scholarly journals Competition for Ammonia Influences the Structure of Chemotrophic Communities in Geothermal Springs

2013 ◽  
Vol 80 (2) ◽  
pp. 653-661 ◽  
Author(s):  
Trinity L. Hamilton ◽  
Evangeline Koonce ◽  
Alta Howells ◽  
Jeff R. Havig ◽  
Talia Jewell ◽  
...  

ABSTRACTSource waters sampled from Perpetual Spouter hot spring (pH 7.03, 86.4°C), Yellowstone National Park, WY, have low concentrations of total ammonia, nitrite, and nitrate, suggesting nitrogen (N) limitation and/or tight coupling of N cycling processes. Dominant small-subunit rRNA sequences in Perpetual Spouter source sediments are closely affiliated with the ammonia-oxidizing archaeon “CandidatusNitrosocaldus yellowstonii” and the putatively nitrogen-fixing (diazotrophic) bacteriumThermocrinis albus, respectively, suggesting that these populations may interact at the level of the bioavailable N pool, specifically, ammonia. This hypothesis was evaluated by using a combination of geochemical, physiological, and transcriptomic analyses of sediment microcosms. Amendment of microcosms with allylthiourea, an inhibitor of ammonia oxidation, decreased rates of acetylene reduction (a proxy for N2fixation) and nitrite production (a proxy for ammonia oxidation) and decreased transcript levels of structural genes involved in both nitrogen fixation (nifH) and ammonia oxidation (amoA). In contrast, amendment of microcosms with ammonia stimulated nitrite production and increasedamoAtranscript levels while it suppressed rates of acetylene reduction and decreasednifHtranscript levels. Sequencing of amplifiednifHandamoAtranscripts from native sediments, as well as microcosms, at 2 and 4 h postamendment, indicates that the dominant and responsive populations involved in ammonia oxidation and N2fixation are closely affiliated withCa. Nitrosocaldus yellowstonii andT. albus, respectively. Collectively, these results suggest that ammonia-oxidizing archaea, such asCa. Nitrosocaldus yellowstonii, have an apparent affinity for ammonia that is higher than that of the diazotrophs present in this ecosystem. Depletion of the bioavailable N pool through the activity of ammonia-oxidizing archaea likely represents a strong selective pressure for the inclusion of organisms capable of nitrogen fixation in geothermal communities. These observations help to explain the strong pattern in the codistribution of ammonia-oxidizing archaea and diazotrophs in circumneutral-to-alkaline geothermal springs.

2013 ◽  
Vol 79 (22) ◽  
pp. 6911-6916 ◽  
Author(s):  
Tatsunori Nakagawa ◽  
David A. Stahl

ABSTRACTThe ability of chemoautotrophic ammonia-oxidizing archaea to compete for ammonia among marine microorganisms at low ambient concentrations has been in part attributed to their extremely high affinity for ammonia, but as yet there is no mechanistic understanding of supporting metabolism. We examined transcription of selected genes for anabolic functions (CO2fixation, ammonia transport, and cell wall synthesis) and a central catabolic function (ammonia oxidation) in the thaumarchaeonNitrosopumilus maritimusSCM1 growing at two ammonia concentrations, as measured by combined ammonia and ammonium, one well above theKmfor ammonia oxidation (∼500 μM) and the other well below theKm(<10 nM). Transcript levels were generally immediately and differentially repressed when cells transitioned from ammonia-replete to ammonia-limiting conditions. Transcript levels for ammonia oxidation, CO2fixation, and one of the ammonia transport genes were approximately the same at high and low ammonia availability. Transcripts for all analyzed genes decreased with time in the complete absence of ammonia, but with various rates of decay. The new steady-state mRNA levels established are presumably more reflective of the natural physiological state of ammonia-oxidizing archaea and offer a reference for interpreting message abundance patterns in the natural environment.


2013 ◽  
Vol 10 (11) ◽  
pp. 7395-7410 ◽  
Author(s):  
A. E. Santoro ◽  
C. M. Sakamoto ◽  
J. M. Smith ◽  
J. N. Plant ◽  
A. L. Gehman ◽  
...  

Abstract. Nitrite (NO2−) is a substrate for both oxidative and reductive microbial metabolism. NO2− accumulates at the base of the euphotic zone in oxygenated, stratified open-ocean water columns, forming a feature known as the primary nitrite maximum (PNM). Potential pathways of NO2− production include the oxidation of ammonia (NH3) by ammonia-oxidizing bacteria and archaea as well as assimilatory nitrate (NO3−) reduction by phytoplankton and heterotrophic bacteria. Measurements of NH3 oxidation and NO3− reduction to NO2− were conducted at two stations in the central California Current in the eastern North Pacific to determine the relative contributions of these processes to NO2− production in the PNM. Sensitive (< 10 nmol L−1), precise measurements of [NH4+] and [NO2−] indicated a persistent NH4+ maximum overlying the PNM at every station, with concentrations as high as 1.5 μmol L−1. Within and just below the PNM, NH3 oxidation was the dominant NO2− producing process, with rates of NH3 oxidation to NO2− of up to 31 nmol L−1 d−1, coinciding with high abundances of ammonia-oxidizing archaea. Though little NO2− production from NO3− was detected, potentially nitrate-reducing phytoplankton (photosynthetic picoeukaryotes, Synechococcus, and Prochlorococcus) were present at the depth of the PNM. Rates of NO2− production from NO3− were highest within the upper mixed layer (4.6 nmol L−1 d−1) but were either below detection limits or 10 times lower than NH3 oxidation rates around the PNM. One-dimensional modeling of water column NO2− production agreed with production determined from 15N bottle incubations within the PNM, but a modeled net biological sink for NO2− just below the PNM was not captured in the incubations. Residence time estimates of NO2− within the PNM ranged from 18 to 470 days at the mesotrophic station and was 40 days at the oligotrophic station. Our results suggest the PNM is a dynamic, rather than relict, feature with a source term dominated by ammonia oxidation.


2016 ◽  
Vol 82 (15) ◽  
pp. 4492-4504 ◽  
Author(s):  
Manabu Nishizawa ◽  
Sanae Sakai ◽  
Uta Konno ◽  
Nozomi Nakahara ◽  
Yoshihiro Takaki ◽  
...  

ABSTRACTAmmonia oxidation regulates the balance of reduced and oxidized nitrogen pools in nature. Although ammonia-oxidizing archaea have been recently recognized to often outnumber ammonia-oxidizing bacteria in various environments, the contribution of ammonia-oxidizing archaea is still uncertain due to difficulties in thein situquantification of ammonia oxidation activity. Nitrogen and oxygen isotope ratios of nitrite (δ15NNO2−and δ18ONO2−, respectively) are geochemical tracers for evaluating the sources and thein siturate of nitrite turnover determined from the activities of nitrification and denitrification; however, the isotope ratios of nitrite from archaeal ammonia oxidation have been characterized only for a few marine species. We first report the isotope effects of ammonia oxidation at 70°C by thermophilicThaumarchaeotapopulations composed almost entirely of “CandidatusNitrosocaldus.” The nitrogen isotope effect of ammonia oxidation varied with ambient pH (25‰ to 32‰) and strongly suggests the oxidation of ammonia, not ammonium. The δ18O value of nitrite produced from ammonia oxidation varied with the δ18O value of water in the medium but was lower than the isotopic equilibrium value in water. Because experiments have shown that the half-life of abiotic oxygen isotope exchange between nitrite and water is longer than 33 h at 70°C and pH ≥6.6, the rate of ammonia oxidation by thermophilicThaumarchaeotacould be estimated using δ18ONO2−in geothermal environments, where the biological nitrite turnover is likely faster than 33 h. This study extended the range of application of nitrite isotopes as a geochemical clock of the ammonia oxidation activity to high-temperature environments.IMPORTANCEBecause ammonia oxidation is generally the rate-limiting step in nitrification that regulates the balance of reduced and oxidized nitrogen pools in nature, it is important to understand the biological and environmental factors underlying the regulation of the rate of ammonia oxidation. The discovery of ammonia-oxidizing archaea (AOA) in marine and terrestrial environments has transformed the concept that ammonia oxidation is operated only by bacterial species, suggesting that AOA play a significant role in the global nitrogen cycle. However, the archaeal contribution to ammonia oxidation in the global biosphere is not yet completely understood. This study successfully identified key factors controlling nitrogen and oxygen isotopic ratios of nitrite produced from thermophilicThaumarchaeotaand elucidated the applicability and its limit of nitrite isotopes as a geochemical clock of ammonia oxidation rate in nature. Oxygen isotope analysis in this study also provided new biochemical information on archaeal ammonia oxidation.


2012 ◽  
Vol 78 (16) ◽  
pp. 5773-5780 ◽  
Author(s):  
Elizabeth French ◽  
Jessica A. Kozlowski ◽  
Maitreyee Mukherjee ◽  
George Bullerjahn ◽  
Annette Bollmann

ABSTRACTAerobic biological ammonia oxidation is carried out by two groups of microorganisms, ammonia-oxidizing bacteria (AOB) and the recently discovered ammonia-oxidizing archaea (AOA). Here we present a study using cultivation-based methods to investigate the differences in growth of three AOA cultures and one AOB culture enriched from freshwater environments. The strain in the enriched AOA culture belong to thaumarchaeal group I.1a, with the strain in one enrichment culture having the highest identity with “CandidatusNitrosoarchaeum koreensis” and the strains in the other two representing a new genus of AOA. The AOB strain in the enrichment culture was also obtained from freshwater and had the highest identity to AOB from theNitrosomonas oligotrophagroup (Nitrosomonascluster 6a). We investigated the influence of ammonium, oxygen, pH, and light on the growth of AOA and AOB. The growth rates of the AOB increased with increasing ammonium concentrations, while the growth rates of the AOA decreased slightly. Increasing oxygen concentrations led to an increase in the growth rate of the AOB, while the growth rates of AOA were almost oxygen insensitive. Light exposure (white and blue wavelengths) inhibited the growth of AOA completely, and the AOA did not recover when transferred to the dark. AOB were also inhibited by blue light; however, growth recovered immediately after transfer to the dark. Our results show that the tested AOB have a competitive advantage over the tested AOA under most conditions investigated. Further experiments will elucidate the niches of AOA and AOB in more detail.


2020 ◽  
Vol 14 (11) ◽  
pp. 2659-2674 ◽  
Author(s):  
Carolina Reyes ◽  
Logan H. Hodgskiss ◽  
Melina Kerou ◽  
Thomas Pribasnig ◽  
Sophie S. Abby ◽  
...  

Abstract Ammonia-oxidizing archaea (AOA) are widespread in nature and are involved in nitrification, an essential process in the global nitrogen cycle. The enzymes for ammonia oxidation and electron transport rely heavily on copper (Cu), which can be limited in nature. In this study the model soil archaeon Nitrososphaera viennensis was investigated via transcriptomic analysis to gain insight regarding possible Cu uptake mechanisms and compensation strategies when Cu becomes limiting. Upon Cu limitation, N. viennensis exhibited impaired nitrite production and thus growth, which was paralleled by downregulation of ammonia oxidation, electron transport, carbon fixation, nucleotide, and lipid biosynthesis pathway genes. Under Cu-limitation, 1547 out of 3180 detected genes were differentially expressed, with 784 genes upregulated and 763 downregulated. The most highly upregulated genes encoded proteins with a possible role in Cu binding and uptake, such as the Cu chelator and transporter CopC/D, disulfide bond oxidoreductase D (dsbD), and multicopper oxidases. While this response differs from the marine strain Nitrosopumilus maritimus, conserved sequence motifs in some of the Cu-responsive genes suggest conserved transcriptional regulation in terrestrial AOA. This study provides possible gene regulation and energy conservation mechanisms linked to Cu bioavailability and presents the first model for Cu uptake by a soil AOA.


2017 ◽  
Author(s):  
Anne Daebeler ◽  
Craig Herbold ◽  
Julia Vierheilig ◽  
Christopher J. Sedlacek ◽  
Petra Pjevac ◽  
...  

AbstractAmmonia-oxidizing archaea (AOA) within the phylumThaumarchaeaare the only known aerobic ammonia oxidizers in geothermal environments. Although molecular data indicate the presence of phylogenetically diverse AOA from theNitrosocaldusclade, group 1.1b and group 1.1aThaumarchaeain terrestrial high-temperature habitats, only one enrichment culture of an AOA thriving above 50 °C has been reported and functionally analyzed. In this study, we physiologically and genomically characterized a novelThaumarchaeonfrom the deep-branchingNitrosocaldaceaefamily of which we have obtained a high (∼85 %) enrichment from biofilm of an Icelandic hot spring (73 °C). This AOA, which we provisionally refer to as “CandidatusNitrosocaldus islandicus”, is an obligately thermophilic, aerobic chemolithoautotrophic ammonia oxidizer, which stoichiometrically converts ammonia to nitrite at temperatures between 50 °C and 70 °C.Ca.N. islandicus encodes the expected repertoire of enzymes proposed to be required for archaeal ammonia oxidation, but unexpectedly lacks anirKgene and also possesses no identifiable other enzyme for nitric oxide (NO) generation. Nevertheless, ammonia oxidation by this AOA appears to be NO-dependent asCa.N. islandicus is, like all other tested AOA, inhibited by the addition of an NO scavenger. Furthermore, comparative genomics revealed thatCa.N. islandicus has the potential for aromatic amino acid fermentation as its genome encodes an indolepyruvate oxidoreductase(iorAB)as well as a type 3b hydrogenase, which are not present in any other sequenced AOA. A further surprising genomic feature of this thermophilic ammonia oxidizer is the absence of DNA polymerase D genes - one of the predominant replicative DNA polymerases in all other ammonia-oxidizingThaumarchaea.Collectively, our findings suggest that metabolic versatility and DNA replication might differ substantially between obligately thermophilic and other AOA.


2013 ◽  
Vol 10 (3) ◽  
pp. 5803-5840 ◽  
Author(s):  
A. E. Santoro ◽  
C. M. Sakamoto ◽  
J. M. Smith ◽  
J. N. Plant ◽  
A. L. Gehman ◽  
...  

Abstract. Nitrite (NO2–) is a substrate for both oxidative and reductive microbial metabolism. NO2– accumulates at the base of the euphotic zone in oxygenated, stratified open ocean water columns, forming a feature known as the primary nitrite maximum (PNM). Potential pathways of NO2– production include the oxidation of ammonia (NH3) by ammonia-oxidizing bacteria or archaea and assimilatory nitrate (NO3–) reduction by phytoplankton or heterotrophic bacteria. Measurements of NH3 oxidation and NO3– reduction to NO2– were conducted at two stations in the central California Current in the eastern North Pacific to determine the relative contributions of these processes to NO2– production in the PNM. Sensitive (< 10 nmol L−1), high-resolution measurements of [NH4+] and [NO2–] indicated a persistent NH4+ maximum overlying the PNM at every station, with concentrations as high as 1.5 μmol L−1. Within and just below the PNM, NH3 oxidation was the dominant NO2– producing process with rates of NH3 oxidation of up to 50 nmol L−1 d−1, coinciding with high abundances of ammonia-oxidizing archaea. Though little NO2– production from NO3– was detected, potentially nitrate-reducing phytoplankton (photosynthetic picoeukaryotes, Synechococcus, and Prochlorococcus) were present at the depth of the PNM. Rates of NO2– production from NO3– were highest within the upper mixed layer (4.6 nmol L−1 d−1) but were either below detection limits or 10 times lower than NH3 oxidation rates around the PNM. One-dimensional modeling of water column NO2– profiles supported direct rate measurements of a net biological sink for NO2– just below the PNM. Residence time estimates of NO2– within the PNM were similar at the mesotrophic and oligotrophic stations and ranged from 150–205 d. Our results suggest the PNM is a dynamic, rather than relict, feature with a source term dominated by ammonia oxidation.


2015 ◽  
Vol 81 (6) ◽  
pp. 1942-1948 ◽  
Author(s):  
A. E. Taylor ◽  
K. Taylor ◽  
B. Tennigkeit ◽  
M. Palatinszky ◽  
M. Stieglmeier ◽  
...  

ABSTRACTA previous study showed that ammonia oxidation by theThaumarchaeotaNitrosopumilus maritimus(group 1.1a) was resistant to concentrations of the C81-alkyne, octyne, which completely inhibits activity by ammonia-oxidizing bacteria. In this study, the inhibitory effects of octyne and other C2to C101-alkynes were evaluated on the nitrite production activity of two pure culture isolates fromThaumarchaeotagroup 1.1b,Nitrososphaera viennensisstrain EN76 andNitrososphaera gargensis. BothN. viennensisandN. gargensiswere insensitive to concentrations of octyne that cause complete and irreversible inactivation of nitrite production by ammonia-oxidizing bacteria. However, octyne concentrations (≥20 μM) that did not inhibitN. maritimuspartially inhibited nitrite production inN. viennensisandN. gargensisin a manner that did not show the characteristics of irreversible inactivation. In contrast to previous studies with an ammonia-oxidizing bacterium,Nitrosomonas europaea, octyne inhibition ofN. viennensiswas: (i) fully and immediately reversible, (ii) not competitive with NH4+, and (iii) without effect on the competitive interaction between NH4+and acetylene. BothN. viennensisandN. gargensisdemonstrated the same overall trend in regard to 1-alkyne inhibition as previously observed forN. maritimus, being highly sensitive to ≤C5alkynes and more resistant to longer-chain length alkynes. Reproducible differences were observed amongN. maritimus,N. viennensis, andN. gargensisin regard to the extent of their resistance/sensitivity to C6and C71-alkynes, which may indicate differences in the ammonia monooxygenase binding and catalytic site(s) among theThaumarchaeota.


2015 ◽  
Vol 12 (19) ◽  
pp. 16255-16283
Author(s):  
S. Chen ◽  
X.-T. Peng ◽  
H.-C. Xu ◽  
K.-W. Ta

Abstract. The oxidation of ammonia by microbes and associated organisms has been shown to occur in diverse natural environments. However, the contribution of ammonia-oxidizing archaea to nitrification in high-temperature environments remains unclear. Here, we studied in situ ammonia oxidation rates and the abundance of ammonia-oxidizing archaea (AOA) in surface and bottom sediments at 77 °C in the Gongxiaoshe hot spring, Tengchong, Yunnan, China. The in situ ammonia oxidation rates measured by the 15N–NO3- pool dilution technique in the surface sinter and bottom sediments were 4.8 and 5.3 nmol N g−1 h−1, respectively. Relative abundances of Crenarchaea in both samples were determined by fluorescence in situ hybridization (FISH). Phylogenetic analysis of 16S rRNA genes showed high sequence similarity to thermophilic "Candidatus Nitrosocaldus yellowstonii", which represented the most abundant operation taxonomic units (OTU) in both sediments. Furthermore, bacterial amoA was not detected in this study. Quantitative PCR (qPCR) indicated that AOA and 16S rRNA genes were present in the range of 2.75 to 9.80 × 105 and 0.128 to 1.96 × 108 gene copies g−1 sediment. The cell-specific nitrification rates were estimated to be in the range of 0.41 to 0.79 fmol N archaeal cell−1 h−1, which is consistent with earlier estimates in estuary environments. This study demonstrated that AOA were widely involved in nitrification in this hot spring. It further indicated the importance of archaea rather than bacteria in driving the nitrogen cycle in terrestrial geothermal environments.


2011 ◽  
Vol 77 (10) ◽  
pp. 3468-3477 ◽  
Author(s):  
Angela Pitcher ◽  
Ellen C. Hopmans ◽  
Annika C. Mosier ◽  
Soo-Je Park ◽  
Sung-Keun Rhee ◽  
...  

ABSTRACTGlycerol dibiphytanyl glycerol tetraether (GDGT)-based intact membrane lipids are increasingly being used as complements to conventional molecular methods in ecological studies of ammonia-oxidizing archaea (AOA) in the marine environment. However, the few studies that have been done on the detailed lipid structures synthesized by AOA in (enrichment) culture are based on species enriched from nonmarine environments, i.e., a hot spring, an aquarium filter, and a sponge. Here we have analyzed core and intact polar lipid (IPL)-GDGTs synthesized by three newly available AOA enriched directly from marine sediments taken from the San Francisco Bay estuary (“CandidatusNitrosoarchaeum limnia”), and coastal marine sediments from Svalbard, Norway, and South Korea. Like previously screened AOA, the sedimentary AOA all synthesize crenarchaeol (a GDGT containing a cyclohexane moiety and four cyclopentane moieties) as a major core GDGT, thereby supporting the hypothesis that crenarchaeol is a biomarker lipid for AOA. The IPL headgroups synthesized by sedimentary AOA comprised mainly monohexose, dihexose, phosphohexose, and hexose-phosphohexose moieties. The hexose-phosphohexose headgroup bound to crenarchaeol was common to all enrichments and, in fact, the only IPL common to every AOA enrichment analyzed to date. This apparent specificity, in combination with its inferred lability, suggests that it may be the most suitable biomarker lipid to trace living AOA. GDGTs bound to headgroups with a mass of 180 Da of unknown structure appear to be specific to the marine group I.1a AOA: they were synthesized by all three sedimentary AOA and “CandidatusNitrosopumilus maritimus”; however, they were absent in the group I.1b AOA “CandidatusNitrososphaera gargensis.”


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