Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic.

Department of Biological Oceanography, Royal Netherlands Institute for Sea Research (Royal NIOZ), PO Box 59, 1790 AB Den Burg, Texel, The Netherlands.
Nature (Impact Factor: 38.6). 12/2008; 456(7223):788-91. DOI: 10.1038/nature07535
Source: PubMed

ABSTRACT Aerobic nitrification of ammonia to nitrite and nitrate is a key process in the oceanic nitrogen cycling mediated by prokaryotes. Apart from Bacteria belonging to the beta- and gamma-Proteobacteria involved in the first nitrification step, Crenarchaeota have recently been recognized as main drivers of the oxidation of ammonia to nitrite in soil as well as in the ocean, as indicated by the dominance of archaeal ammonia monooxygenase (amoA) genes over bacterial amoA. Evidence is accumulating that archaeal amoA genes are common in a wide range of marine systems. Essentially, all these reports focused on surface and mesopelagic (200-1,000 m depth) waters, where ammonia concentrations are higher than in waters below 1,000 m depth. However, Crenarchaeota are also abundant in the water column below 1,000 m, where ammonia concentrations are extremely low. Here we show that, throughout the North Atlantic Ocean, the abundance of archaeal amoA genes decreases markedly from subsurface waters to 4,000 m depth, and from subpolar to equatorial deep waters, leading to pronounced vertical and latitudinal gradients in the ratio of archaeal amoA to crenarchaeal 16S ribosomal RNA (rRNA) genes. The lack of significant copy numbers of amoA genes and the very low fixation rates of dark carbon dioxide in the bathypelagic North Atlantic suggest that most bathypelagic Crenarchaeota are not autotrophic ammonia oxidizers: most likely, they utilize organic matter and hence live heterotrophically.

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    ABSTRACT: Previous studies had suggested the presence of ammonium oxidizing Thaumarchaeota as well as nitrite oxidizing Bacteria in the subsurface spring called Franz Josef Quelle (FJQ), a slightly radioactive thermal mineral spring with a temperature of 43.6-47°C near the alpine village of Bad Gastein, Austria. The microbiological consortium of the FJQ was investigated for its utilization of nitrogen compounds and the putative presence of a subsurface nitrogen cycle. Microcosm experiments made with samples from the spring water, containing planktonic microorganisms, or from biofilms, were used in this study. Three slightly different media, enriched with vitamins and trace elements, and two incubation temperatures (30 and 40°C, respectively) were employed. Under aerobic conditions, high rates of conversion of ammonium to nitrite, as well as nitrite to nitrate were measured. Under oxygen-limited conditions nitrate was converted to gaseous compounds. Stable isotope probing with (15)NH4Cl or ((15)NH4)2SO4as sole energy sources revealed incorporation of (15)N into community DNA. Genomic DNA as well as RNA were extracted from all microcosms. The following genes or fragments of genes were successfully amplified, cloned and sequenced by standard PCR from DNA extracts: Ammonia monooxygenase subunit A (amoA), nitrite oxidoreductase subunits A and B (nxrA and nxrB), nitrate reductase (narG), nitrite reductase (nirS), nitric oxide reductases (cnorB and qnorB), nitrous oxide reductase (nosZ). Reverse transcription of extracted total RNA and real-time PCR suggested the expression of each of those genes. Nitrogen fixation (as probed with nifH and nifD) was not detected. However, a geological origin of NH(+) 4 in the water of the FJQ cannot be excluded, considering the silicate, granite and gneiss containing environment. The data suggested the operation of a nitrogen cycle in the subsurface environment of the FJQ.
    Frontiers in microbiology. 01/2014; 5:225.
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    ABSTRACT: 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 release of NO with quasi-steady state concentrations between 0.05 and 0.08 μM. Nitric oxide 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.
    Environmental Microbiology 10/2014; · 6.24 Impact Factor
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    ABSTRACT: Ammonia-oxidizing archaea (AOA) are now implicated in exerting significant control over the form and availability of reactive nitrogen species in marine environments. Detailed studies of specific metabolic traits and physicochemical factors controlling their activities and distribution have not been well constrained in part due to the scarcity of isolated AOA strains. Here, we report the isolation of two new coastal marine AOA, strains PS0 and HCA1. Comparison of the new strains to Nitrosopumilus maritimus strain SCM1, the only marine AOA in pure culture thus far, demonstrated distinct adaptations to pH, salinity, organic carbon, temperature, and light. Strain PS0 sustained nearly 80% of ammonia oxidation activity at a pH as low as 5.9, indicating that coastal strains may be less sensitive to the ongoing reduction in ocean pH. Notably, the two novel isolates are obligate mixotrophs that rely on uptake and assimilation of organic carbon compounds, suggesting a direct coupling between chemolithotrophy and organic matter assimilation in marine food webs. All three isolates showed only minor photoinhibition at 15 µE⋅m(-2)⋅s(-1) and rapid recovery of ammonia oxidation in the dark, consistent with an AOA contribution to the primary nitrite maximum and the plausibility of a diurnal cycle of archaeal ammonia oxidation activity in the euphotic zone. Together, these findings highlight an unexpected adaptive capacity within closely related marine group I Archaea and provide new understanding of the physiological basis of the remarkable ecological success reflected by their generally high abundance in marine environments.
    Proceedings of the National Academy of Sciences 08/2014; · 9.81 Impact Factor