Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean
11 Oct 2005-Proceedings of the National Academy of Sciences of the United States of America (National Academy of Sciences)-Vol. 102, Iss: 41, pp 14683-14688
TL;DR: Using PCR primers designed to specifically target archaeal amoA, AOA is found 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.
Abstract: 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 β- and γ-Proteobacteria. However, recent metagenomic studies have revealed the existence of unique ammonia monooxygenase α-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.
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TL;DR: This Review summarizes the current understanding of the microbial nitrogen-cycling network, including novel processes, their underlying biochemical pathways, the involved microorganisms, their environmental importance and industrial applications.
Abstract: Nitrogen is an essential component of all living organisms and the main nutrient limiting life on our planet By far, the largest inventory of freely accessible nitrogen is atmospheric dinitrogen, but most organisms rely on more bioavailable forms of nitrogen, such as ammonium and nitrate, for growth The availability of these substrates depends on diverse nitrogen-transforming reactions that are carried out by complex networks of metabolically versatile microorganisms In this Review, we summarize our current understanding of the microbial nitrogen-cycling network, including novel processes, their underlying biochemical pathways, the involved microorganisms, their environmental importance and industrial applications
1,794 citations
TL;DR: In 1909, H. Joel Conn expressed the hope that methods would soon be at hand by which the significance of the different bacteria present in any soil could be understood.
Abstract: From near to far ,
from here to there ,
funny things are everywhere.
—Dr. Seuss, One Fish Two Fish Red Fish Blue Fish
In 1909, H. Joel Conn ([25][1]) expressed the hope that methods would soon be at hand by which the significance of the different bacteria present in any soil could be
1,568 citations
Cites background from "Ubiquity and diversity of ammonia-o..."
...Some of these soil archaea may prove to have unexpected physiologies (42), and they appear to be culturable (99)....
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TL;DR: Oligotrophic ammonia oxidation kinetics and cellular characteristics of the mesophilic crenarchaeon ‘Candidatus Nitrosopumilus maritimus’ strain SCM1 support the hypothesis that nitrification is more prevalent in the marine nitrogen cycle than accounted for in current biogeochemical models.
Abstract: The discovery of ammonia oxidation by mesophilic and thermophilic Crenarchaeota and the widespread distribution of these organisms in marine and terrestrial environments indicated an important role for them in the global nitrogen cycle. However, very little is known about their physiology or their contribution to nitrification. Here we report oligotrophic ammonia oxidation kinetics and cellular characteristics of the mesophilic crenarchaeon 'Candidatus Nitrosopumilus maritimus' strain SCM1. Unlike characterized ammonia-oxidizing bacteria, SCM1 is adapted to life under extreme nutrient limitation, sustaining high specific oxidation rates at ammonium concentrations found in open oceans. Its half-saturation constant (K(m) = 133 nM total ammonium) and substrate threshold (
1,389 citations
TL;DR: Analysis of Atlantic waters of the upper 1,000 m, where most of the ammonium regeneration and oxidation takes place, showed that crenarchaeotal amoA copy numbers are also 1–3 orders of magnitude higher than those of bacterial amoB, suggesting a major role for Archaea in oceanic nitrification.
Abstract: Marine Crenarchaeota are the most abundant single group of prokaryotes in the ocean, but their physiology and role in marine biogeochemical cycles are unknown. Recently, a member of this clade was isolated from a sea aquarium and shown to be capable of nitrification, tentatively suggesting that Crenarchaeota may play a role in the oceanic nitrogen cycle. We enriched a crenarchaeote from North Sea water and showed that its abundance, and not that of bacteria, correlates with ammonium oxidation to nitrite. A time series study in the North Sea revealed that the abundance of the gene encoding for the archaeal ammonia monooxygenase alfa subunit (amoA) is correlated with a decline in ammonium concentrations and with the abundance of Crenarchaeota. Remarkably, the archaeal amoA abundance was 1–2 orders of magnitude higher than those of bacterial nitrifiers, which are commonly thought to mediate the oxidation of ammonium to nitrite in marine environments. Analysis of Atlantic waters of the upper 1,000 m, where most of the ammonium regeneration and oxidation takes place, showed that crenarchaeotal amoA copy numbers are also 1–3 orders of magnitude higher than those of bacterial amoA. Our data thus suggest a major role for Archaea in oceanic nitrification.
1,087 citations
15 Apr 2008
TL;DR: For example, the World Health Organization and U.S. Environmental Protection Agency have set a limit of 10 mg L nitrate (as N) for drinking water because nitrate poses a health risk, especially for children, who can contract methemoglobinemia (blue-baby syndrome) as mentioned in this paper.
Abstract: Nitrate (NO3 ) concentrations in public water supplies have risen above acceptable levels in many areas of the world, largely as a result of overuse of fertilizers and contamination by human and animal waste. The World Health Organization and the U.S. Environmental Protection Agency have set a limit of 10 mg L nitrate (as N) for drinking water because nitrate poses a health risk, especially for children, who can contract methemoglobinemia (blue-baby syndrome). Nitrate in lower concentrations is non-toxic, but the risks from long-term exposure are unknown, although nitrate is a suspected carcinogen. High concentrations of nitrate in rivers, lakes, and coastal areas can cause eutrophication, often followed by fi sh-kills, due to oxygen depletion. Increased atmospheric loads of anthropogenic nitric and sulfuric acids have caused many sensitive, low-alkalinity streams in North America and Europe to become acidifi ed. Still more streams that are not yet chronically acidic could undergo acidic episodes in response to large rain storms and/or spring snowmelt, seriously damaging sensitive local ecosystems. Future climate changes may exacerbate the situation by affecting biogeochemical controls on the transport of water, nutrients, and other materials from land to freshwater ecosystems. The development of effective management practices to preserve water quality, and remediation plans for sites that are already polluted, requires the identifi cation of actual N sources and an understanding of the processes affecting local nitrate concentrations. In particular, a better understanding of hydrologic fl owpaths and solute sources is required to determine the potential impact of contaminants on water supplies. Determination of the relation between nitrate concentrations in groundwater and surface water and the quantity of nitrate introduced from a particular source is complicated by:
963 citations
Cites background from "Ubiquity and diversity of ammonia-o..."
...The recent discovery of ammonium-oxidizing archaea may raise new questions about the role of archaea in N cycling (Francis et al. 2005; Könneke et al. 2005; Schleper et al. 2005)....
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References
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TL;DR: In this paper, the authors compared the natural and anthropogenic controls on the conversion of unreactive N2 to more reactive forms of nitrogen (Nr) and found that human activities increasingly dominate the N budget at the global and at most regional scales, and the terrestrial and open ocean N budgets are essentially dis-connected.
Abstract: This paper contrasts the natural and anthropogenic controls on the conversion of unreactive N2 to more reactive forms of nitrogen (Nr). A variety of data sets are used to construct global N budgets for 1860 and the early 1990s and to make projections for the global N budget in 2050. Regional N budgets for Asia, North America, and other major regions for the early 1990s, as well as the marine N budget, are presented to highlight the dominant fluxes of nitrogen in each region. Important findings are that human activities increasingly dominate the N budget at the global and at most regional scales, the terrestrial and open ocean N budgets are essentially dis- connected, and the fixed forms of N are accumulating in most environmental reservoirs. The largest uncertainties in our understanding of the N budget at most scales are the rates of natural biological nitrogen fixation, the amount of Nr storage in most environmental reservoirs, and the production rates of N2 by denitrification.
4,555 citations
TL;DR: Over 1.2 million previously unknown genes represented in these samples, including more than 782 new rhodopsin-like photoreceptors are identified, suggesting substantial oceanic microbial diversity.
Abstract: We have applied “whole-genome shotgun sequencing” to microbial populations collected en masse on tangential flow and impact filters from seawater samples collected from the Sargasso Sea near Bermuda. A total of 1.045 billion base pairs of nonredundant sequence was generated, annotated, and analyzed to elucidate the gene content, diversity, and relative abundance of the organisms within these environmental samples. These data are estimated to derive from at least 1800 genomic species based on sequence relatedness, including 148 previously unknown bacterial phylotypes. We have identified over 1.2 million previously unknown genes represented in these samples, including more than 782 new rhodopsin-like photoreceptors. Variation in species present and stoichiometry suggests substantial oceanic microbial diversity. Microorganisms are responsible for most of the biogeochemical cycles that shape the environment of Earth and its oceans. Yet, these organisms are the least well understood on Earth, as the ability to study and understand the metabolic potential of microorganisms has been hampered by the inability to generate pure cultures. Recent studies have begun to explore environ
4,210 citations
TL;DR: Evidence for the widespread occurrence of unusual archaea in oxygenated coastal surface waters of North America is provided and it is suggested that these microorganisms represent undescribed physiological types of archaea, which reside and compete with aerobic, mesophilic eubacteria in marine coastal environments.
Abstract: Archaea (archaebacteria) are a phenotypically diverse group of microorganisms that share a common evolutionary history. There are four general phenotypic groups of archaea: the methanogens, the extreme halophiles, the sulfate-reducing archaea, and the extreme thermophiles. In the marine environment, archaeal habitats are generally limited to shallow or deep-sea anaerobic sediments (free-living and endosymbiotic methanogens), hot springs or deep-sea hydrothermal vents (methanogens, sulfate reducers, and extreme thermophiles), and highly saline land-locked seas (halophiles). This report provides evidence for the widespread occurrence of unusual archaea in oxygenated coastal surface waters of North America. Quantitative estimates indicated that up to 2% of the total ribosomal RNA extracted from coastal bacterioplankton assemblages was archaeal. Archaeal small-subunit ribosomal RNA-encoding DNAs (rDNAs) were cloned from mixed bacterioplankton populations collected at geographically distant sampling sites. Phylogenetic and nucleotide signature analyses of these cloned rDNAs revealed the presence of two lineages of archaea, each sharing the diagnostic signatures and structural features previously established for the domain Archaea. Both of these lineages were found in bacterioplankton populations collected off the east and west coasts of North America. The abundance and distribution of these archaea in oxic coastal surface waters suggests that these microorganisms represent undescribed physiological types of archaea, which reside and compete with aerobic, mesophilic eubacteria in marine coastal environments.
2,687 citations
TL;DR: The isolation of a marine crenarchaeote that grows chemolithoautotrophically by aerobically oxidizing ammonia to nitrite—the first observation of nitrification in the Archaea is reported, suggesting that nitrifying marine Cren archaeota may be important to global carbon and nitrogen cycles.
Abstract: For years, microbiologists characterized the Archaea as obligate extremophiles that thrive in environments too harsh for other organisms. The limited physiological diversity among cultivated Archaea suggested that these organisms were metabolically constrained to a few environmental niches. For instance, all Crenarchaeota that are currently cultivated are sulphur-metabolizing thermophiles. However, landmark studies using cultivation-independent methods uncovered vast numbers of Crenarchaeota in cold oxic ocean waters. Subsequent molecular surveys demonstrated the ubiquity of these low-temperature Crenarchaeota in aquatic and terrestrial environments. The numerical dominance of marine Crenarchaeota--estimated at 10(28) cells in the world's oceans--suggests that they have a major role in global biogeochemical cycles. Indeed, isotopic analyses of marine crenarchaeal lipids suggest that these planktonic Archaea fix inorganic carbon. Here we report the isolation of a marine crenarchaeote that grows chemolithoautotrophically by aerobically oxidizing ammonia to nitrite--the first observation of nitrification in the Archaea. The autotrophic metabolism of this isolate, and its close phylogenetic relationship to environmental marine crenarchaeal sequences, suggests that nitrifying marine Crenarchaeota may be important to global carbon and nitrogen cycles.
2,564 citations
TL;DR: A computer program, DOTUR, is developed, which assigns sequences to OTUs by using either the furthest, average, or nearest neighbor algorithm for each distance level, which addresses the challenge of assigning sequences to operational taxonomic units (OTUs) based on the genetic distances between sequences.
Abstract: Although copious qualitative information describes the members of the diverse microbial communities on Earth, statistical approaches for quantifying and comparing the numbers and compositions of lineages in communities are lacking. We present a method that addresses the challenge of assigning sequences to operational taxonomic units (OTUs) based on the genetic distances between sequences. We developed a computer program, DOTUR, which assigns sequences to OTUs by using either the furthest, average, or nearest neighbor algorithm for each distance level. DOTUR uses the frequency at which each OTU is observed to construct rarefaction and collector's curves for various measures of richness and diversity. We analyzed 16S rRNA gene libraries derived from Scottish and Amazonian soils and the Sargasso Sea with DOTUR, which assigned sequences to OTUs rapidly and reliably based on the genetic distances between sequences and identified previous inconsistencies and errors in assigning sequences to OTUs. An analysis of the two 16S rRNA gene libraries from soil demonstrated that they do not contain enough sequences to support a claim that they contain different numbers of bacterial lineages with statistical confidence (P > 0.05), nor do they contain enough sequences to provide a robust estimate of species richness when an OTU is defined as containing sequences that are no more than 3% different from each other. In contrast, the richness of OTUs at the 3% level in the Sargasso Sea collection began to plateau after the sampling of 690 sequences. We anticipate that an equivalent extent of sampling for soil would require sampling more than 10,000 sequences, almost 100 times the size of typical sequence collections obtained from soil.
2,314 citations