Autotrophic Ammonia Oxidation at Low pH through Urea Hydrolysis

Burton, Simon A. Q.; Prosser, Jim

doi:10.1128/aem.67.7.2952-2957.2001

Cited by 187 publications

(130 citation statements)

References 36 publications

(35 reference statements)

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“…Keeping spatial and temporal variability and the limited duration of our experiments in mind, it is nevertheless instructive to use our results to estimate the potential overall impact of acidification on marine nitrification and associated nitrogen cycle processes. All published data indicate that ammonia oxidation slows as pH decreases (8,(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30)(31)(32), and our results are no different: Across multiple experiments conducted in high and low productivity regions of two oceans (Fig. 1), ammonia oxidation rates declined by 8-38% (Figs.…”

Section: Resultsmentioning

confidence: 46%

“…Although sensitivity to pH change is a long-recognized characteristic of nitrification (20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30)(31)(32), little information is available for marine organisms and ecosystems, and these few studies have manipulated pH by >0. 4 (8, 29).…”

Section: Resultsmentioning

confidence: 99%

“…In contrast, laboratory-and field-based studies indicate that reduced pH has a nearly universal detrimental effect on nitrification, with lower ammonia oxidation rates and slower AOB growth rates occurring under reduced pH in freshwater (20), soils (21,22), activated sludge (23)(24)(25), and bacterial cultures (26)(27)(28)(29)(30)(31)(32). Reduced pH can inhibit AOB and AOA because uncharged ammonia (NH 3 )-rather than NH 4 + ion-is the substrate used (28,29).…”

mentioning

confidence: 99%

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Global declines in oceanic nitrification rates as a consequence of ocean acidification

Beman

Chow

King

et al. 2010

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

315

260

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Ocean acidification produced by dissolution of anthropogenic carbon dioxide (CO 2 ) emissions in seawater has profound consequences for marine ecology and biogeochemistry. The oceans have absorbed one-third of CO 2 emissions over the past two centuries, altering ocean chemistry, reducing seawater pH, and affecting marine animals and phytoplankton in multiple ways. Microbially mediated ocean biogeochemical processes will be pivotal in determining how the earth system responds to global environmental change; however, how they may be altered by ocean acidification is largely unknown. We show here that microbial nitrification rates decreased in every instance when pH was experimentally reduced (by 0.05-0.14) at multiple locations in the Atlantic and Pacific Oceans. Nitrification is a central process in the nitrogen cycle that produces both the greenhouse gas nitrous oxide and oxidized forms of nitrogen used by phytoplankton and other microorganisms in the sea; at the Bermuda Atlantic Time Series and Hawaii Ocean Time-series sites, experimental acidification decreased ammonia oxidation rates by 38% and 36%. Ammonia oxidation rates were also strongly and inversely correlated with pH along a gradient produced in the oligotrophic Sargasso Sea (r 2 = 0.87, P < 0.05). Across all experiments, rates declined by 8-38% in low pH treatments, and the greatest absolute decrease occurred where rates were highest off the California coast. Collectively our results suggest that ocean acidification could reduce nitrification rates by 3-44% within the next few decades, affecting oceanic nitrous oxide production, reducing supplies of oxidized nitrogen in the upper layers of the ocean, and fundamentally altering nitrogen cycling in the sea.A tmospheric carbon dioxide (CO 2 ) concentrations are projected to double over the next century as human societies continue to burn fossil fuels and biomass (1), yet a large proportion of emitted anthropogenic CO 2 will dissolve in the ocean rather than accumulate in the atmosphere (1-4). Dissolution of CO 2 in seawater produces a weak acid that has decreased surface ocean pH by ∼0.1 below preindustrial levels, and an additional 0.3-0.4 decline is expected by the year 2100 (2, 4). This more than twofold increase in surface ocean hydrogen ion concentrations [H + ] will be accompanied by increasing CO 2 partial pressures (pCO 2 ), increasing bicarbonate ion concentrations [HCO 3 − ], decreasing carbonate ion concentrations [CO 3 2− ], and multiple shifts in trace metal and nutrient chemistry (2-4). Predicting the responses of marine organisms, ecosystems, and biogeochemical processes to these fundamental changes in ocean chemistry is consequently a major scientific challenge (5-9). Although marine bacteria and archaea constitute the majority of biomass in the sea, sustain a large percentage of global primary production, and govern biogeochemical cycling of carbon and nitrogen (10), we lack a clear understanding of how they will react to ocean acidification (9, 11).In an acidifying ocean, microbial comm...

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Section: Resultsmentioning

confidence: 46%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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Global declines in oceanic nitrification rates as a consequence of ocean acidification

Beman

Chow

King

et al. 2010

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

315

260

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“…These findings suggest that polar MGI Archaea, in addition to ammonia, may exploit some organic compounds to supplement their growth, as found for the thaumarchaeon Nitrososphaera viennensis (55) or some ammonia oxidizing bacteria (58). Interestingly, urea serves as a source of nitrogen and also carbon for certain ammonia oxidizing bacteria in soil (59,60). The detectable in situ incorporation of 14 C-labeled urea shows that the carbon of urea was assimilated by polar prokaryotes (Fig.…”

Section: Quantification Of Amoa and Urec Gene Abundances In Arctic Andmentioning

confidence: 94%

Role for urea in nitrification by polar marine Archaea

Alonso‐Sáez

Waller

Mende

et al. 2012

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

244

231

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Despite the high abundance of Archaea in the global ocean, their metabolism and biogeochemical roles remain largely unresolved. We investigated the population dynamics and metabolic activity of Thaumarchaeota in polar environments, where these microorganisms are particularly abundant and exhibit seasonal growth. Thaumarchaeota were more abundant in deep Arctic and Antarctic waters and grew throughout the winter at surface and deeper Arctic halocline waters. However, in situ single-cell activity measurements revealed a low activity of this group in the uptake of both leucine and bicarbonate (<5% Thaumarchaeota cells active), which is inconsistent with known heterotrophic and autotrophic thaumarchaeal lifestyles. These results suggested the existence of alternative sources of carbon and energy. Our analysis of an environmental metagenome from the Arctic winter revealed that Thaumarchaeota had pathways for ammonia oxidation and, unexpectedly, an abundance of genes involved in urea transport and degradation. Quantitative PCR analysis confirmed that most polar Thaumarchaeota had the potential to oxidize ammonia, and a large fraction of them had urease genes, enabling the use of urea to fuel nitrification. Thaumarchaeota from Arctic deep waters had a higher abundance of urease genes than those near the surface suggesting genetic differences between closely related archaeal populations. In situ measurements of urea uptake and concentration in Arctic waters showed that small-sized prokaryotes incorporated the carbon from urea, and the availability of urea was often higher than that of ammonium. Therefore, the degradation of urea may be a relevant pathway for Thaumarchaeota and other microorganisms exposed to the low-energy conditions of dark polar waters.amoA | ureC | Beaufort Sea | Ross Sea | Amundsen Sea

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“…According to Suzuki et al (1974), the NH 3 concentration as substrate for the ammonia monooxygenase enzyme decreases exponentially compared to NH 4 + as pH declines. In contrast to NH 3 , uptake of NH 4 + by microorganisms requires an active, energy-consuming mechanism of membrane transport, and therefore an energy source which may be limited at lower pH value (Burton and Prosser 2001). Baggs et al (2010) found a pH-induced change in the source strength of N 2 O production in soils.…”

Section: Nitrous Oxide Emissionsmentioning

confidence: 99%

Effects of anaerobic digestion on soil carbon and nitrogen turnover, N emissions, and soil biological activity. A review

Möller¹

2015

Agron. Sustain. Dev.

230

139

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Sustainability in agriculture means the inclusion of several aspects, as sustainable agriculture systems must not compromise not only their ability to satisfy future needs by undermining soil fertility and the natural resource base but also sustainable agriculture has had to address a range of other issues including energy use, efficient use, and recycling of nutrients, the effects on adjacent ecosystems including the effects on water bodies and climate change. Organic manures are an important factor to keep the soil fertility level of soils. However, their management is often related to large emissions. In this context, anaerobic digestion is-similarly to composting-a treatment option for stabilization of biogenic wastes leading to a residual product called digestates, enabling the sanitation and the recycling and use as fertilizer. It is also a means to obtain energy from wastes as well as from dedicated energy crops. Therefore, anaerobic digestion potentially addresses several aspects of agricultural sustainability. This review discusses the current state of knowledge on the effects of anaerobic digestion on organic compounds in digestates and the most important processes influencing N emissions in the field, as well as the possible longterm effects on soil microbial biomass and soil fertility. The main findings are that (1) the direct effects of anaerobic digestion on long-term sustainability in terms of soil fertility and environmental impact at the field level are of minor relevance. (2) The most relevant effects of anaerobic digestion on soil fertility as well as on N emissions will be expected from indirect effects related to cropping system changes such as changes in crop rotation, crop acreage, cover cropping, and total amounts of organic manures including digestates. Furthermore, (3) the remaining organic fraction after anaerobic digestion is much more recalcitrant than the input feedstocks leading to a stabilization of the organic matter and a lower organic matter degradation rate after field application, enabling a similar reproduction of the soil organic matter as obtained by direct application of the feedstock or by composting of the feedstock. (4) Regarding emissions, the main direct effect of anaerobic digestion on a farm level is the influence on gaseous emissions during manure or digestate treatment and handling, whereas the direct effects of anaerobic digestion on a field level on emissions (NH 3 − and N 2 O − emissions, NO 3 -leaching) are negligible or at least ambiguous. (5) The main direct effects of anaerobic digestion on the field level are short-term effects on soil microbial activity and changes in the soil microbial community. Therefore, in terms of the effects on agricultural sustainability, potential cropping system-based changes induced by introduction of biogas plants are probably much more relevant for the overall performance and sustainability of the cropping system than the direct effects triggered by application of digestates in comparison to the undigested feedstock...

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Autotrophic Ammonia Oxidation at Low pH through Urea Hydrolysis

Cited by 187 publications

References 36 publications

Global declines in oceanic nitrification rates as a consequence of ocean acidification

Global declines in oceanic nitrification rates as a consequence of ocean acidification

Role for urea in nitrification by polar marine Archaea

Effects of anaerobic digestion on soil carbon and nitrogen turnover, N emissions, and soil biological activity. A review

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