Responses of Ammonia-Oxidizing Bacterial and Archaeal Populations to Organic Nitrogen Amendments in Low-Nutrient Groundwater

Reed, David W.; Smith, Jay W.; Francis, Christopher A.; Fujita, Yoshiko

doi:10.1128/aem.02436-09

Cited by 39 publications

(27 citation statements)

References 43 publications

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“…Only a few freshwater planktonic environments have been prospected so far, but AOA have been detected in rivers (26,31), in the oligotrophic African Lake Kivu (44), in groundwater (57), and in drinking water (66). Here, we have extended the survey to ultraoligotrophic mountain lakes, showing that freshwater amoA sequences mainly formed coherent freshwater clusters (Fig.…”

Section: Discussionmentioning

confidence: 98%

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Seasonal Changes of Freshwater Ammonia-Oxidizing Archaeal Assemblages and Nitrogen Species in Oligotrophic Alpine Lakes

Auguet

Nomokonova

Camarero

et al. 2011

Appl Environ Microbiol

105

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The annual changes in the composition and abundance of ammonia-oxidizing archaea (AOA) were analyzed monthly in surface waters of three high mountain lakes within the Limnological Observatory of the Pyrenees (LOOP; northeast Spain) using both 16S rRNA and functional (ammonia monooxygenase gene, amoA) gene sequencing as well as quantitative PCR amplification. The set of biological data was related to changes in nitrogen species and to other relevant environmental variables. The whole archaeal assemblage was dominated by phylotypes closely related to the crenarchaeal 1.1a group (58% ؎ 18% of total 16S rRNA gene sequences), and consistent structural changes were detected during the study. Water temperature was the environmental variable that better explained spring, summer, and winter (ice-covered lakes) archaeal assemblage structure. The amoA gene was detected year round, and seasonal changes in amoA gene composition were well correlated with changes in the archaeal 16S rRNA gene pool. In addition, copy numbers of both the specific 1.1a group 16 rRNA and archaeal amoA genes were well correlated, suggesting that most freshwater 1.1a Crenarchaeota had the potential to carry out ammonia oxidation. Seasonal changes in the diversity and abundance of AOA (i.e., amoA) were better explained by temporal changes in ammonium, the substrate for nitrification, and mostly nitrite, the product of ammonia oxidation. Lacustrine amoA gene sequences grouped in coherent freshwater phylogenetic clusters, suggesting that freshwater habitats harbor typical amoA-containing ecotypes, which is different from soils and seas. We observed within the freshwater amoA gene sequence pool a high genetic divergence (translating to up to 32% amino acid divergence) between the spring and the remaining AOA assemblages. This suggests that different AOA ecotypes are adapted to different temporal ecological niches in these lakes.For almost 30 years, the ubiquity of nitrification, particularly in the most oligotrophic environments, had constituted an enigma for ecologists (28,52). First, because of very low natural abundances of ammonia-oxidizing bacteria (AOB), the a priori unique microorganisms with the potential to catalyze the first step of nitrification had been reported (e.g., 0.1% of total bacterial assemblage in oceanic habitats) (9, 38), and second, because field measurements indicated that the oxidation of ammonia (NH 4 ϩ ) to nitrate was feasible in situ even in the most oligotrophic habitats, where NH 4 ϩ concentrations were below the affinity threshold for AOB (8). Five years ago, metagenomics provided an answer to the enigma and radically changed the general perception of the nitrification process (65, 67). The presence of putative ammonia monooxygenase subunits (amoA, amoB, and amoC) within the genomes of widespread and abundant microorganisms of the domain Archaea (65, 67), as well as the chemolithoautotrophic growth using ammonia as an energy source observed in the recently isolated Crenarchaeota Nitrosopumilus maritimus (37), has fuelled...

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Section: Discussionmentioning

confidence: 98%

“…4). Indeed, the closest relatives in GenBank for most of the recovered amoA sequences were obtained from rhizosphere, groundwater, and drinking waters (33,57,66) (Table 3).…”

Section: Seasonal Environmental Changesmentioning

confidence: 99%

Seasonal Changes of Freshwater Ammonia-Oxidizing Archaeal Assemblages and Nitrogen Species in Oligotrophic Alpine Lakes

Auguet

Nomokonova

Camarero

et al. 2011

Appl Environ Microbiol

105

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“…For both groups, the gene encoding the alpha-subunit of ammonia monooxygenase (amoA) has been widely used as a functional marker to analyze their community compositions. Recent studies demonstrated the wide distribution of AOA in aqueous environments by its existence in members of the Thaumarchaea I.1a (also named Marine Group I) or I.1b, showing the AOA predominance over AOB in a broad range of environments (Herrmann et al, 2009;Reed et al, 2010;Cao et al, 2011;Isobe et al, 2012). Environmental elements such as pH, ammonia and dissolved oxygen (DO) concentrations, are important factors which define the differences between AOA and AOB in distinct ecological niches (Altmann et al, 2004;Erguder et al, 2009;Herrmann et al, 2011;Bouskill et al, 2012;Vissers et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Spatial distribution of ammonia-oxidizing archaea and bacteria across eight freshwater lakes in sediments from Jiangsu of China

et al. 2014

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“…S4 in the supplemental material). Here, sequences formed a cluster together with sequences obtained from groundwater (32) and from a drinking water distribution system (41), which may point to a special affiliation of this group with freshwater environments. However, we did not detect novel AOA AmoA clusters that would indicate the existence of special creek-associated AOA.…”

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confidence: 99%

Ammonium Availability Affects the Ratio of Ammonia-Oxidizing Bacteria to Ammonia-Oxidizing Archaea in Simulated Creek Ecosystems

Herrmann

Scheibe

Avrahami

et al. 2011

Appl Environ Microbiol

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The ammonia-oxidizing microbial community colonizing clay tiles in flow channels changed in favor of ammonia-oxidizing bacteria during a 12-week incubation period even at originally high ratios of ammoniaoxidizing archaea to ammonia-oxidizing bacteria (AOB). AOB predominance was established more rapidly in flow channels incubated at 350 M NH 4 ؉ than in those incubated at 50 or 20 M NH 4 ؉ . Biofilm-associated potential nitrification activity was first detected after 28 days and was positively correlated with bacterial but not archaeal amoA gene copy numbers.Nitrogen transformation processes in small-river ecosystems are primarily associated with the sediment or epilithic biofilms (4,5,18). Here, nitrification as the first step in coupled nitrification-denitrification is a key step in the removal of the allochthonous nitrogen load, preventing the eutrophication of downstream ecosystems (1,5,29,39). The activity and community composition of biofilm-associated nitrifying microorganisms have been investigated extensively in wastewater treatment systems (27,36), in drinking water distribution systems (17, 41), and in lakes, large rivers, and estuaries (7,19,21,39) but only rarely in small-creek ecosystems. The first and ratelimiting step in nitrification, oxidation of ammonia, is carried out by ammonia-oxidizing archaea (AOA) (14) and ammoniaoxidizing bacteria (AOB) (16). Molecular surveys targeting the amoA gene, which encodes catalytic subunit A of ammonia monooxygenase, the key enzyme of ammonia oxidation (33), as well as cultivation-based studies, indicated that pH (26), salinity (25, 34), and especially ammonium availability (6, 22) could play important roles in the ecological niche differentiation of AOA and AOB. However, only little is known about archaeal versus bacterial ammonia oxidizers in creek or river ecosystems or about the association of AOA with biofilms (37,43). In this study, we used flow channels (FC) as simulated creek ecosystems to investigate the influence of ammonium availability (i) on the establishment of biofilm-associated nitrification activity, (ii) on the community composition of biofilm-associated AOA and AOB, and (iii) on temporal patterns of the abundance of AOA and AOB during a 12-week incubation period.FC experiment. Water for FC was obtained from three shell limestone creeks (Ammerbach, Leutra South, and Leutra North) located near the city of Jena (Thuringia, Germany). The creeks differed in their nutrient concentrations, with the highest nutrient load at Ammerbach resulting from diffuse wastewater inputs (Table 1). Flow velocities ranged from 0.105 Ϯ 0.092 to 0.230 Ϯ 0.224 m s Ϫ1 . Plexiglas FC measuring 160 by 10 by 18 cm (see Fig. S1 in the supplemental material) were set up in triplicate for each creek. Concentrations of NH 4 ϩ in the water phase of the FC were adjusted to 350 mol liter Ϫ1 (Ammerbach; FC 1 to 3), 50 mol liter Ϫ1 (Leutra South, FC 4 to 6), and 20 mol liter Ϫ1 (Leutra North, FC 7 to 9) to run the experiment at three distinct levels of NH 4 ϩ . pHs and concentrat...

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Responses of Ammonia-Oxidizing Bacterial and Archaeal Populations to Organic Nitrogen Amendments in Low-Nutrient Groundwater

Cited by 39 publications

References 43 publications

Seasonal Changes of Freshwater Ammonia-Oxidizing Archaeal Assemblages and Nitrogen Species in Oligotrophic Alpine Lakes

Seasonal Changes of Freshwater Ammonia-Oxidizing Archaeal Assemblages and Nitrogen Species in Oligotrophic Alpine Lakes

Spatial distribution of ammonia-oxidizing archaea and bacteria across eight freshwater lakes in sediments from Jiangsu of China

Ammonium Availability Affects the Ratio of Ammonia-Oxidizing Bacteria to Ammonia-Oxidizing Archaea in Simulated Creek Ecosystems

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