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  • 1
    Publication Date: 2022-05-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Long, M. H., Sutherland, K., Wankel, S. D., Burdige, D. J., & Zimmerman, R. C. Ebullition of oxygen from seagrasses under supersaturated conditions. Limnology and Oceanography, (2019), doi:10.1002/lno.11299.
    Description: Gas ebullition from aquatic systems to the atmosphere represents a potentially important fraction of primary production that goes unquantified by measurements of dissolved gas concentrations. Although gas ebullition from photosynthetic surfaces has often been observed, it is rarely quantified. The resulting underestimation of photosynthetic activity may significantly bias the determination of ecosystem trophic status and estimated rates of biogeochemical cycling from in situ measures of dissolved oxygen. Here, we quantified gas ebullition rates in Zostera marina meadows in Virginia, U.S.A. using simple funnel traps and analyzed the oxygen concentration and isotopic composition of the captured gas. Maximum hourly rates of oxygen ebullition (3.0 mmol oxygen m−2 h−1) were observed during the coincidence of high irradiance and low tides, particularly in the afternoon when oxygen and temperature maxima occurred. The daily ebullition fluxes (up to 11 mmol oxygen m−2 d−1) were roughly equivalent to net primary production rates determined from dissolved oxygen measurements indicating that bubble ebullition can represent a major component of primary production that is not commonly included in ecosystem‐scale estimates. Oxygen content comprised 20–40% of the captured bubble gas volume and correlated negatively with its δ18O values, consistent with a predominance of mixing between the higher δ18O of atmospheric oxygen in equilibrium with seawater and the lower δ18O of oxygen derived from photosynthesis. Thus, future studies interested in the metabolism of highly productive, shallow water ecosystems, and particularly those measuring in situ oxygen flux, should not ignore the bubble formation and ebullition processes described here.
    Description: Two anonymous reviewers provided thoughtful contributions that improved this manuscript. We thank Miraflor Santos, Victoria Hill, David Ruble, Jeremy Bleakney, and Brian Collister for assistance in the field and the staff of the Anheuser‐Busch Coastal Research Center for logistical support. This work was supported by NSF OCE grants 1633951 (to MHL) and 1635403 (to RCZ and DJB), NASA Fellowship NESSF NNX15AR62H (to KS), and a fellowship from the Hansewissenschaftskolleg (Institute for Advanced Studies; to SDW).
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 2
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    Massachusetts Institute of Technology and Woods Hole Oceanographic Institution
    Publication Date: 2022-05-26
    Description: Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Oceanography and Applied Ocean Science and Engineering at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution February 2020.
    Description: The redox cycling of oxygen between O2, water, and intermediate redox states including hydrogen peroxide and superoxide, has profound impact on the availability and distribution of dissolved O2, the habitability of the marine biosphere, and cellular metabolic and physiological reactions that utilize O2. The sum total of processes that produce, consume, and exchange atoms with O2 in the atmosphere, oceans, and subsurface leave their isotopic fingerprints on the abundance of the three stable isotopes of O2 in the environment. In this thesis, I explore two aspects of the oxygen cycle in the past and present. First, I investigate the ability of manganese (Mn) oxide minerals to capture and retain the oxygen isotopic signature of dissolved O2 during the oxidation of aqueous Mn(II) to Mn-oxide minerals. I determine that approximately half of the oxygen atoms in Mn(III,IV) oxides are directly incorporated from dissolved oxygen, and use isotope labeling techniques to further constrain how the dissolved oxygen isotope signature may be determined from that of Mn oxides. I perform an in-depth characterization of a ferromanganese crust from the central Pacific and, using triple oxygen isotope measurements, demonstrate that Mn oxides in ferromanganese crusts from around the world retain signatures of dissolved oxygen for at least 30 million years. I next turn to a previously unconsidered aspect of the global oxygen cycle: dark, extracellular superoxide production by marine microbes. I measure extracellular superoxide production rates by some of the ocean’s most abundant organisms. I use these rates along with previous measurements to estimate that extracellular superoxide production yields a net sink of 5-19% of marine dissolved oxygen. Ultimately, the degree to which superoxide production is a sink of oxygen lies in the fate of its primary decay product, hydrogen peroxide. I determine the range of oxidative and reductive decay of hydrogen peroxide across a range of environmental conditions in a meromictic pond, thus validating several assumptions from our global estimate. Altogether, this thesis illuminates a path toward investigating the oxygen cycle on million-year timescales in Earth’s recent past and demonstrates the importance of microbial superoxide production in the biogeochemical cycling of O2.
    Description: This work was funded by the following grants and organizations: NASA Earth and Space Science Fellowship (NNX15AR62H), MIT Praecis Presidential Graduate Fellowship, NASA Exobiology (NNX15AM046), NSF-OCE grant 1355720, WHOI Ocean Ventures Fund, MIT Student Assistance Fund, WHOI Academic Programs Office, and the Stanford Synchrotron Radiation Lightsource. Use of the Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, is supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences under Contract No. DEAC02-76SF00515.
    Repository Name: Woods Hole Open Access Server
    Type: Thesis
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  • 3
    Publication Date: 2022-10-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Sutherland, K. M., Grabb, K. C., Karolewski, J. S., Plummer, S., Farfan, G. A., Wankel, S. D., Diaz, J. M., Lamborg, C. H., & Hansel, C. M. Spatial heterogeneity in particle-associated, light-independent superoxide production within productive coastal waters. Journal of Geophysical Research: Oceans, 125(10), (2020): e2020JC016747, https://doi.org/10.1029/2020JC016747.
    Description: In the marine environment, the reactive oxygen species (ROS) superoxide is produced through a diverse array of light‐dependent and light‐independent reactions, the latter of which is thought to be primarily controlled by microorganisms. Marine superoxide production influences organic matter remineralization, metal redox cycling, and dissolved oxygen concentrations, yet the relative contributions of different sources to total superoxide production remain poorly constrained. Here we investigate the production, steady‐state concentration, and particle‐associated nature of light‐independent superoxide in productive waters off the northeast coast of North America. We find exceptionally high levels of light‐independent superoxide in the marine water column, with concentrations ranging from 10 pM to in excess of 2,000 pM. The highest superoxide concentrations were particle associated in surface seawater and in aphotic seawater collected meters off the seafloor. Filtration of seawater overlying the continental shelf lowered the light‐independent, steady‐state superoxide concentration by an average of 84%. We identify eukaryotic phytoplankton as the dominant particle‐associated source of superoxide to these coastal waters. We contrast these measurements with those collected at an off‐shelf station, where superoxide concentrations did not exceed 100 pM, and particles account for an average of 40% of the steady‐state superoxide concentration. This study demonstrates the primary role of particles in the production of superoxide in seawater overlying the continental shelf and highlights the importance of light‐independent, dissolved‐phase reactions in marine ROS production.
    Description: This work was funded by grants from the Chemical Oceanography program of the National Science Foundation (OCE‐1355720 to C. M. H. and C. H. L.), NASA Earth and Space Science Fellowship (Grant NNX15AR62H to K. M. S.), Agouron Institute Postdoctoral Fellowship (K. M. S.), NSF GRFPs (2016230268 to K. C. G. and 2017250547 to S. P.), and a Sloan Research Fellowship (J. M. D.). The Guava flow cytometer was purchased through an NSF equipment improvement grant (1624593).
    Keywords: reactive oxygen species ; Extracellular superoxide ; Light‐independent ROS
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 4
    Publication Date: 2022-05-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Sutherland, K. M., Coe, A., Gast, R. J., Plummer, S., Suffridge, C. P., Diaz, J. M., Bowman, J. S., Wankel, S. D., & Hansel, C. M. Extracellular superoxide production by key microbes in the global ocean. Limnology and Oceanography, (2019), doi:10.1002/lno.11247.
    Description: Bacteria and eukaryotes produce the reactive oxygen species superoxide both within and outside the cell. Although superoxide is typically associated with the detrimental and sometimes fatal effects of oxidative stress, it has also been shown to be involved in a range of essential biochemical processes, including cell signaling, growth, differentiation, and defense. Light‐independent extracellular superoxide production has been shown to be widespread among many marine heterotrophs and phytoplankton, but the extent to which this trait is relevant to marine microbial physiology and ecology throughout the global ocean is unknown. Here, we investigate the dark extracellular superoxide production of five groups of organisms that are geographically widespread and represent some of the most abundant organisms in the global ocean. These include Prochlorococcus, Synechococcus, Pelagibacter, Phaeocystis, and Geminigera. Cell‐normalized net extracellular superoxide production rates ranged seven orders of magnitude, from undetectable to 14,830 amol cell−1 h−1, with the cyanobacterium Prochlorococcus being the lowest producer and the cryptophyte Geminigera being the most prolific producer. Extracellular superoxide production exhibited a strong inverse relationship with cell number, pointing to a potential role in cell signaling. We demonstrate that rapid, cell‐number–dependent changes in the net superoxide production rate by Synechococcus and Pelagibacter arose primarily from changes in gross production of extracellular superoxide, not decay. These results expand the relevance of dark extracellular superoxide production to key marine microbes of the global ocean, suggesting that superoxide production in marine waters is regulated by a diverse suite of marine organisms in both dark and sunlit waters.
    Description: The authors would like to acknowledge their funding sources including NASA NESSF NNX15AR62H (K.M.S.), NASA Exobiology grant NNX15AM04G to S.D.W. and C.M.H., NSF‐OCE grant 1355720 to C.M.H., NSF‐OPP 1641019 (J.S.B), and Simons Foundation SCOPE Award ID 329108 (Sallie W. Chisholm). The authors would also like to thank the Harvey lab (Skidaway Institute of Oceanography) for use of their flow cytometer in this study. We thank Stephen Giovannoni and Sallie Chisholm for providing bacteria strains and laboratory facilities. Additional thanks to Marianne Acker, Rogier Braakman, and Aldo Arellano for assistance in lab and helpful conversations.
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 5
    Publication Date: 2022-10-26
    Description: Author Posting. © American Geophysical Union, 2019. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Geophysical Research Letters 46(12), (2019): 6745-6754, doi:10.1029/2019GL082867.
    Description: Although photochemical oxidation is an environmental process that drives organic carbon (OC) cycling, its quantitative detection remains analytically challenging. Here, we use samples from the Deepwater Horizon oil spill to test the hypothesis that the stable oxygen isotope composition of oil (δ18OOil) is a sensitive marker for photochemical oxidation. In less than one‐week, δ18OOil increased from −0.6 to 7.2‰, a shift representing ~25% of the δ18OOC dynamic range observed in nature. By accounting for different oxygen sources (H2O or O2) and kinetic isotopic fractionation of photochemically incorporated O2, which was −9‰ for a wide range of OC sources, a mass balance was established for the surface oil's elemental oxygen content and δ18O. This δ18O‐based approach provides novel insights into the sources and pathways of hydrocarbon photo‐oxidation, thereby improving our understanding of the fate and transport of petroleum hydrocarbons in sunlit waters, and our capacity to respond effectively to future spills.
    Description: We thank Robert Ricker and Greg Baker (NOAA) for helping secure the oil residues, James Payne (Payne Environmental Consultants, Inc.) for collecting many of the surface oil residues, Joy Matthews (UC Davis) for exceptional assistance in preparing and analyzing the oil residues for oxygen content and isotopes, Hank Levi and Art Gatenby at CSC Scientific Company for assistance with the water content measurements, Robyn Comny (US EPA) for providing the Alaska North Slope oil, and Rose Cory (UMich) for discussions about our findings. Special thanks to John Hayes who provided constructive feedback on a preliminary version of this dataset prior to his passing in February of 2017. We thank Alex Sessions (CalTech) for his constructive feedback during the review process. This work was supported, in part, by National Science Foundation grants RAPID OCE‐1043976 (CMR), OCE‐1333148 (CMR), OCE‐1333026 (CMS), OCE‐1333162 (DLV), OCE‐1841092 (CPW), NASA NESSF NNX15AR62H (KMS), the Gulf of Mexico Research Initiative grants ‐ 015, SA 16‐30, and DEEP‐C consortium, a fellowship through the Hansewissenschaftskolleg (Institute for Advanced Studies) to SDW, and assistant scientist salary support from the Frank and Lisina Hoch Endowed Fund (CPW).
    Description: 2019-11-30
    Keywords: Petroleum hydrocarbons ; Photochemical oxidation ; Deepwater Horizon ; Stable oxygen isotopes ; Organic carbon
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 6
    Publication Date: 2022-10-26
    Description: Author Posting. © American Geophysical Union, 2020. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Geochemistry, Geophysics, Geosystems 21(11), (2020): e2020GC009074, doi:10.1029/2020GC009074.
    Description: Marine ferromanganese deposits, often called the scavengers of the sea, adsorb and coprecipitate with a wide range of metals of great interest for paleo‐environmental reconstructions and economic geology. The long (up to ∼75 Ma), near‐continuous record of seawater chemistry afforded by ferromanganese deposits offers much historical information about the global ocean and surface earth including crustal processes, mantle processes, ocean circulation, and biogeochemical cycles. The extent to which the ferromanganese deposits hosting these geochemical proxies undergo diagenesis on the seafloor, however, remains an important and challenging factor in assessing the fidelity of such records. In this study, we employ multiple X‐ray techniques including micro–X‐ray fluorescence, bulk and micro–X‐ray absorption spectroscopy, and X‐ray powder diffraction to probe the structural, compositional, redox, and mineral changes within a single ferromanganese crust. These techniques illuminate a complex two‐dimensional structure characterized by crust growth controlled by the availability of manganese (Mn), a dynamic range in Mn oxidation state from +3.4 to +4.0, changes in Mn mineralogy over time, and recrystallization in the lower phosphatized portions of the crust. Iron (Fe) similarly demonstrates spatial complexity with respect to concentration and mineralogy, but lacks the dynamic range of oxidation state seen for Mn. Micrometer‐scale measurements of metal abundances reveal complex element associations between trace elements and the two major oxide phases, which are not typically resolvable via bulk analytical methods. These findings provide evidence of post‐depositional processes altering chemistry and mineralogy, and provide important geochemical context for the interpretation of element and isotopic records in ferromanganese crusts.
    Description: This research is supported by NASA Exobiology NNX15AM046 to Scott D. Wankel and Colleen M. Hansel, NASA NESSF NNX15AR62H to Kevin M. Sutherland, and WHOI Ocean Exploration Institute to Colleen M. Hansel. The Stanford Synchrotron Radiation Lightsource was utilized in this study. Use of the Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, is supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences under Contract No. DE‐AC02‐76SF00515.
    Description: 2021-04-26
    Keywords: Diagenesis ; Ferromanganese crust ; Manganese oxide minerals ; X‐ray absorption spectroscopy
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 7
    Publication Date: 2022-10-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Sutherland, K. M., Wankel, S. D., & Hansel, C. M. Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen. Proceedings of the National Academy of Sciences of the United States of America, 117(7), (2020): 3433-3439, doi:10.1073/pnas.1912313117.
    Description: The balance between sources and sinks of molecular oxygen in the oceans has greatly impacted the composition of Earth’s atmosphere since the evolution of oxygenic photosynthesis, thereby exerting key influence on Earth’s climate and the redox state of (sub)surface Earth. The canonical source and sink terms of the marine oxygen budget include photosynthesis, respiration, photorespiration, the Mehler reaction, and other smaller terms. However, recent advances in understanding cryptic oxygen cycling, namely the ubiquitous one-electron reduction of O2 to superoxide by microorganisms outside the cell, remains unexplored as a potential player in global oxygen dynamics. Here we show that dark extracellular superoxide production by marine microbes represents a previously unconsidered global oxygen flux and sink comparable in magnitude to other key terms. We estimate that extracellular superoxide production represents a gross oxygen sink comprising about a third of marine gross oxygen production, and a net oxygen sink amounting to 15 to 50% of that. We further demonstrate that this total marine dark extracellular superoxide flux is consistent with concentrations of superoxide in marine environments. These findings underscore prolific marine sources of reactive oxygen species and a complex and dynamic oxygen cycle in which oxygen consumption and corresponding carbon oxidation are not necessarily confined to cell membranes or exclusively related to respiration. This revised model of the marine oxygen cycle will ultimately allow for greater reconciliation among estimates of primary production and respiration and a greater mechanistic understanding of redox cycling in the ocean.
    Description: This work was supported by NASA Earth and Space Science Fellowship NNX15AR62H to K.M.S., NASA Exobiology grant NNX15AM04G to S.D.W. and C.M.H., and NSF Division of Ocean Sciences grant 1355720 to C.M.H. This research was further supported in part by Hanse-Wissenschaftskolleg Institute of Advanced Study fellowships to C.M.H. and S.D.W. We thank Danielle Hicks for assistance with figures and Community Earth Systems Model (CESM) Large Ensemble Project for the availability and use of its data product. The CESM project is primarily supported by the NSF.
    Keywords: Microbial superoxide ; Reactive oxygen species ; Marine dissolved oxygen
    Repository Name: Woods Hole Open Access Server
    Type: Article
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