Ammonia availability shapes the seasonal distribution and activity of archaeal and bacterial ammonia oxidizers in the Puget Sound Estuary

Urakawa, Hidetoshi; Martens‐Habbena, Willm; Huguet, Carme; Torre, José R. de la; Ingalls, Anitra E.; Devol, Allan H.; Stahl, David A.

doi:10.4319/lo.2014.59.4.1321

Cited by 40 publications

(27 citation statements)

References 46 publications

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“…We also calculated per cell NH 1 4 oxidation rates for each individual sample for which both NH 1 4 oxidation rates and amoA gene abundance data were available. Per cell NH 1 4 oxidation rate ranged from 0.1 to 2.1 fmol cell 21 d 21 , and was similar to rates measured in other field experiments (0.2-15 fmol cell 21 d 21 in Santoro et al [2010], 0.10-5.96 fmol cell 21 d 21 in Urakawa et al [2014], 0.1-4.1 fmol cell 21 d 21 in Peng et al [2015]), but on the lower range of those determined in culture (1.8-15.4 fmol cell 21 d 21 in Konneke et al [2005]; 2-4 fmol cell 21 d 21 in Wuchter et al [2006]).…”

Section: 1002/2015jc011455supporting

confidence: 88%

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Revisiting nitrification in the Eastern Tropical South Pacific: A focus on controls

et al. 2016

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Nitrification, the oxidation of ammonium ( NH4+) to nitrite ( NO2−) and to nitrate ( NO3−), is a component of the nitrogen (N) cycle internal to the fixed N pool. In oxygen minimum zones (OMZs), which are hotspots for oceanic fixed N loss, nitrification plays a key role because it directly supplies substrates for denitrification and anaerobic ammonia oxidation (anammox), and may compete for substrates with these same processes. However, the control of oxygen and substrate concentrations on nitrification are not well understood. We performed onboard incubations with 15N‐labeled substrates to measure rates of NH4+ and NO2− oxidation in the eastern tropical South Pacific (ETSP). The spatial and depth distributions of NH4+ and NO2− oxidation rates were primarily controlled by NH4+ and NO2− availability, oxygen concentration, and light. In the euphotic zone, nitrification was partially photoinhibited. In the anoxic layer, NH4+ oxidation was negligible or below detection, but high rates of NO2− oxidation were observed. NH4+ oxidation displayed extremely high affinity for both NH4+ and oxygen. The positive linear correlations between NH4+ oxidation rates and in situ NH4+ concentrations and ammonia monooxygenase subunit A (amoA) gene abundances in the upper oxycline indicate that the natural assemblage of ammonia oxidizers responds to in situ NH4+ concentrations or supply by adjusting their population size, which determines the NH4+ oxidation potential. The depth distribution of archaeal and bacterial amoA gene abundances and N2O concentration, along with independently reported simultaneous direct N2O production rate measurements, suggests that AOA were predominantly responsible for NH4+ oxidation, which was a major source of N2O production at oxygen concentrations > 5 µM.

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Section: 1002/2015jc011455supporting

confidence: 88%

“…[], 0.10–5.96 fmol cell −1 d −1 in Urakawa et al . [], 0.1–4.1 fmol cell −1 d −1 in Peng et al . []), but on the lower range of those determined in culture (1.8–15.4 fmol cell −1 d −1 in Konneke et al .…”

Section: Discussionmentioning

confidence: 88%

Revisiting nitrification in the Eastern Tropical South Pacific: A focus on controls

et al. 2016

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“…Despite the lack of direct measurements of AOA ammonia oxidation in the environment, several lines of evidence suggested their global importance to nitrification, particularly in nutrient‐depleted systems typical of large parts of the global oceans. AOA vastly outnumber AOB in these environments and transcripts from genes coding for the AMO are dominated by thaumarchaeal sequences, implicating AOA as significant contributors to in situ nitrification (Wuchter et al ., ; Beman et al ., ; Löscher et al ., ; Horak et al ., ; Urakawa et al ., ). These molecular inferences of AOA primacy was supported by our earlier physiological characterization of SCM1, demonstrating that this organism is particularly well adapted to environments of sub‐micromolar ammonium (Martens‐Habbena et al ., ).…”

Section: Discussionmentioning

confidence: 97%

“…These molecular inferences of AOA primacy was supported by our earlier physiological characterization of SCM1, demonstrating that this organism is particularly well adapted to environments of sub‐micromolar ammonium (Martens‐Habbena et al ., ). This physiology is also consistent with ammonia oxidation kinetics and AOA abundance patterns we previously reported for one of our field sites, Hood Canal, a highly productive coastal system in the Puget Sound Estuary (Urakawa et al ., 2010; 2014; Horak et al ., ). Demonstration in this study of an in situ response to PTIO and ATU that is comparable with that of AOA in culture provides more direct attribution, indicating at least 95% of the bulk ammonia oxidation rate in Hood Canal and Ocean Station Papa water columns was mediated by AOA.…”

Section: Discussionmentioning

confidence: 99%

The production of nitric oxide by marine ammonia‐oxidizing archaea and inhibition of archaeal ammonia oxidation by a nitric oxide scavenger

Martens‐Habbena

Qin

Horak

et al. 2015

Environmental Microbiology

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Nitrification is a critical process for the balance of reduced and oxidized nitrogen pools in nature, linking mineralization to the nitrogen loss processes of denitrification and anammox. Recent studies indicate a significant contribution of ammonia-oxidizing archaea (AOA) to nitrification. However, quantification of the relative contributions of AOA and ammonia-oxidizing bacteria (AOB) to in situ ammonia oxidation remains challenging. We show here the production of nitric oxide (NO) by Nitrosopumilus maritimus SCM1. Activity of SCM1 was always associated with the release of NO with quasi-steady state concentrations between 0.05 and 0.08 μM. NO production and metabolic activity were inhibited by the nitrogen free radical scavenger 2-phenyl-4,4,5,5,-tetramethylimidazoline-1-oxyl-3-oxide (PTIO). Comparison of marine and terrestrial AOB strains with SCM1 and the recently isolated marine AOA strain HCA1 demonstrated a differential sensitivity of AOB and AOA to PTIO and allylthiourea (ATU). Similar to the investigated AOA strains, bulk water column nitrification at coastal and open ocean sites with sub-micromolar ammonia/ammonium concentrations was inhibited by PTIO and insensitive to ATU. These experiments support predictions from kinetic, molecular and biogeochemical studies, indicating that marine nitrification at low ammonia/ammonium concentrations is largely driven by archaea and suggest an important role of NO in the archaeal metabolism.

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“…therein). A co‐occurrence of micromolar nitrite and oxygen is observed occasionally in other environments, including diverse coastal ecosystems as a result of Thaumarchaeota ammonia‐oxidizer blooms (Pitcher et al ; Hollibaugh et al ; Urakawa et al ) and as transient occurrences due, for example, to mixing events, with a lifetime on the order of days (Mordy et al ; De Brabandere et al ). However, in other hypoxic shelf waters, nitrite typically remains below 1 μmol L –1 (Dale et al , ; Galán et al ), with higher levels only reached, with nitrate reduction as the source, when oxygen approaches complete depletion (Naqvi et al ; Füssel et al ; Galán et al ).…”

Section: Discussionmentioning

confidence: 99%

Biogeochemical and metagenomic analysis of nitrite accumulation in the Gulf of Mexico hypoxic zone

Bristow

Sarode

Cartee

et al. 2015

Limnology & Oceanography

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The Louisiana Shelf in the Gulf of Mexico experiences recurrent bottom water hypoxia under summertime eutrophic conditions. The onset, maintenance, and breakdown of hypoxia are associated with dynamic microbial biogeochemical cycles. However, the distribution of microbial taxa and metabolisms across Shelf oxygen gradients remains under-characterized. We combined biogeochemical analyses of nitrogen (N) distributions and metabolic rates with metagenomic and metatranscriptomic analysis of summertime Shelf waters. Samples from an east-west transect during July 2012 revealed an inverse relationship between nitrite and oxygen concentrations, with concentrations exceeding 1 lmol L 21 at 50% oxygen saturation and reaching 4.6 lmol L 21 at the most oxygen-depleted sites. Historical data confirms that nitrite accumulation occurs frequently in this region both above and below the hypoxic threshold. Experimental incubations demonstrated a strong decoupling between the two steps of nitrification, with ammonia oxidation proceeding up to 30 times faster than nitrite oxidation under low oxygen. 16S rRNA gene, metagenome, and metatranscriptome sequencing revealed a diverse microbial community, stratified over shallow (< 10 m) depth gradients, with an enrichment of ammonia-oxidizing Thaumarchaeota genes and transcripts in deeper more oxygendepleted layers, and a comparatively low representation of sequences related to nitrite oxidation. A range of factors, including temperature and substrate availability, which may be linked indirectly to bottom water oxygen content, potentially drives decoupling of ammonia and nitrite oxidation on the Louisiana Shelf. Nitrite accumulation in hypoxic zones remains understudied and may have important effects on microbial nitrogen flux, algal dynamics, and production.

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Ammonia availability shapes the seasonal distribution and activity of archaeal and bacterial ammonia oxidizers in the Puget Sound Estuary

Cited by 40 publications

References 46 publications

Revisiting nitrification in the Eastern Tropical South Pacific: A focus on controls

Revisiting nitrification in the Eastern Tropical South Pacific: A focus on controls

The production of nitric oxide by marine ammonia‐oxidizing archaea and inhibition of archaeal ammonia oxidation by a nitric oxide scavenger

Biogeochemical and metagenomic analysis of nitrite accumulation in the Gulf of Mexico hypoxic zone

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