Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Visser, A., Wankel, S. D., Niklaus, P. A., Byrne, J. M., Kappler, A. A., & Lehmann, M. F. Impact of reactive surfaces on the abiotic reaction between nitrite and ferrous iron and associated nitrogen and oxygen isotope dynamics. Biogeosciences, 17(16), (2020): 4355-4374, doi:10.5194/bg-17-4355-2020.

Description: Anaerobic nitrate-dependent Fe(II) oxidation (NDFeO) is widespread in various aquatic environments and plays a major role in iron and nitrogen redox dynamics. However, evidence for truly enzymatic, autotrophic NDFeO remains limited, with alternative explanations involving the coupling of heterotrophic denitrification with the abiotic oxidation of structurally bound or aqueous Fe(II) by reactive intermediate nitrogen (N) species (chemodenitrification). The extent to which chemodenitrification is caused (or enhanced) by ex vivo surface catalytic effects has not been directly tested to date. To determine whether the presence of either an Fe(II)-bearing mineral or dead biomass (DB) catalyses chemodenitrification, two different sets of anoxic batch experiments were conducted: 2 mM Fe(II) was added to a low-phosphate medium, resulting in the precipitation of vivianite (Fe3(PO4)2), to which 2 mM nitrite (NO−2) was later added, with or without an autoclaved cell suspension (∼1.96×108 cells mL−1) of Shewanella oneidensis MR-1. Concentrations of nitrite (NO−2), nitrous oxide (N2O), and iron (Fe2+, Fetot) were monitored over time in both set-ups to assess the impact of Fe(II) minerals and/or DB as catalysts of chemodenitrification. In addition, the natural-abundance isotope ratios of NO−2 and N2O (δ15N and δ18O) were analysed to constrain the associated isotope effects. Up to 90 % of the Fe(II) was oxidized in the presence of DB, whereas only ∼65 % of the Fe(II) was oxidized under mineral-only conditions, suggesting an overall lower reactivity of the mineral-only set-up. Similarly, the average NO−2 reduction rate in the mineral-only experiments (0.004±0.003 mmol L−1 d−1) was much lower than in the experiments with both mineral and DB (0.053±0.013 mmol L−1 d−1), as was N2O production (204.02±60.29 nmol L−1 d−1). The N2O yield per mole NO−2 reduced was higher in the mineral-only set-ups (4 %) than in the experiments with DB (1 %), suggesting the catalysis-dependent differential formation of NO. N-NO−2 isotope ratio measurements indicated a clear difference between both experimental conditions: in contrast to the marked 15N isotope enrichment during active NO−2 reduction (15εNO2=+10.3 ‰) observed in the presence of DB, NO−2 loss in the mineral-only experiments exhibited only a small N isotope effect (〈+1 ‰). The NO−2-O isotope effect was very low in both set-ups (18εNO2 〈1 ‰), which was most likely due to substantial O isotope exchange with ambient water. Moreover, under low-turnover conditions (i.e. in the mineral-only experiments as well as initially in experiments with DB), the observed NO−2 isotope systematics suggest, transiently, a small inverse isotope effect (i.e. decreasing NO−2 δ15N and δ18O with decreasing concentrations), which was possibly related to transitory surface complexation mechanisms. Site preference (SP) of the 15N isotopes in the linear N2O molecule for both set-ups ranged between 0 ‰ and 14 ‰, which was notably lower than the values previously reported for chemodenitrification. Our results imply that chemodenitrification is dependent on the available reactive surfaces and that the NO−2 (rather than the N2O) isotope signatures may be useful for distinguishing between chemodenitrification catalysed by minerals, chemodenitrification catalysed by dead microbial biomass, and possibly true enzymatic NDFeO.

Description: This research has been supported by the Deutsche Forschungsgemeinschaft (DFG; grant no. GRK 1708, “Molecular principles of bacterial survival strategies”) and the University of Basel, Switzerland.

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

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.

Description: Seafloor hydrothermalism plays a critical role in fundamental interactions between geochemical and biological processes in the deep ocean. A significant number of hydrothermal vents are hypothesized to exist, but many of these remain undiscovered due in part to the difficulty of detecting hydrothermalism using standard sensors on rosettes towed in the water column or robotic platforms performing surveys. Here, we use in situ methane sensors to complement standard sensing technology for hydrothermalism discovery and compare sensing equipment on a towed rosette and autonomous underwater vehicle (AUV) during a 17 km long transect in the Northern Guaymas Basin. This transect spatially intersected with a known hydrothermally active venting site. These data show that methane signaled possible hydrothermal activity 1.5-3 km laterally (100-150m vertically) from a known vent. Methane as a signal for hydrothermalism performed similarly to standard turbidity sensors (plume detection 2.2-3.3 km from reference source), and more sensitively and clearly than temperature, salinity, and oxygen instruments which readily respond to physical mixing in background seawater. We additionally introduce change-point detection algorithms---streaming cross-correlation and regime identification---as a means of real-time hydrothermalism discovery and discuss related data monitoring technologies that could be used in planning, executing, and monitoring explorative surveys for hydrothermalism.

Description: NSF OCE OTIC: #1842053 Woods Hole Oceanographic Institution: Innovative Technology Award NOAA Ocean Exploration: #NA18OAR0110354 Schmidt Marine Technology Partners: #G-21-62431 NASA: #NNX17AB31G NSF OCE: #0838107 Gordon and Betty Moore Foundation: #9208 NDSEG: Graduate Fellowship MIT Martin Family Society of Fellows: Graduate Fellowship Microsoft: Graduate Research Fellowship DOE/National Nuclear Security Administration: #DE-NA000392 MIT EAPS: Houghton Fund

Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Babbin, A. R., Tamasi, T., Dumit, D., Weber, L., Rodríguez, M. V. I., Schwartz, S. L., Armenteros, M., Wankel, S. D., & Apprill, A. Discovery and quantification of anaerobic nitrogen metabolisms among oxygenated tropical Cuban stony corals. ISME Journal, (2020), doi:10.1038/s41396-020-00845-2.

Description: Coral reef health depends on an intricate relationship among the coral animal, photosynthetic algae, and a complex microbial community. The holobiont can impact the nutrient balance of their hosts amid an otherwise oligotrophic environment, including by cycling physiologically important nitrogen compounds. Here we use 15N-tracer experiments to produce the first simultaneous measurements of ammonium oxidation, nitrate reduction, and nitrous oxide (N2O) production among five iconic species of reef-building corals (Acropora palmata, Diploria labyrinthiformis, Orbicella faveolata, Porites astreoides, and Porites porites) in the highly protected Jardines de la Reina reefs of Cuba. Nitrate reduction is present in most species, but ammonium oxidation is low potentially due to photoinhibition and assimilatory competition. Coral-associated rates of N2O production indicate a widespread potential for denitrification, especially among D. labyrinthiformis, at rates of ~1 nmol cm−2 d−1. In contrast, A. palmata displays minimal active nitrogen metabolism. Enhanced rates of nitrate reduction and N2O production are observed coincident with dark net respiration periods. Genomes of bacterial cultures isolated from multiple coral species confirm that microorganisms with the ability to respire nitrate anaerobically to either dinitrogen gas or ammonium exist within the holobiont. This confirmation of anaerobic nitrogen metabolisms by coral-associated microorganisms sheds new light on coral and reef productivity.

Description: Research was conducted in the Gardens of the Queen, Cuba in accordance with the requirements of the Republic of Cuba, conducted under permit NV2370 and NV2568 issued by the Ministerio de Relaciones Exteriores. We gratefully acknowledge funding for this research by MIT Sea Grant award #2018-DOH-49-LEV, Simons Foundation award #622065, and MIT ESI seed funding to ARB, the MIT Montrym, Ferry, and mTerra Seed Grant Funds, and the generous contributions by Dr Bruce L. Heflinger.

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).

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.).

Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Gomaa, F., Utter, D. R., Powers, C., Beaudoin, D. J., Edgcomb, V. P., Filipsson, H. L., Hansel, C. M., Wankel, S. D., Zhang, Y., & Bernhard, J. M. Multiple integrated metabolic strategies allow foraminiferan protists to thrive in anoxic marine sediments. Science Advances, 7(22), (2021): eabf1586, https://doi.org/10.1126/sciadv.abf1586.

Description: Oceanic deoxygenation is increasingly affecting marine ecosystems; many taxa will be severely challenged, yet certain nominally aerobic foraminifera (rhizarian protists) thrive in oxygen-depleted to anoxic, sometimes sulfidic, sediments uninhabitable to most eukaryotes. Gene expression analyses of foraminifera common to severely hypoxic or anoxic sediments identified metabolic strategies used by this abundant taxon. In field-collected and laboratory-incubated samples, foraminifera expressed denitrification genes regardless of oxygen regime with a putative nitric oxide dismutase, a characteristic enzyme of oxygenic denitrification. A pyruvate:ferredoxin oxidoreductase was highly expressed, indicating the capability for anaerobic energy generation during exposure to hypoxia and anoxia. Near-complete expression of a diatom’s plastid genome in one foraminiferal species suggests kleptoplasty or sequestration of functional plastids, conferring a metabolic advantage despite the host living far below the euphotic zone. Through a unique integration of functions largely unrecognized among “typical” eukaryotes, benthic foraminifera represent winning microeukaryotes in the face of ongoing oceanic deoxygenation.

Description: his project was funded by the U.S. NSF IOS 1557430 and 1557566. H.L.F. acknowledges support from the Swedish Research Council VR (grant number 2017-04190).

Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Beman, J. M., Vargas, S. M., Wilson, J. M., Perez-Coronel, E., Karolewski, J. S., Vazquez, S., Yu, A., Cairo, A. E., White, M. E., Koester, I., Aluwihare, L. I., & Wankel, S. D. Substantial oxygen consumption by aerobic nitrite oxidation in oceanic oxygen minimum zones. Nature Communications, 12(1), (2021): 7043, https://doi.org/10.1038/s41467-021-27381-7.

Description: Oceanic oxygen minimum zones (OMZs) are globally significant sites of biogeochemical cycling where microorganisms deplete dissolved oxygen (DO) to concentrations 〈20 µM. Amid intense competition for DO in these metabolically challenging environments, aerobic nitrite oxidation may consume significant amounts of DO and help maintain low DO concentrations, but this remains unquantified. Using parallel measurements of oxygen consumption rates and 15N-nitrite oxidation rates applied to both water column profiles and oxygen manipulation experiments, we show that the contribution of nitrite oxidation to overall DO consumption systematically increases as DO declines below 2 µM. Nitrite oxidation can account for all DO consumption only under DO concentrations 〈393 nM found in and below the secondary chlorophyll maximum. These patterns are consistent across sampling stations and experiments, reflecting coupling between nitrate reduction and nitrite-oxidizing Nitrospina with high oxygen affinity (based on isotopic and omic data). Collectively our results demonstrate that nitrite oxidation plays a pivotal role in the maintenance and biogeochemical dynamics of OMZs.

Description: This work was supported by NSF CAREER Grant OCE-1555375 to J.M.B. Metagenome sequencing was supported by the UCMEXUS-CONACyT Collaborative Grants Program (joint awards to J.M.B. and José García Maldonado).

Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Sigler, W. A., Ewing, S. A., Wankel, S. D., Jones, C. A., Leuthold, S., Brookshire, E. N. J., & Payn, R. A. Isotopic signals in an agricultural watershed suggest denitrification is locally intensive in riparian areas but extensive in upland soils. Biogeochemistry, 158, (2022): 251–268, https://doi.org/10.1007/s10533-022-00898-9.

Description: Nitrogen loss from cultivated soils threatens the economic and environmental sustainability of agriculture. Nitrate (NO3−) derived from nitrification of nitrogen fertilizer and ammonified soil organic nitrogen may be lost from soils via denitrification, producing dinitrogen gas (N2) or the greenhouse gas nitrous oxide (N2O). Nitrate that accumulates in soils is also subject to leaching loss, which can degrade water quality and make NO3− available for downstream denitrification. Here we use patterns in the isotopic composition of NO3− observed from 2012 to 2017 to characterize N loss to denitrification within soils, groundwater, and stream riparian corridors of a non-irrigated agroecosystem in the northern Great Plains (Judith River Watershed, Montana, USA). We find evidence for denitrification across these domains, expressed as a positive linear relationship between δ15N and δ18O values of NO3−, as well as increasing δ15N values with decreasing NO3− concentration. In soils, isotopic evidence of denitrification was present during fallow periods (no crop growing), despite net accumulation of NO3− from the nitrification of ammonified soil organic nitrogen. We combine previous results for soil NO3− mass balance with δ15N mass balance to estimate denitrification rates in soil relative to groundwater and streams. Substantial denitrification from soils during fallow periods may be masked by nitrification of ammonified soil organic nitrogen, representing a hidden loss of soil organic nitrogen and an under-quantified flux of N to the atmosphere. Globally, cultivated land spends ca. 50% of time in a fallow condition; denitrification in fallow soils may be an overlooked but globally significant source of agricultural N2O emissions, which must be reduced along-side other emissions to meet Paris Agreement goals for slowing global temperature increase.

Description: National Institute of Food and Agriculture, 2011–51130-31121, S. A. Ewing, 2011, S. A. Ewing, 2016–67026-25067, S. A. Ewing, Montana State University Extension, Montana Fertilizer Advisory Committee, Montana Agricultural Experiment Station, Montana State University Vice President of Research, Montana State University College of Agriculture, Montana Institute on Ecosystems, NSF EPSCoR, OIA-1757351, S. A. Ewing, OIA-1443108, S. A. Ewing, EPS-110134, S. A. Ewing.