Agogué H, Brink M, Dinasquet J, Herndl GJ.. Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 456: 788-791

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: 41.46). 12/2008; 456(7223):788-91. DOI: 10.1038/nature07535
Source: PubMed


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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    • "c o m / l o c a t e / o r g g e o c h e m the domain Archaea (formerly known as Group I Crenarchaeota; Brochiet-Armanet et al., 2008), even though it has been recently suggested that it could also be produced by Marine Group II Euryarchaeota (Lincoln et al., 2014). Thaumarchaeota are among the most abundant oceanic microorganisms (Karner et al., 2001; Agogué et al., 2008). Schouten et al. (2002) showed that the relative distribution of iGDGTs in Thaumarchaeota depends on environmental conditions, the number of cyclopentyl moieties increasing with sea surface temperature (SST). "
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    ABSTRACT: The occurrence and distribution of archaeal and bacterial glycerol dialkyl glycerol tetraether lipids (GDGTs) in continental saline environments have been rarely investigated. Here, the abundance and distribution of archaeal isoprenoid GDGTs (iGDGTs) and archaeol, and of bacterial branched GDGTs (brGDGTs) in four tropical water ponds of contrasting salinity in two islands from the French Western Indies, Grande-Terre and La Désirade, have been determined. The sedimentary distribution of the GDGTs strongly differed between the two islands. Caldarchaeol was largely predominant among iGDGTs in the (hyper)saline ponds from Grande-Terre, suggesting a substantial contribution of iGDGTs derived from methanogenic Archaea. In contrast, both caldarchaeol and crenarchaeol were present in high relative abundance in the low salinity ponds from La Désirade, suggesting that iGDGTs were derived from mixed archaeal communities. In addition, the relative proportion of the most methylated brGDGTs was much higher in Grande-Terre ponds than in La Désirade ponds. The applicability of different proxies based on GDGTs and archaeol was tested for these specific environments. The relative abundance of archaeol vs. caldarchaeol (ACE index) was comparable for the four ponds, independent of salinity, showing that the ACE might not necessarily track salinity change. Moreover, the relative proportion of caldarchaeol vs. total iGDGTs was unexpectedly observed to increase with salinity, suggesting production of this compound by halophilic Archaea. The supposed high abundance of methanogenic Archaea in Grande-Terre ponds prevented the application of TEX86 as a temperature proxy, whereas the TEX86 could be successfully used for local temperature reconstruction in La Désirade ponds. BrGDGTs seem to be produced predominantly in situ (water column and/or sediment) in hypersaline ponds from Grande-Terre, but in La Désirade ponds likely result from a mixture of soil and aquatic sources. In Grande-Terre ponds, brGDGT-derived temperature estimates generated using either soil or lacustrine calibrations were much lower than expected. The mismatch between expected and estimated temperature might be explained by the presence of halophilic microbial communities producing specific brGDGT distributions in the saline ponds from Grande-Terre. The study shows that the sources of brGDGTs, iGDGTs and archaeol (i) may strongly differ in aquatic environments of varying salinity, even at a regional scale, and (ii) have to be constrained before tetraether-derived proxies in such settings can be confidently applied.
    Full-text · Article · Mar 2015 · Organic Geochemistry
    • "The relative contributions to ammonia oxidation by autotrophic AOA and ammonia-oxidizing bacteria (AOB) have been inferred using the archaeal and bacterial amoA genes that encode subunit A of the key enzyme ammonia monooxygenase (see, for example, Rotthauwe et al., 1997; De Corte et al., 2009; Sauder et al., 2011; Auguet et al., 2012). These studies often revealed the dominance of archaeal over bacterial ammonia oxidizers (Francis et al., 2005; Wuchter et al., 2006; Mincer et al., 2007; Agogué et al., 2008; Newell et al., 2013). Further support for the strong role for AOA in nitrification comes from observations of the co-occurrence of archaeal amoA in areas of nitrification activity (Caffrey et al., 2007; Beman et al., 2008; Alves et al., 2013) and from metatranscriptomic studies (Baker et al., 2012; Lesniewski et al., 2012). "
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    ABSTRACT: Ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread, and their abundance in many terrestrial and aquatic ecosystems suggests a prominent role in nitrification. AOA also occur in high numbers in oxygen-deficient marine environments, such as the pelagic redox gradients of the central Baltic Sea; however, data on archaeal nitrification rates are scarce and little is known about the factors, for example sulfide, that regulate nitrification in this system. In the present work, we assessed the contribution of AOA to ammonia oxidation rates in Baltic deep basins and elucidated the impact of sulfide on this process. Rate measurements with 15N-labeled ammonium, CO2 dark fixation measurements and quantification of AOA by catalyzed reporter deposition–fluorescence in situ hybridization revealed that among the three investigated sites the highest potential nitrification rates (122–884 nmol l−1per day) were measured within gradients of decreasing oxygen, where thaumarchaeotal abundance was maximal (2.5–6.9 × 105 cells per ml) and CO2 fixation elevated. In the presence of the archaeal-specific inhibitor GC7, nitrification was reduced by 86–100%, confirming the assumed dominance of AOA in this process. In samples spiked with sulfide at concentrations similar to those of in situ conditions, nitrification activity was inhibited but persisted at reduced rates. This result together with the substantial nitrification potential detected in sulfidic waters suggests the tolerance of AOA to periodic mixing of anoxic and sulfidic waters. It begs the question of whether the globally distributed Thaumarchaeota respond similarly in other stratified water columns or whether the observed robustness against sulfide is a specific feature of the thaumarchaeotal subcluster present in the Baltic Deeps.
    No preview · Article · Nov 2014 · The ISME Journal
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    • "Although their contribution to soil nitrification is still under debate, recent reports were able to distinguish between the activities of ammonia-oxidizing bacteria (AOB) and AOA (Eloy Alves et al., 2013; Taylor et al., 2013). In the oceans, ammonia concentrations are extremely low (below 5 nM; Agogué et al., 2008), which led to the assumption that ammonia as an energy source is rather unlikely. However, reports of a very high affinity of AOAs to ammonia (Martens-Habbena et al., 2009) suggested that oligotrophic AOAs are equipped to compete for ammonium as energy source in nutrient-deprived waters. "
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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.
    Full-text · Article · May 2014 · Frontiers in Microbiology
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