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Global Ecological Pattern of Ammonia-Oxidizing Archaea  [PDF]
Huiluo Cao, Jean-Christophe Auguet, Ji-Dong Gu
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0052853
Abstract: Background The global distribution of ammonia-oxidizing archaea (AOA), which play a pivotal role in the nitrification process, has been confirmed through numerous ecological studies. Though newly available amoA (ammonia monooxygenase subunit A) gene sequences from new environments are accumulating rapidly in public repositories, a lack of information on the ecological and evolutionary factors shaping community assembly of AOA on the global scale is apparent. Methodology and Results We conducted a meta-analysis on uncultured AOA using over ca. 6,200 archaeal amoA gene sequences, so as to reveal their community distribution patterns along a wide spectrum of physicochemical conditions and habitat types. The sequences were dereplicated at 95% identity level resulting in a dataset containing 1,476 archaeal amoA gene sequences from eight habitat types: namely soil, freshwater, freshwater sediment, estuarine sediment, marine water, marine sediment, geothermal system, and symbiosis. The updated comprehensive amoA phylogeny was composed of three major monophyletic clusters (i.e. Nitrosopumilus, Nitrosotalea, Nitrosocaldus) and a non-monophyletic cluster constituted mostly by soil and sediment sequences that we named Nitrososphaera. Diversity measurements indicated that marine and estuarine sediments as well as symbionts might be the largest reservoirs of AOA diversity. Phylogenetic analyses were further carried out using macroevolutionary analyses to explore the diversification pattern and rates of nitrifying archaea. In contrast to other habitats that displayed constant diversification rates, marine planktonic AOA interestingly exhibit a very recent and accelerating diversification rate congruent with the lowest phylogenetic diversity observed in their habitats. This result suggested the existence of AOA communities with different evolutionary history in the different habitats. Conclusion and Significance Based on an up-to-date amoA phylogeny, this analysis provided insights into the possible evolutionary mechanisms and environmental parameters that shape AOA community assembly at global scale.
Production of oceanic nitrous oxide by ammonia-oxidizing archaea
C. R. L scher, A. Kock, M. K nneke, J. LaRoche, H. W. Bange,R. A. Schmitz
Biogeosciences (BG) & Discussions (BGD) , 2012,
Abstract: The recent finding that microbial ammonia oxidation in the ocean is performed by archaea to a greater extent than by bacteria has drastically changed the view on oceanic nitrification. The numerical dominance of archaeal ammonia-oxidizers (AOA) over their bacterial counterparts (AOB) in large parts of the ocean leads to the hypothesis that AOA rather than AOB could be the key organisms for the oceanic production of the strong greenhouse gas nitrous oxide (N2O) that occurs as a by-product of nitrification. Very recently, enrichment cultures of marine ammonia-oxidizing archaea have been reported to produce N2O. Here, we demonstrate that archaeal ammonia monooxygenase genes (amoA) were detectable throughout the water column of the eastern tropical North Atlantic (ETNA) and eastern tropical South Pacific (ETSP) Oceans. Particularly in the ETNA, comparable patterns of abundance and expression of archaeal amoA genes and N2O co-occurred in the oxygen minimum, whereas the abundances of bacterial amoA genes were negligible. Moreover, selective inhibition of archaea in seawater incubations from the ETNA decreased the N2O production significantly. In studies with the only cultivated marine archaeal ammonia-oxidizer Nitrosopumilus maritimus SCM1, we provide the first direct evidence for N2O production in a pure culture of AOA, excluding the involvement of other microorganisms as possibly present in enrichments. N. maritimus showed high N2O production rates under low oxygen concentrations comparable to concentrations existing in the oxycline of the ETNA, whereas the N2O production from two AOB cultures was comparably low under similar conditions. Based on our findings, we hypothesize that the production of N2O in tropical ocean areas results mainly from archaeal nitrification and will be affected by the predicted decrease in dissolved oxygen in the ocean.
Production of oceanic nitrous oxide by ammonia-oxidizing archaea  [PDF]
C. R. Loescher,A. Kock,M. Koenneke,J. LaRoche
Biogeosciences Discussions , 2012, DOI: 10.5194/bgd-9-2095-2012
Abstract: The recent finding that microbial ammonia oxidation in the ocean is performed by archaea to a greater extent than by bacteria has drastically changed the view on oceanic nitrification. The numerical dominance of archaeal ammonia-oxidizers (AOA) over their bacterial counterparts (AOB) in large parts of the ocean leads to the hypothesis that AOA rather than AOB could be the key organisms for the oceanic production of the strong greenhouse gas nitrous oxide (N2O) which occurs as a by-product of nitrification. Very recently, enrichment cultures of marine ammonia-oxidizing archaea have been described to produce N2O. Here, we demonstrate that archaeal ammonia monooxygenase genes (amoA) were detectable throughout the water column of the Eastern Tropical North Atlantic (ETNA) and Eastern Tropical South Pacific Oceans (ETSP). Particularly in the ETNA, maxima in abundance and expression of archaeal amoA genes correlated with the N2O maximum and the oxygen minimum, whereas the abundances of bacterial amoA genes were negligible. Moreover, selective inhibition of archaea in seawater incubations from the ETNA decreased the N2O production significantly. In studies with the only cultivated marine archaeal ammonia-oxidizer Nitrosopumilus maritimus SCM1, we provide the first direct evidence for N2O production in a pure culture of AOA, excluding the involvement of other microorganisms as possibly present in enrichments. N. maritimus showed high N2O production rates under low oxygen concentrations comparable to concentrations existing in the oxycline of the ETNA, whereas the N2O production from two AOB cultures was comparably low under similar conditions. Based on our findings, we hypothesize that the production of N2O in tropical ocean areas results mainly from archaeal nitrification and will be affected by the predicted decrease in dissolved oxygen in the ocean.
Impacts of Edaphic Factors on Communities of Ammonia-Oxidizing Archaea, Ammonia-Oxidizing Bacteria and Nitrification in Tropical Soils  [PDF]
Vidya de Gannes, Gaius Eudoxie, William J. Hickey
PLOS ONE , 2014, DOI: 10.1371/journal.pone.0089568
Abstract: Nitrification is a key process in soil nitrogen (N) dynamics, but relatively little is known about it in tropical soils. In this study, we examined soils from Trinidad to determine the edaphic drivers affecting nitrification levels and community structure of ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) in non-managed soils. The soils were naturally vegetated, ranged in texture from sands to clays and spanned pH 4 to 8. The AOA were detected by qPCR in all soils (ca. 105 to 106 copies archaeal amoA g?1 soil), but AOB levels were low and bacterial amoA was infrequently detected. AOA abundance showed a significant negative correlation (p<0.001) with levels of soil organic carbon, clay and ammonium, but was not correlated to pH. Structures of AOA and AOB communities, as determined by amoA terminal restriction fragment (TRF) analysis, differed significantly between soils (p<0.001). Variation in AOA TRF profiles was best explained by ammonium-N and either Kjeldahl N or total N (p<0.001) while variation in AOB TRF profiles was best explained by phosphorus, bulk density and iron (p<0.01). In clone libraries, phylotypes of archaeal amoA (predominantly Nitrososphaera) and bacterial amoA (predominanatly Nitrosospira) differed between soils, but variation was not correlated with pH. Nitrification potential was positively correlated with clay content and pH (p<0.001), but not to AOA or AOB abundance or community structure. Collectively, the study showed that AOA and AOB communities were affected by differing sets of edaphic factors, notably that soil N characteristics were significant for AOA, but not AOB, and that pH was not a major driver for either community. Thus, the effect of pH on nitrification appeared to mainly reflect impacts on AOA or AOB activity, rather than selection for AOA or AOB phylotypes differing in nitrifying capacity.
Distribution and Abundance of Archaea in South China Sea Sponge Holoxea sp. and the Presence of Ammonia-Oxidizing Archaea in Sponge Cells  [PDF]
Fang Liu,Minqi Han,Fengli Zhang,Baohua Zhang,Zhiyong Li
Evidence-Based Complementary and Alternative Medicine , 2011, DOI: 10.1155/2011/723696
Abstract: Compared with bacterial symbionts, little is known about archaea in sponges especially about their spatial distribution and abundance. Understanding the distribution and abundance of ammonia-oxidizing archaea will help greatly in elucidating the potential function of symbionts in nitrogen cycling in sponges. In this study, gene libraries of 16S rRNA gene and ammonia monooxygenase subunit A (amoA) genes and quantitative real-time PCR were used to study the spatial distribution and abundance of archaea in the South China Sea sponge Holoxea sp. As a result, Holoxea sp. specific AOA, mainly group C1a (marine group I: Crenarchaeota) were identified. The presence of ammonia-oxidizing crenarchaea was observed for the first time within sponge cells. This study suggested a close relationship between sponge host and its archaeal symbionts as well as the archaeal potential contribution to sponge host in the ammonia-oxidizing process of nitrification. 1. Introduction The biodiversity and biogeography of sponge microbial symbionts has received a great deal of attention, and the past 10 years has witnessed huge advances in revealing the phylogenetic diversity of sponge symbionts. Until the beginning of 2011, 30 bacterial phyla and 2 archaeal phyla have been detected in sponges [1]. However, the role of microbial symbionts remains largely unknown [2–4] and the nature of the sponge-microorganism interaction has to date only been inferred from loose correlations [2]. The present information of sponge microbial symbionts is mainly on the microorganisms in sponge mesohyl, that is, extracellular symbionts [5]. The difficulty in identifying and discriminating between intra- and extracellular symbionts has made it hard to determine the true nature of sponge-microorganism interactions. Therefore, investigation of the intracellular symbionts, which are likely “true” and “stable” symbiotic populations and may play a more significant role in the sponge biology and ecology, is very helpful for the understanding of sponge-microorganism interaction and the roles of sponge microbial symbionts. Up to now, evidence of intracellular symbionts of sponges is mainly derived from transmission electronic microscopy (TEM) visualization analyses. For example, intracellular algal symbionts in sponges were first confirmed by TEM in 1979 [6]. Using a similar approach, intracellular dinoflagellates [7], filamentous unicellular cyanobacteria [8], and yeast [9] have been observed in sponges. Furthermore, a complex bacterial consortium was revealed in Ectyoplasia ferox oocytes using fluorescent in
Metagenomic Analysis of Ammonia-Oxidizing Archaea Affiliated with the Soil Group  [PDF]
Christa Schleper
Frontiers in Microbiology , 2012, DOI: 10.3389/fmicb.2012.00208
Abstract: Ammonia-oxidizing archaea (AOA) have recently been recognized as a significant component of many microbial communities and represent one of the most abundant prokaryotic groups in the biosphere. However, only few AOA have been successfully cultivated so far and information on the physiology and genomic content remains scarce. We have performed a metagenomic analysis to extend the knowledge of the AOA affiliated with group I.1b that is widespread in terrestrial habitats and of which no genome sequences has been described yet. A fosmid library was generated from samples of a radioactive thermal cave (46°C) in the Austrian Central Alps in which AOA had been found as a major part of the microbial community. Out of 16 fosmids that possessed either an amoA or 16S rRNA gene affiliating with AOA, 5 were fully sequenced, 4 of which grouped with the soil/I.1b (Nitrososphaera-) lineage, and 1 with marine/I.1a (Nitrosopumilus-) lineage. Phylogenetic analyses of amoBC and an associated conserved gene were congruent with earlier analyses based on amoA and 16S rRNA genes and supported the separation of the soil and marine group. Several putative genes that did not have homologs in currently available marine Thaumarchaeota genomes indicated that AOA of the soil group contain specific genes that are distinct from their marine relatives. Potential cis-regulatory elements around conserved promoter motifs found upstream of the amo genes in sequenced (meta-) genomes differed in marine and soil group AOA. On one fosmid, a group of genes including amoA and amoB were flanked by identical transposable insertion sequences, indicating that amoAB could potentially be co-mobilized in the form of a composite transposon. This might be one of the mechanisms that caused the greater variation in gene order compared to genomes in the marine counterparts. Our findings highlight the genetic diversity within the two major and widespread lineages of Thaumarchaeota.
Does the nitrification inhibitor dicyandiamide affect the abundance of ammonia-oxidizing bacteria and archaea in a Hap-Udic Luvisol?  [cached]
P Gong,L Zhang,Z Wu,Z Shang
Journal of Soil Science and Plant Nutrition , 2013,
Abstract: To date, there are several studies on the responses of ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) to nitrification inhibitors, but only a limited number of observations are available for higher than regular application rates. Here, we report the results of a study investigating the responses of AOB and AOA to the nitrification inhibitor, dicyandiamide (DCD). DCD suppressed growth of AOB significantly, whereas there was no significant difference between a single or a double dose of DCD on inhibiting the growth of AOB for 91 days. AOA abundance was stable among treatments, regardless of the addition of a single or a double dose of DCD. When DCD was applied alone, the AOA abundance was not appreciably changed at day 14. The results clearly show that AOA was not sensitive to the nitrification inhibitor DCD under our experimental conditions.
Differential responses of ammonia-oxidizing archaea and bacteria to long-term fertilization in a New England salt marsh  [PDF]
Xuefeng Peng,Erik Yando,Erica Hildebrand,Courtney Dwyer,Ivan Valiela,Anne E. Bernhard
Frontiers in Microbiology , 2013, DOI: 10.3389/fmicb.2012.00445
Abstract: Since the discovery of ammonia-oxidizing archaea (AOA), new questions have arisen about population and community dynamics and potential interactions between AOA and ammonia-oxidizing bacteria (AOB). We investigated the effects of long-term fertilization on AOA and AOB in the Great Sippewissett Marsh, Falmouth, MA, USA to address some of these questions. Sediment samples were collected from low and high marsh habitats in July 2009 from replicate plots that received low (LF), high (HF), and extra high (XF) levels of a mixed NPK fertilizer biweekly during the growing season since 1974. Additional untreated plots were included as controls (C). Terminal restriction fragment length polymorphism analysis of the amoA genes revealed distinct shifts in AOB communities related to fertilization treatment, but the response patterns of AOA were less consistent. Four AOB operational taxonomic units (OTUs) predictably and significantly responded to fertilization, but only one AOA OTU showed a significant pattern. Betaproteobacterial amoA gene sequences within the Nitrosospira-like cluster dominated at C and LF sites, while sequences related to Nitrosomonas spp. dominated at HF and XF sites. We identified some clusters of AOA sequences recovered primarily from high fertilization regimes, but other clusters consisted of sequences recovered from all fertilization treatments, suggesting greater physiological diversity. Surprisingly, fertilization appeared to have little impact on abundance of AOA or AOB. In summary, our data reveal striking patterns for AOA and AOB in response to long-term fertilization, and also suggest a missing link between community composition and abundance and nitrogen processing in the marsh.
Abundance and Diversity of Ammonia-Oxidizing Archaea and Bacteria in Sediments of Trophic End Members of the Laurentian Great Lakes, Erie and Superior  [PDF]
Annette Bollmann, George S. Bullerjahn, Robert Michael McKay
PLOS ONE , 2014, DOI: 10.1371/journal.pone.0097068
Abstract: Ammonia oxidation is the first step of nitrification carried out by ammonia-oxidizing Archaea (AOA) and Bacteria (AOB). Lake Superior and Erie are part of the Great Lakes system differing in trophic status with Lake Superior being oligotrophic and Lake Erie meso- to eutrophic. Sediment samples were collected from both lakes and used to characterize abundance and diversity of AOA and AOB based on the ammonia monooxygenase (amoA) gene. Diversity was accessed by a pyro-sequencing approach and the obtained sequences were used to determine the phylogeny and alpha and beta diversity of the AOA and AOB populations. In Lake Erie copy numbers of bacterial amoA genes were in the same order of magnitude or even higher than the copy numbers of the archaeal amoA genes, while in Lake Superior up to 4 orders of magnitude more archaeal than bacterial amoA copies were detected. The AOB detected in the samples from Lake Erie belonged to AOB that are frequently detected in freshwater. Differences were detected between the phylogenetic affiliations of the AOA from the two lakes. Most sequences detected in Lake Erie clustered in the Nitrososphaera cluster (Thaumarchaeal soil group I.1b) where as most of the sequences in Lake Superior were found in the Nitrosopumilus cluster (Thaumarchaeal marine group I.1a) and the Nitrosotalea cluster. Pearson correlations and canonical correspondence analysis (CCA) showed that the differences in abundance and diversity of AOA are very likely related to the sampling location and thereby to the different trophic states of the lakes.
Genomes of Two New Ammonia-Oxidizing Archaea Enriched from Deep Marine Sediments  [PDF]
Soo-Je Park, Rohit Ghai, Ana-Belén Martín-Cuadrado, Francisco Rodríguez-Valera, Won-Hyong Chung, KaeKyoung Kwon, Jung-Hyun Lee, Eugene L. Madsen, Sung-Keun Rhee
PLOS ONE , 2014, DOI: 10.1371/journal.pone.0096449
Abstract: Ammonia-oxidizing archaea (AOA) are ubiquitous and abundant and contribute significantly to the carbon and nitrogen cycles in the ocean. In this study, we assembled AOA draft genomes from two deep marine sediments from Donghae, South Korea, and Svalbard, Arctic region, by sequencing the enriched metagenomes. Three major microorganism clusters belonging to Thaumarchaeota, Epsilonproteobacteria, and Gammaproteobacteria were deduced from their 16S rRNA genes, GC contents, and oligonucleotide frequencies. Three archaeal genomes were identified, two of which were distinct and were designated Ca. “Nitrosopumilus koreensis” AR1 and “Nitrosopumilus sediminis” AR2. AR1 and AR2 exhibited average nucleotide identities of 85.2% and 79.5% to N. maritimus, respectively. The AR1 and AR2 genomes contained genes pertaining to energy metabolism and carbon fixation as conserved in other AOA, but, conversely, had fewer heme-containing proteins and more copper-containing proteins than other AOA. Most of the distinctive AR1 and AR2 genes were located in genomic islands (GIs) that were not present in other AOA genomes or in a reference water-column metagenome from the Sargasso Sea. A putative gene cluster involved in urea utilization was found in the AR2 genome, but not the AR1 genome, suggesting niche specialization in marine AOA. Co-cultured bacterial genome analysis suggested that bacterial sulfur and nitrogen metabolism could be involved in interactions with AOA. Our results provide fundamental information concerning the metabolic potential of deep marine sedimentary AOA.
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