Abiotic nitrous oxide emission from the hypersaline Don Juan Pond in Antarctica

Samarkin, V.; Madigan, Michael T.; Bowles, Marshall W.; Casciotti, Karen L.; Priscu, John C.; McKay, Christopher P.; Joye, Samantha B.

doi:10.1038/ngeo847

Cited by 143 publications

(160 citation statements)

References 26 publications

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“…This possible path may explain the absence of sulfides in LVBr, but is clearly discordant with the high concentration of DOC, and the lack of sulfur intermediates observed. Another study conducted with soils near the hypersaline (>600), ice-free Don Juan Pond of a neighboring dry valley, demonstrated that abiotic rock-brine reactions, akin to serpentinization, produce copious amounts of H 2 and N 2 O via coupling of oxidation of Fe 2+ -rich minerals of dolerite, with reduction of nitrite and nitrate to nitrous oxide (21). Although Don Juan Pond does not support life because of low water activity, there are several parallels between the abiotic reaction proposed and LVBr geochemistry.…”

Section: Resultsmentioning

confidence: 99%

Microbial life at −13 °C in the brine of an ice-sealed Antarctic lake

Murray

Kenig

Fritsen

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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149

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The permanent ice cover of Lake Vida (Antarctica) encapsulates an extreme cryogenic brine ecosystem (−13°C; salinity, 200). This aphotic ecosystem is anoxic and consists of a slightly acidic (pH 6.2) sodium chloride-dominated brine. Expeditions in 2005 and 2010 were conducted to investigate the biogeochemistry of Lake Vida's brine system. A phylogenetically diverse and metabolically active Bacteria dominated microbial assemblage was observed in the brine. These bacteria live under very high levels of reduced metals, ammonia, molecular hydrogen (H 2 ), and dissolved organic carbon, as well as high concentrations of oxidized species of nitrogen (i.e., supersaturated nitrous oxide and ∼1 mmol·L −1 nitrate) and sulfur (as sulfate). The existence of this system, with active biota, and a suite of reduced as well as oxidized compounds, is unusual given the millennial scale of its isolation from external sources of energy. The geochemistry of the brine suggests that abiotic brine-rock reactions may occur in this system and that the rich sources of dissolved electron acceptors prevent sulfate reduction and methanogenesis from being energetically favorable. The discovery of this ecosystem and the in situ biotic and abiotic processes occurring at low temperature provides a tractable system to study habitability of isolated terrestrial cryoenvironments (e.g., permafrost cryopegs and subglacial ecosystems), and is a potential analog for habitats on other icy worlds where water-rock reactions may cooccur with saline deposits and subsurface oceans.astrobiology | geomicrobiology | microbial ecology | extreme environment T he observation of microbes surviving and growing in a variety of icy systems on Earth has expanded our understanding of how life pervades, functions, and persists under challenging conditions (e.g., refs. 1-3). Studies of the physical characteristics, the geochemical properties, and microbes in ice (triple point junctions, brine channels, gas bubbles) have also changed our perceptions of the environments that may contain traces of, or even sustain, life beyond Earth [e.g., Mars (4), Europa (5), and Enceladus (6)].Solute depression of ice crystal formation or solar radiation melting of water ice are key processes that provide liquid waterthe key solvent that makes life possible-within icy systems. Microbial communities in these conditions are often sustained by a supply of energy that ultimately derives from photosynthesis (present or past). The understanding of ecosystems based on energy sources other than the Sun comes mainly from realms where hydrothermal processes have provided reduced compounds necessary to fuel chemosynthetically driven ecosystems. Methane derived from thermogenic or biogenic sources can also support microbial communities in deep sea (7) and high arctic cold saline seeps (8). More recently, discoveries of life and associated processes in deep terrestrial subsurface ecosystems (9) provide compelling evidence of subsurface life that in some cases is fueled by nonphotosynthetic processes. Ou...

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Section: Resultsmentioning

confidence: 99%

Microbial life at −13 °C in the brine of an ice-sealed Antarctic lake

Murray

Kenig

Fritsen

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

149

190

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“…Under anoxic conditions, in which the metal components of the medium are reduced, the Fe(II) and reduced trace metals act as chemical catalysts for NO reduction to N 2 O. This 'chemodenitrification' process has been implicated by hypothesis in contributing to abiotic N 2 O production in reduced environments where Fe(II) is abundant (Samarkin et al, 2010;Kampschreur et al, 2011;Jones et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota

et al. 2016

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Chemolithotrophic ammonia-oxidizing bacteria and Thaumarchaeota are central players in the global nitrogen cycle. Obligate ammonia chemolithotrophy has been characterized for bacteria; however, large gaps remain in the Thaumarchaeotal pathway. Using batch growth experiments and instantaneous microrespirometry measurements of resting biomass, we show that the terrestrial Thaumarchaeon Nitrososphaera viennensis EN76 T exhibits tight control over production and consumption of nitric oxide (NO) during ammonia catabolism, unlike the ammonia-oxidizing bacterium Nitrosospira multiformis ATCC 25196 T . In particular, pulses of hydroxylamine into a microelectrode chamber as the sole substrate for N. viennensis resulted in iterative production and consumption of NO followed by conversion of hydroxylamine to nitrite. In support of these observations, oxidation of ammonia in growing cultures of N. viennensis, but not of N. multiformis, was inhibited by the NO-scavenger PTIO. When based on the marginal nitrous oxide (N 2 O) levels detected in cell-free media controls, the higher levels produced by N. multiformis were explained by enzyme activity, whereas N 2 O in N. viennensis cultures was attributed to abiotic reactions of released N-oxide intermediates with media components. Our results are conceptualized in a pathway for ammonia-dependent chemolithotrophy in Thaumarchaea, which identifies NO as an essential intermediate in the pathway and implements known biochemistry to be executed by a proposed but still elusive copper enzyme. Taken together, this work identifies differences in ammonia-dependent chemolithotrophy between bacteria and the Thaumarchaeota, advances a central catabolic role of NO only in the Thaumarchaeotal pathway and reveals stark differences in how the two microbial cohorts contribute to N 2 O emissions.

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“…The enzyme nitrous oxide reductase (N 2 OR), which catalyzes this reaction, is sensitive to dioxygen, so that denitrifi cation frequently ceases at this step and gaseous N 2 O is released to the atmosphere (Canfi eld et al , 2010 ). Recent years have witnessed a signifi cant increase in atmospheric levels of nitrous oxide (Schmittner and Galbraith , 2008 ;Samarkin et al , 2010 ), and the gas has been heavily scrutinized for its twofold deleterious effect on the global climate. As a ' greenhouse gas ' , its global warming potential exceeds that of CO 2 by a factor of 300, and through absorption of solar radiation in the upper troposphere and the stratosphere various NO x compounds are generated that react with atmospheric ozone, depleting the compound with an effi ciency similar to that of the largely banned hydrochlorofl uorocarbons.…”

Section: Introductionmentioning

confidence: 99%

Nature’s way of handling a greenhouse gas: the copper-sulfur cluster of purple nitrous oxide reductase

Wüst

Schneider

Pomowski

et al. 2012

Biological Chemistry

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The tetranuclear Cu Z cluster is the unique active site of nitrous oxide reductase, the enzyme that catalyzes the reduction of nitrous oxide to dinitrogen as the fi nal reaction in bacterial denitrifi cation. Three-dimensional structures of orthologs of the enzyme from a variety of different bacterial species were essential steps in the elucidation of the properties of this center. However, while structural data fi rst revealed and later confi rmed the presence of four copper ions in spectroscopically distinct forms of Cu Z , the exact structure and stoichiometry of the cluster showed signifi cant variations. A ligand bridging ions Cu Z1 and Cu Z2 was initially assigned as a water or hydroxo species in the structures from Pseudomonas nautica (now Marinobacter hydrocarbonoclasticus ) and Paracoccus denitrifi cans . This ligand was absent in a structure from ' Achromobacter cycloclastes ' , and could be reconstituted by iodide that acted as an inhibitor of catalysis. A recent structure of anoxically isolated nitrous oxide reductase from Pseudomonas stutzeri revealed the bridging ligand to be sulfi de, S 2-, and showed an unprecedented side-on mode of nitrous oxide binding to this form of Cu Z .

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Abiotic nitrous oxide emission from the hypersaline Don Juan Pond in Antarctica

Cited by 143 publications

References 26 publications

Microbial life at −13 °C in the brine of an ice-sealed Antarctic lake

Microbial life at −13 °C in the brine of an ice-sealed Antarctic lake

Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota

Nature’s way of handling a greenhouse gas: the copper-sulfur cluster of purple nitrous oxide reductase

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