing ligands played a role in stabilizing Mn(III), they did not eliminate the inhibition of net Mn(III) formation by H2O2. The Mn oxides precipitated were highly disordered colloidal hexagonal birnessite, similar to those produced by biotically generated superoxide. Yet, in contrast to the large particulate Mn oxides formed by biogenic superoxide, abiotic Mn oxides did not ripen to larger, more crystalline phases. This suggests that the deposition of crystalline Mn oxides within the environment requires a biological, or at least organic, influence. This work provides the first direct evidence that, under conditions relevant to natural waters, oxidation of Mn(II) by superoxide can occur and lead to formation of Mn oxides. For organisms that oxidize Mn(II) by producing superoxide, these findings may also point to other microbially mediated processes, in particular enzymatic hydrogen peroxide degradation and/or production of organic ligand metabolites, that allow for Mn oxide formation.
    Description: This project was supported by the National Science Foundation, grants EAR-1245919/1025077 (awarded to Colleen M. Hansel and Bettina M. Voelker), and by the Radcliffe Institute for Advanced Study at Harvard University (through a fellowship to Bettina M. Voelker).
    Keywords: Manganese oxidation ; Manganese oxides ; Superoxide ; Reactive oxygen species ; Mn(III) complexes ; Organic ligands
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 2
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    Species-level variability in extracellular production rates of reactive oxygen species by diatoms (2016)
    Frontiers Media
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    Publication Date: 2022-05-25
    Description: © The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Chemistry 4 (2016): 5, doi:10.3389/fchem.2016.00005.
    Description: Biological production and decay of the reactive oxygen species (ROS) hydrogen peroxide (H2O2) and superoxide (O−2) likely have significant effects on the cycling of trace metals and carbon in marine systems. In this study, extracellular production rates of H2O2 and O−2 were determined for five species of marine diatoms in the presence and absence of light. Production of both ROS was measured in parallel by suspending cells on filters and measuring the ROS downstream using chemiluminescence probes. In addition, the ability of these organisms to break down O−2 and H2O2 was examined by measuring recovery of O−2 and H2O2 added to the influent medium. O−2 production rates ranged from undetectable to 7.3 × 10−16 mol cell−1 h−1, while H2O2 production rates ranged from undetectable to 3.4 × 10−16 mol cell−1 h−1. Results suggest that extracellular ROS production occurs through a variety of pathways even amongst organisms of the same genus. Thalassiosira spp. produced more O−2 in light than dark, even when the organisms were killed, indicating that O−2 is produced via a passive photochemical process on the cell surface. The ratio of H2O2 to O−2 production rates was consistent with production of H2O2 solely through dismutation of O−2 for T. oceanica, while T. pseudonana made much more H2O2 than O−2. T. weissflogii only produced H2O2 when stressed or killed. P. tricornutum cells did not make cell-associated ROS, but did secrete H2O2-producing substances into the growth medium. In all organisms, recovery rates for killed cultures (94–100% H2O2; 10–80% O−2) were consistently higher than those for live cultures (65–95% H2O2; 10–50% O−2). While recovery rates for killed cultures in H2O2 indicate that nearly all H2O2 was degraded by active cell processes, O−2 decay appeared to occur via a combination of active and passive processes. Overall, this study shows that the rates and pathways for ROS production and decay vary greatly among diatom species, even between those that are closely related, and as a function of light conditions.
    Description: This research was supported by NSF grant OCE-1131734/1246174 to BV and CH.
    Keywords: Reactive oxygen species ; Superoxide ; Hydrogen peroxide ; Diatoms ; Culture
    Repository Name: Woods Hole Open Access Server
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  • 3
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    Dynamic regulation of extracellular superoxide production by the coccolithophore Emiliania huxleyi (CCMP 374) (2019)
    Frontiers Media
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    Publication Date: 2022-10-26
    Description: © 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.
    Description: 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.
    Description: This research was supported by a Junior Faculty Seed Grant from the University of Georgia Research Foundation (JD), a National Science Foundation (NSF) Graduate Research Fellowship (SP), and NSF grant OCE-1355720 (CH). The FlowCam® and FIRe were purchased through a NSF Equipment Improvement Grant (1624593).
    Keywords: Reactive oxygen species ; Superoxide ; Emiliania huxleyi ; Photophysiology ; Oxidative stress ; Redox homeostasis ; Biogeochemical cycling
    Repository Name: Woods Hole Open Access Server
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  • 4
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    Development of a deep-sea submersible chemiluminescent analyzer for sensing short-lived reactive chemicals (2022)
    MDPI
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    Publication Date: 2022-10-20
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Taenzer, L., Grabb, K., Kapit, J., Pardis, W., Wankel, S. D., & Hansel, C. M. Development of a deep-sea submersible chemiluminescent analyzer for sensing short-lived reactive chemicals. Sensors, 22(5), (2022): 1709, https://doi.org/10.3390/s22051709.
    Description: Based on knowledge of their production pathways, and limited discrete observations, a variety of short-lived chemical species are inferred to play active roles in chemical cycling in the sea. In some cases, these species may exert a disproportionate impact on marine biogeochemical cycles, affecting the redox state of metal and carbon, and influencing the interaction between organisms and their environment. One such short-lived chemical is superoxide, a reactive oxygen species (ROS), which undergoes a wide range of environmentally important reactions. Yet, due to its fleeting existence which precludes traditional shipboard analyses, superoxide concentrations have never been characterized in the deep sea. To this end, we have developed a submersible oceanic chemiluminescent analyzer of reactive intermediate species (SOLARIS) to enable continuous measurements of superoxide at depth. Fluidic pumps on SOLARIS combine seawater for analysis with reagents in a spiral mixing cell, initiating a chemiluminescent reaction that is monitored by a photomultiplier tube. The superoxide in seawater is then related to the quantity of light produced. Initial field deployments of SOLARIS have revealed high-resolution trends in superoxide throughout the water column. SOLARIS presents the opportunity to constrain the distributions of superoxide, and any number of chemiluminescent species in previously unexplored environments.
    Description: This research was funded by the NSF Oceanographic Technology and Interdisciplinary Coordination (OTIC) program grant number 1736332 and NSF Chemical Oceanography program grant number 1924236. Partial support was provided by the Link Foundation Ocean Engineering and Instrumentation Fellowship (L.T.).
    Keywords: Superoxide ; Chemiluminescence ; Deep-sea
    Repository Name: Woods Hole Open Access Server
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  • 5
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    Dark production of extracellular superoxide by the coral Porites astreoides and representative symbionts (2017)
    Frontiers Media
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    Publication Date: 2022-05-26
    Description: © The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Marine Science 3 (2016): 232, doi:10.3389/fmars.2016.00232.
    Description: The reactive oxygen species (ROS) superoxide has been implicated in both beneficial and detrimental processes in coral biology, ranging from pathogenic disease resistance to coral bleaching. Despite the critical role of ROS in coral health, there is a distinct lack of ROS measurements and thus an incomplete understanding of underpinning ROS sources and production mechanisms within coral systems. Here, we quantified in situ extracellular superoxide concentrations at the surfaces of aquaria-hosted Porites astreoides during a diel cycle. High concentrations of superoxide (~10's of nM) were present at coral surfaces, and these levels did not change significantly as a function of time of day. These results indicate that the coral holobiont produces extracellular superoxide in the dark, independent of photosynthesis. As a short-lived anion at physiological pH, superoxide has a limited ability to cross intact biological membranes. Further, removing surface mucus layers from the P. astreoides colonies did not impact external superoxide concentrations. We therefore attribute external superoxide derived from the coral holobiont under these conditions to the activity of the coral host epithelium, rather than mucus-derived epibionts or internal sources such as endosymbionts (e.g., Symbiodinium). However, endosymbionts likely contribute to internal ROS levels via extracellular superoxide production. Indeed, common coral symbionts, including multiple strains of Symbiodinium (clades A to D) and the bacterium Endozoicomonas montiporae LMG 24815, produced extracellular superoxide in the dark and at low light levels. Further, representative P. astreoides symbionts, Symbiodinium CCMP2456 (clade A) and E. montiporae, produced similar concentrations of superoxide alone and in combination with each other, in the dark and low light, and regardless of time of day. Overall, these results indicate that healthy, non-stressed P. astreoides and representative symbionts produce superoxide externally, which is decoupled from photosynthetic activity and circadian control. Corals may therefore produce extracellular superoxide constitutively, highlighting an unclear yet potentially beneficial role for superoxide in coral physiology and health.
    Description: This work was supported by a Postdoctoral Fellowship from the Ford Foundation (JD), the National Science Foundation under grants OCE 1225801 (JD) and OCE 1233612 (AA), the Ocean and Climate Change Institute of the Woods Hole Oceanographic Institution (CH), a BIOS Grant in aid award (SM), the Sidney Stern Memorial Trust (CH and AA), as well as an anonymous donor.
    Keywords: Coral ; Superoxide ; Reactive oxygen species ; Photosynthesis ; Symbiodinium ; Stress
    Repository Name: Woods Hole Open Access Server
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  • 6
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    Design optimization of a submersible chemiluminescent sensor (DISCO) for improved quantification of reactive oxygen species (ROS) in surface waters (2023)
    MDPI
    Details
    Publication Date: 2023-03-08
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Grabb, K., Pardis, W., Kapit, J., Wankel, S., Hayden, E., & Hansel, C. Design optimization of a submersible chemiluminescent sensor (DISCO) for improved quantification of reactive oxygen species (ROS) in surface waters. Sensors, 22(17), (2022): 6683, https://doi.org/10.3390/s22176683.
    Description: Reactive oxygen species (ROS) are key drivers of biogeochemical cycling while also exhibiting both positive and negative effects on marine ecosystem health. However, quantification of the ROS superoxide (O2−) within environmental systems is hindered by its short half-life. Recently, the development of the diver-operated submersible chemiluminescent sensor (DISCO), a submersible, handheld instrument, enabled in situ superoxide measurements in real time within shallow coral reef ecosystems. Here, we present a redesigned and improved instrument, DISCO II. Similar to the previous DISCO, DISCO II is a self-contained, submersible sensor, deployable to 30 m depth and capable of measuring reactive intermediate species in real time. DISCO II is smaller, lighter, lower cost, and more robust than its predecessor. Laboratory validation of DISCO II demonstrated an average limit of detection in natural seawater of 133.1 pM and a percent variance of 0.7%, with stable photo multiplier tube (PMT) counts, internal temperature, and flow rates. DISCO II can also be optimized for diverse environmental conditions by adjustment of the PMT supply voltage and integration time. Field tests showed no drift in the data with a percent variance of 3.0%. Wand tip adaptations allow for in situ calibrations and decay rates of superoxide using a chemical source of superoxide (SOTS-1). Overall, DISCO II is a versatile, user-friendly sensor that enables measurements in diverse environments, thereby improving our understanding of the cycling of reactive intermediates, such as ROS, across various marine ecosystems.
    Description: The development and verification of DISCO was funded by Schmidt Marine Technology Partners (G-2010-59878 to C.M.H., S.D.W. and J.K.). This research was further supported, in part, by grants from NSF GRFP (2016230168 to K.C.G.), WHOI Ocean Ventures Fund (2020 and 2021 to K.C.G.), and the MIT Wellington and Irene Loh Fund Fellowship (4000111995 to K.C.G.).
    Keywords: Reactive oxygen species ; Superoxide ; Chemiluminescent ; In situ analysis ; Ocean sensor ; Corals
    Repository Name: Woods Hole Open Access Server
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