Nitrification, the microbial oxidation of ammonia to nitrite and nitrate, occurs in a wide variety of environments and plays a central role in the global nitrogen cycle. Catalyzed by the enzyme ammonia monooxygenase, the ability to oxidize ammonia was previously thought to be restricted to a few groups within the -and ␥-Proteobacteria. However, recent metagenomic studies have revealed the existence of unique ammonia monooxygenase ␣-subunit (amoA) genes derived from uncultivated, nonextremophilic Crenarchaeota. Here, we report molecular evidence for the widespread presence of ammonia-oxidizing archaea (AOA) in marine water columns and sediments. Using PCR primers designed to specifically target archaeal amoA, we find AOA to be pervasive in areas of the ocean that are critical for the global nitrogen cycle, including the base of the euphotic zone, suboxic water columns, and estuarine and coastal sediments. Diverse and distinct AOA communities are associated with each of these habitats, with little overlap between water columns and sediments. Within marine sediments, most AOA sequences are unique to individual sampling locations, whereas a small number of sequences are evidently cosmopolitan in distribution. Considering the abundance of nonextremophilic archaea in the ocean, our results suggest that AOA may play a significant, but previously unrecognized, role in the global nitrogen cycle.Crenarchaeota ͉ nitrification ͉ ammonia monooxygenase
Nitrification plays an important role in marine biogeochemistry, yet efforts to link this process to the microorganisms that mediate it are surprisingly limited. In particular, ammonia oxidation is the first and rate-limiting step of nitrification, yet ammonia oxidation rates and the abundance of ammoniaoxidizing bacteria (AOB) have rarely been measured in tandem. Ammonia oxidation rates have not been directly quantified in conjunction with ammonia-oxidizing archaea (AOA), although mounting evidence indicates that marine Crenarchaeota are capable of ammonia oxidation, and they are among the most abundant microbial groups in the ocean. Here, we have directly quantified ammonia oxidation rates by 15 N labeling, and AOA and AOB abundances by quantitative PCR analysis of ammonia monooxygenase subunit A (amoA) genes, in the Gulf of California. Based on markedly different archaeal amoA sequence types in the upper water column (60 m) and oxygen minimum zone (OMZ; 450 m), novel amoA PCR primers were designed to specifically target and quantify 'shallow' (group A) and 'deep' (group B) clades. These primers recovered extensive variability with depth. Within the OMZ, AOA were most abundant where nitrification may be coupled to denitrification. In the upper water column, group A tracked variations in nitrogen biogeochemistry with depth and between basins, whereas AOB were present in relatively low numbers or undetectable. Overall, 15 NH 4 þ oxidation rates were remarkably well correlated with AOA group A amoA gene copies (r 2 ¼ 0.90, Po0.001), and with 16S rRNA gene copies from marine Crenarchaeota (r 2 ¼ 0.85, Po0.005). These findings represent compelling evidence for an archaeal role in oceanic nitrification.
Microbial activities drive the global nitrogen cycle, and in the past few years, our understanding of nitrogen cycling processes and the micro-organisms that mediate them has changed dramatically. During this time, the processes of anaerobic ammonium oxidation (anammox), and ammonia oxidation within the domain Archaea, have been recognized as two new links in the global nitrogen cycle. All available evidence indicates that these processes and organisms are critically important in the environment, and particularly in the ocean. Here we review what is currently known about the microbial ecology of anaerobic and archaeal ammonia oxidation, highlight relevant unknowns and discuss the implications of these discoveries for the global nitrogen and carbon cycles.
A combination of stable isotope and molecular biological approaches was used to determine the activity, abundance and diversity of nitrifying organisms in the central California Current. Using (15)NH(4)(+) incubations, nitrification was detectable in the upper water column down to 500 m; maximal rates were observed just below the euphotic zone. Crenarchaeal and betaproteobacterial ammonia monooxygenase subunit A genes (amoA), and 16S ribosomal RNA (rRNA) genes of Marine Group I Crenarchaeota and a putative nitrite-oxidizing genus, Nitrospina, were quantified using quantitative PCR. Crenarchaeal amoA abundance ranged from three to six genes ml(-1) in oligotrophic surface waters to > 8.7 x 10(4) genes ml(-1) just below the core of the California Current at 200 m depth. Bacterial amoA abundance was lower than archaeal amoA and ranged from below detection levels to 400 genes ml(-1). Nitrification rates were not directly correlated to bacterial or archaeal amoA abundance. Archaeal amoA and Marine Group I crenarchaeal 16S rRNA gene abundances were correlated with Nitrospina 16S rRNA gene abundance at all stations, indicating that similar factors may control the distribution of these two groups. Putatively shallow water-associated archaeal amoA types ('Cluster A') decreased in relative abundance with depth, while a deep water-associated amoA type ('Cluster B') increased with depth. Although some Cluster B amoA sequences were found in surface waters, expressed amoA gene sequences were predominantly from Cluster A. Cluster B amoA transcripts were detected between 100 and 500 m depths, suggesting an active role in ammonia oxidation in the mesopelagic. Expression of marine Nitrosospira-like bacterial amoA genes was detected throughout the euphotic zone down to 200 m. Natural abundance stable isotope ratios (delta(15)N and delta(18)O) in nitrate (NO(3)(-)) and nitrous oxide (N(2)O) were used to evaluate the importance of nitrification over longer time scales. Using an isotope mass balance model, we calculate that nitrification could produce between 0.45 and 2.93 micromol m(-2) day(-1) N(2)O in the central California Current, or approximately 1.5-4 times the local N(2)O flux from deep water.
It has long been assumed that differences in the relative abundance of taxa in microbial communities reflect differences in environmental conditions. Here we show that in the economically and environmentally important microbial communities in a wastewater treatment plant, the population dynamics are consistent with neutral community assembly, where chance and random immigration play an important and predictable role in shaping the communities. Using dynamic observations, we demonstrate a straightforward calibration of a purely neutral model and a parsimonious method to incorporate environmental influence on the reproduction (or birth) rate of individual taxa. The calibrated model parameters are biologically plausible, with the population turnover and diversity in the heterotrophic community being higher than for the ammonia oxidizing bacteria (AOB) and immigration into AOB community being relatively higher. When environmental factors were incorporated more of the variance in the observations could be explained but immigration and random reproduction and deaths remained the dominant driver in determining the relative abundance of the common taxa. Consequently we suggest that neutral community models should be the foundation of any description of an open biological system. microbial community assembly
Ammonia oxidation in marine and estuarine sediments plays a pivotal role in the cycling and removal of nitrogen. Recent reports have shown that the newly discovered ammonia-oxidizing archaea can be both abundant and diverse in aquatic and terrestrial ecosystems. In this study, we examined the abundance and diversity of ammonia-oxidizing archaea (AOA) and betaproteobacteria (beta-AOB) across physicochemical gradients in San Francisco Bay--the largest estuary on the west coast of the USA. In contrast to reports that AOA are far more abundant than beta-AOB in both terrestrial and marine systems, our quantitative PCR estimates indicated that beta-AOB amoA (encoding ammonia monooxygenase subunit A) copy numbers were greater than AOA amoA in most of the estuary. Ammonia-oxidizing archaea were only more pervasive than beta-AOB in the low-salinity region of the estuary. Both AOA and beta-AOB communities exhibited distinct spatial structure within the estuary. AOA amoA sequences from the north part of the estuary formed a large and distinct low-salinity phylogenetic group. The majority of the beta-AOB sequences were closely related to other marine/estuarine Nitrosomonas-like and Nitrosospira-like sequences. Both ammonia-oxidizer community composition and abundance were strongly correlated with salinity. Ammonia-oxidizing enrichment cultures contained AOA and beta-AOB amoA sequences with high similarity to environmental sequences. Overall, this study significantly enhances our understanding of estuarine ammonia-oxidizing microbial communities and highlights the environmental conditions and niches under which different AOA and beta-AOB phylotypes may thrive.
Submarine groundwater discharge to coastal waters can be a significant source of both contaminants and biologically limiting nutrients. Nitrogen cycling across steep gradients in salinity, oxygen and dissolved inorganic nitrogen in sandy 'subterranean estuaries' controls both the amount and form of nitrogen discharged to the coastal ocean. We determined the effect of these gradients on betaproteobacterial ammonia-oxidizing bacteria (beta-AOB) and ammonia-oxidizing archaea (AOA) in a subterranean estuary using the functional gene encoding ammonia monooxygenase subunit A (amoA). The abundance of beta-AOB was dramatically lower in the freshwater stations compared with saline stations, while AOA abundance remained nearly constant across the study site. This differing response to salinity altered the ratio of beta-AOB to AOA such that bacterial amoA was 30 times more abundant than crenarchaeal amoA at the oxic marine station, but nearly 10 times less abundant at the low-oxygen fresh and brackish stations. As the location of the brackish mixing zone within the aquifer shifted from landward in winter to oceanward in summer, the location of the transition from a beta-AOB-dominated to an AOA-dominated community also shifted, demonstrating the intimate link between microbial communities and coastal hydrology. Analysis of ammonia-oxidizing enrichment cultures at a range of salinities revealed that AOA persisted solely in the freshwater enrichments where they actively express amoA. Diversity (as measured by total richness) of crenarchaeal amoA was high at all stations and time points, in sharp contrast to betaproteobacterial amoA for which only two sequence types were found. These results offer new insights into the ecology of AOA and beta-AOB by elucidating conditions that may favour the numerical dominance of beta-AOB over AOA in coastal sediments.
Ammonia-oxidizing archaea (AOA) are thought to be among the most abundant microorganisms on Earth and may significantly impact the global nitrogen and carbon cycles. We sequenced the genome of AOA in an enrichment culture from low-salinity sediments in San Francisco Bay using single-cell and metagenomic genome sequence data. Five single cells were isolated inside an integrated microfluidic device using laser tweezers, the cells' genomic DNA was amplified by multiple displacement amplification (MDA) in 50 nL volumes and then sequenced by high-throughput DNA pyrosequencing. This microscopy-based approach to single-cell genomics minimizes contamination and allows correlation of high-resolution cell images with genomic sequences. Statistical properties of coverage across the five single cells, in combination with the contrasting properties of the metagenomic dataset allowed the assembly of a high-quality draft genome. The genome of this AOA, which we designate Candidatus Nitrosoarchaeum limnia SFB1, is ∼1.77 Mb with >2100 genes and a G+C content of 32%. Across the entire genome, the average nucleotide identity to Nitrosopumilus maritimus, the only AOA in pure culture, is ∼70%, suggesting this AOA represents a new genus of Crenarchaeota. Phylogenetically, the 16S rRNA and ammonia monooxygenase subunit A (amoA) genes of this AOA are most closely related to sequences reported from a wide variety of freshwater ecosystems. Like N. maritimus, the low-salinity AOA genome appears to have an ammonia oxidation pathway distinct from ammonia oxidizing bacteria (AOB). In contrast to other described AOA, these low-salinity AOA appear to be motile, based on the presence of numerous motility- and chemotaxis-associated genes in the genome. This genome data will be used to inform targeted physiological and metabolic studies of this novel group of AOA, which may ultimately advance our understanding of AOA metabolism and their impacts on the global carbon and nitrogen cycles.
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