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Jaap Sinninghe S Damste - One of the best experts on this subject based on the ideXlab platform.
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membrane lipid composition of the moderately thermophilic ammonia oxidizing archaeon candidatus nitrosotenuis uzonensis at different growth temperatures
Applied and Environmental Microbiology, 2019Co-Authors: Nicole J Bale, Marton Palatinszky, Irene W C Rijpstra, Craig W Herbold, Michael Wagner, Jaap Sinninghe S DamsteAbstract:ABSTRACT “Candidatus Nitrosotenuis uzonensis” is the only cultured moderately thermophilic member of the Thaumarchaeotal order Nitrosopumilales (NP) that contains many mesophilic marine strains. We examined its membrane lipid composition at different growth temperatures (37°C, 46°C, and 50°C). Its lipids were all membrane-spanning glycerol dialkyl glycerol tetraethers (GDGTs), with 0 to 4 cyclopentane moieties. Crenarchaeol (cren), the characteristic Thaumarchaeotal GDGT, and its isomer (crenʹ) were present in high abundance (30 to 70%). The GDGT polar headgroups were mono-, di-, and trihexoses and hexose/phosphohexose. The ratio of glycolipid to phospholipid GDGTs was highest in the cultures grown at 50°C. With increasing growth temperatures, the relative contributions of cren and crenʹ increased, while those of GDGT-0 to GDGT-4 (including isomers) decreased. TEX86 (tetraether index of tetraethers consisting of 86 carbons)-derived temperatures were much lower than the actual growth temperatures, further demonstrating that TEX86 does not accurately reflect the membrane lipid adaptation of thermophilic Thaumarchaeota. As the temperature increased, specific GDGTs changed relative to their isomers, possibly representing temperature adaption-induced changes in cyclopentane ring stereochemistry. Comparison of a wide range of Thaumarchaeotal core lipid compositions revealed that the “Ca. Nitrosotenuis uzonensis” cultures clustered separately from other members of the NP order and the Nitrososphaerales (NS) order. While phylogeny generally seems to have a strong influence on GDGT distribution, our analysis of “Ca. Nitrosotenuis uzonensis” demonstrates that its terrestrial, higher-temperature niche has led to a lipid composition that clearly differentiates it from other NP members and that this difference is mostly driven by its high crenʹ content. IMPORTANCE For Thaumarchaeota, the ratio of their glycerol dialkyl glycerol tetraether (GDGT) lipids depends on growth temperature, a premise that forms the basis of the widely applied TEX86 paleotemperature proxy. A thorough understanding of which GDGTs are produced by which Thaumarchaeota and what the effect of temperature is on their GDGT composition is essential for constraining the TEX86 proxy. “Ca. Nitrosotenuis uzonensis” is a moderately thermophilic thaumarchaeote enriched from a thermal spring, setting it apart in its environmental niche from the other marine mesophilic members of its order. Indeed, we found that the GDGT composition of “Ca. Nitrosotenuis uzonensis” cultures was distinct from those of other members of its order and was more similar to those of other thermophilic, terrestrial Thaumarchaeota. This suggests that while phylogeny has a strong influence on GDGT distribution, the environmental niche that a thaumarchaeote inhabits also shapes its GDGT composition.
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the vertical distribution of Thaumarchaeota in the water column of lake malawi inferred from core and intact polar tetraether lipids
Organic Geochemistry, 2019Co-Authors: Jaap Sinninghe S Damste, Ellen C Hopmans, Dervla Meegan Kumar, Martijn Woltering, Stefan Schouten, Josef P WerneAbstract:Abstract Several long paleoclimate records generated from Lake Malawi sediments rely on an assumption that the TEX86 paleothermometer reflects annual mean lake surface temperatures. Thaumarchaeota, the producers of the isoprenoid glycerol dialkyl glycerol tetraether (iGDGT) lipids that are the basis of the TEX86 proxy, can occupy a wide range of habitats in the upper water column of lacustrine systems, so it is crucial to specifically constrain the ecology of Thaumarchaeota in Lake Malawi to properly interpret its sedimentary TEX86 record. To investigate the spatial and vertical distribution of Thaumarchaeotal iGDGT production in Lake Malawi, suspended particulate matter (SPM) was collected from the upper water column (>300 m) at three sites spanning the north, central, and south basins of the lake and analyzed for intact polar (IPL) and core (CL) iGDGT lipid abundances. Samples were collected in January during the austral summer when the lake is strongly stratified. Concentrations of the most labile IPL, hexose-phosphohexose (HPH)-crenarchaeol, were greatest just below the deep chlorophyll maximum at ∼50 m water depth in the deeper north and central basins and ∼30 m in the shallow south basin. Maximum CL concentrations occur below the maximum HPH-crenarchaeol concentrations and therefore possibly reflect the accumulation of recently produced IPL GDGT degradation products. If the export of CLs to the sediments is dominated by this CL pool, sedimentary TEX86 would reflect Thaumarchaeota living within the thermocline during the stratified season and therefore may have a cool bias rather than reflecting true surface water temperatures. An increase in abundances of GDGT-2, crenarchaeol isomer, and monohexose (MH)-crenarchaeol at ∼150–200 m suggests that a secondary Thaumarchaeotal population, likely Group I.1b Thaumarchaeota, inhabits the subsurface water column near the anoxic-suboxic boundary. Total production of iGDGTs by this group appears to be much lower than the surface-dwelling clade, but its imprint on sedimentary TEX86 is unknown. An analysis of iGDGT production in the water column throughout the annual cycle is needed to resolve the timing and magnitude of export of CLs to the sediments from these two Thaumarchaeotal populations.
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depth related distribution of a key gene of the tetraether lipid biosynthetic pathway in marine Thaumarchaeota
Environmental Microbiology, 2015Co-Authors: Laura Villanueva, Stefan Schouten, Jaap Sinninghe S DamsteAbstract:The distribution of isoprenoid glycerol dialkyl glycerol tetraethers (GDGT) lipids synthesized by Thaumarchaeota has been shown to be temperature-dependent in world oceans. Depth-related differences in the ammonia monooxygenase (amoA) of Thaumarchaeota have led to the classification of ‘shallow’ and ‘deep water’ clusters, potentially affecting GDGT distributions. Here, we investigate if this classification is also reflected in a key gene of the Thaumarchaeotal lipid biosynthetic pathway coding for geranylgeranylglyceryl phosphate (GGGP) synthase. We investigated metagenomic databases, suspended particulate matter and surface sediment of the Arabian Sea oxygen minimum zone. These revealed significant differences in amoA and GGGP synthase between ‘shallow’ and ‘deep water’ Thaumarchaeota. Intriguingly, amoA and GGGP synthase sequences of benthic Thaumarchaeota clustered with the ‘shallow water’ rather than with ‘deep water’ Thaumarchaeota. This suggests that pressure and temperature are unlikely factors that drive the differentiation, and suggests an important role of ammonia concentration that is higher in benthic and ‘shallow water’ niches. Analysis of the relative abundance of GDGTs in the Arabian Sea and in globally distributed surface sediments showed differences in GDGT distributions from subsurface to deep waters that may be explained by differences in the GGGP synthase, suggesting a genetic control on GDGT distributions.
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linking isoprenoidal gdgt membrane lipid distributions with gene abundances of ammonia oxidizing Thaumarchaeota and uncultured crenarchaeotal groups in the water column of a tropical lake lake challa east africa
Environmental Microbiology, 2013Co-Authors: L K Buckles, Laura Villanueva, Johan W H Weijers, Dirk Verschuren, Jaap Sinninghe S DamsteAbstract:Stratified lakes are important reservoirs of microbial diversity and provide habitats for niche differentiation of Archaea. In this study, we used a lipid biomarker/DNA-based approach to reveal the diversity and abundance of Archaea in the water column of Lake Challa (East Africa). Concentrations of intact polar lipid (IPL) crenarchaeol, a specific biomarker of Thaumarchaeota, were enhanced (1ng l(-1)) at the oxycline/nitrocline. The predominance of the more labile IPL hexose-phosphohexose crenarchaeol indicated the presence of an actively living community of Thaumarchaeota. Archaeal 16S rRNA clone libraries revealed the presence of Thaumarchaeotal groups 1.1a and 1.1b at and above the oxycline. In the anoxic deep water, amoA gene abundance was an order of magnitude lower than at the oxycline and high abundance (approximate to 90ng l(-1)) of an IPL with the acyclic glycerol dialkyl glycerol tetraether (GDGT-0) was evident. The predominance of archaeal 16S rRNA sequences affiliated to the uncultured crenarchaeota groups 1.2 and miscellaneous crenarchaeotic group (MCG) points to an origin of GDGT-0 from uncultured crenarchaeota. This study demonstrates the importance of thermal stratification and nutrient availability in the distribution of archaeal groups in lakes, which is relevant to constrain and validate temperature proxies based on archaeal GDGTs (i.e. TEX86).
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recognition of early eocene global carbon isotope excursions using lipids of marine Thaumarchaeota
Earth and Planetary Science Letters, 2013Co-Authors: Petra L Schoon, Jaap Sinninghe S Damste, Claus Heilmannclausen, Bo Pagh Schultz, Appy Sluijs, Stefan SchoutenAbstract:The Paleocene–Eocene Thermal Maximum (PETM; ∼56 Ma) and Eocene Thermal Maximum 2 (ETM2; ∼53 Ma) are geological short (<200,000 years) episodes of extreme global warming and environmental change. Both the PETM and ETM2 are associated with the injection of 13C-depleted carbon into the ocean–atmosphere system as revealed through a globally recognized carbon isotope excursion (CIE) and massive dissolution of deep sea carbonate. However, the magnitude of these CIEs vary with the type of fossil matter, i.e. multiple carbonate phases, bulk organic matter, and terrestrial and marine biomarker lipids, making it difficult to constrain the actual CIE in atmospheric and oceanic carbon pools. Here we analyzed the stable carbon isotopic composition (δ13C) of glycerol dibiphytanyl glycerol tetraether lipids (GDGTs) derived from marine Thaumarchaeota in sediments deposited during the PETM in the North Sea Basin and ETM2 in the Arctic Ocean. The δ13C values of these lipids are potentially directly recording variations in δ13C dissolved inorganic carbon (DIC) and can thus provide a record of marine δ13C DIC across both these Eocene carbon cycle perturbations. Reconstructed pre-CIE δ13CDIC values are slightly lower (0.5–1‰) than modern day values, possibly because Thaumarchaeotal lipids are not only derived from surface waters but also from 13C-depleted subsurface waters. Their values decrease by ∼3.6 (±0.3) ‰ and ∼2.5 (±0.7)‰ during the PETM and ETM2, respectively. The CIE in crenarchaeol for ETM2 is higher than that in marine calcite from other locations, possibly because of the admixture of deep water 13C-depleted CO2 generated by the euxinic conditions that developed occasionally during ETM2. However, the reconstructed PETM CIE lies close to the CIE inferred from marine calcite, suggesting that the δ13C record of crenarchaeol may document changes in marine DIC during the PETM in the North Sea Basin. The δ13C of Thaumarchaeotal lipids may thus be a novel tool to reconstruct the δ13C of DIC in sediments that are devoid of carbonates, but relatively rich in organic matter, such as shallow marine coastal settings.
James T Hollibaugh - One of the best experts on this subject based on the ideXlab platform.
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Correction: Single-cell genomics shedding light on marine Thaumarchaeota diversification.
The ISME Journal, 2019Co-Authors: Bradley B Tolar, Chuanlun L. Zhang, Mary Ann Moran, Brandon K Swan, Ramunas Stepanauskas, James T HollibaughAbstract:An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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phylogenomics suggests oxygen availability as a driving force in Thaumarchaeota evolution
The ISME Journal, 2019Co-Authors: Xiaoyuan Feng, Brandon K Swan, Ramunas Stepanauskas, Yongjie Huang, Hui Wang, Zhong Hu, Scott Clingenpeel, Miguel M Fonseca, David Posada, James T HollibaughAbstract:Ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread in marine and terrestrial habitats, playing a major role in the global nitrogen cycle. However, their evolutionary history remains unexplored, which limits our understanding of their adaptation mechanisms. Here, our comprehensive phylogenomic tree of Thaumarchaeota supports three sequential events: origin of AOA from terrestrial non-AOA ancestors, colonization of the shallow ocean, and expansion to the deep ocean. Careful molecular dating suggests that these events coincided with the Great Oxygenation Event around 2300 million years ago (Mya), and oxygenation of the shallow and deep ocean around 800 and 635–560 Mya, respectively. The first transition was likely enabled by the gain of an aerobic pathway for energy production by ammonia oxidation and biosynthetic pathways for cobalamin and biotin that act as cofactors in aerobic metabolism. The first transition was also accompanied by the loss of dissimilatory nitrate and sulfate reduction, loss of oxygen-sensitive pyruvate oxidoreductase, which reduces pyruvate to acetyl-CoA, and loss of the Wood–Ljungdahl pathway for anaerobic carbon fixation. The second transition involved gain of a K+ transporter and of the biosynthetic pathway for ectoine, which may function as an osmoprotectant. The third transition was accompanied by the loss of the uvr system for repairing ultraviolet light-induced DNA lesions. We conclude that oxygen availability drove the terrestrial origin of AOA and their expansion to the photic and dark oceans, and that the stressors encountered during these events were partially overcome by gene acquisitions from Euryarchaeota and Bacteria, among other sources.
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light and temperature control the seasonal distribution of Thaumarchaeota in the south atlantic bight
The ISME Journal, 2018Co-Authors: Bradley B Tolar, Natalie J Wallsgrove, Brian N Popp, Meredith J Ross, Jelani B Cheek, Corinne M Sweeney, James T HollibaughAbstract:Mid-summer peaks in the abundance of Thaumarchaeota and nitrite concentration observed on the Georgia, USA, coast could result from in situ activity or advection of populations from another source. We collected data on the distribution of Thaumarchaeota, ammonia-oxidizing betaproteobacteria (AOB), Nitrospina, environmental variables and rates of ammonia oxidation during six cruises in the South Atlantic Bight (SAB) from April to November 2014. These data were used to examine seasonality of nitrification in offshore waters and to test the hypothesis that the bloom was localized to inshore waters. The abundance of Thaumarchaeota marker genes (16S rRNA and amoA) increased at inshore and nearshore stations starting in July and peaked in August at >107 copies L−1. The bloom did not extend onto the mid-shelf, where Thaumarchaeota genes ranged from 103 to 105 copies L−1. Ammonia oxidation rates (AO) were highest at inshore stations during summer (to 840 nmol L−1 d−1) and were always at the limit of detection at mid-shelf stations. Nitrite concentrations were correlated with AO (R = 0.94) and were never elevated at mid-shelf stations. Gene sequences from samples collected at mid-shelf stations generated using Archaea 16S rRNA primers were dominated by Euryarchaeota; sequences from inshore and nearshore stations were dominated by Thaumarchaeota. Thaumarchaeota were also abundant at depth at the shelf-break; however, this population was phylogenetically distinct from the inshore/nearshore population. Our analysis shows that the bloom is confined to inshore waters during summer and suggests that Thaumarchaeota distributions in the SAB are controlled primarily by photoinhibition and secondarily by water temperature.
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oxidation of urea derived nitrogen by Thaumarchaeota dominated marine nitrifying communities
Environmental Microbiology, 2017Co-Authors: Bradley B Tolar, Natalie J Wallsgrove, Brian N Popp, James T HollibaughAbstract:Urea nitrogen has been proposed to contribute significantly to nitrification by marine thaumarchaeotes. These inferences are based on distributions of thaumarchaeote urease genes rather than activity measurements. We found that ammonia oxidation rates were always higher than oxidation rates of urea-derived N in samples from coastal Georgia, USA (means±SEM: 382±35 versus 73±24 nmol L−1 d−1, Mann-Whitney U-test p 0.05). Urea-derived N was relatively more important in samples from Antarctic continental shelf waters, though the difference was not statistically significant (19.4±4.8 versus 12.0±2.7 nmol L−1 d−1, p>0.05). We found only weak correlations between oxidation rates of urea-derived N and the abundance or transcription of putative Thaumarchaeota ureC genes. Dependence on urea-derived N does not appear to be directly related to pH or ammonium concentrations. Competition experiments and release of 15NH3 suggest that urea is hydrolyzed to ammonia intracellularly, then a portion is lost to the dissolved pool. The contribution of urea-derived N to nitrification appears to be minor in temperate coastal waters, but may represent a significant portion of the nitrification flux in Antarctic coastal waters. This article is protected by copyright. All rights reserved.
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chemical speciation of copper in a salt marsh estuary and bioavailability to Thaumarchaeota
Frontiers in Marine Science, 2017Co-Authors: Hannah Whitby, James T Hollibaugh, Constant M G Van Den BergAbstract:The concentrations of dissolved copper (Cud), copper-binding ligands, thiourea-type thiols and humic substances (HSCu) were measured in estuarine waters adjacent to Sapelo Island, Georgia, USA, on a monthly basis from April to December 2014. Here we present the seasonal cycle of copper speciation within the estuary and compare it to the development of an annually occurring bloom of Ammonia Oxidising Archaea (AOA), which require copper for many enzymes. Two types of complexing ligands (L1 and L2) were found to dominate with mean complex stabilities (log K′CuL) of 14.5 and 12.8. Strong complexation resulted in lowering the concentration of free cupric ion (Cu2+) to femtomolar (fM) levels throughout the study and to sub-fM levels during the summer months. A Thaumarchaeota bloom during this period suggests that this organism manages to grow at very low Cu2+ concentrations. Correlation of the concentration of the L1 ligand class with a thiourea-type thiol and the L2 ligand class with HSCu provide an interesting dimension to the identity of the ligand classes. Due to the stronger complex stability, 82 - 99% of the copper was bound to L1. Thiourea-type thiols typically form Cu(I) species, which would suggest that up to ~90% copper could be present as Cu(I) in this region. In view of the very low concentration of free copper (pCu >15 at the onset and during the bloom) and a reputedly high requirement for copper, it is likely that the Thaumarchaeota are able to access thiol-bound copper directly.
Christa Schleper - One of the best experts on this subject based on the ideXlab platform.
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candidatus nitrosocaldus cavascurensis an ammonia oxidizing extremely thermophilic archaeon with a highly mobile genome
Frontiers in Microbiology, 2018Co-Authors: Michaela Stieglmeier, Sophie S Abby, Michael Melcher, Melina Kerou, Mart Krupovic, Kevin Pfeifer, Claudia Rossel, Christa SchleperAbstract:Ammonia oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread in moderate environments but their occurrence and activity has also been demonstrated in hot springs. Here we present the first enrichment of a thermophilic representative with a sequenced genome, which facilitates the search for adaptive strategies and for traits that shape the evolution of Thaumarchaeota. Candidatus Nitrosocaldus cavascurensis has been enriched from a hot spring in Ischia, Italy. It grows optimally at 68 • C under chemolithoautotrophic conditions on ammonia or urea converting ammonia stoichiometrically into nitrite with a generation time of approximately 23 h. Phylogenetic analyses based on ribosomal proteins place the organism as a sister group to all known mesophilic AOA. The 1.58 Mb genome of Ca. N. cavascurensis harbors an amoAXCB gene cluster encoding ammonia monooxygenase and genes for a 3-hydroxypropionate/4-hydroxybutyrate pathway for autotrophic carbon fixation, but also genes that indicate potential alternative energy metabolisms. Although a bona fide gene for nitrite reductase is missing, the organism is sensitive to NO-scavenging, underlining the potential importance of this compound for AOA metabolism. Ca. N. cavascurensis is distinct from all other AOA in its gene repertoire for replication, cell division and repair. Its genome has an impressive array of mobile genetic elements and other recently acquired gene sets, including conjugative systems, a provirus, transposons and cell appendages. Some of these elements indicate recent exchange with the environment, whereas others seem to have been domesticated and might convey crucial metabolic traits.
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candidatus nitrosocaldus cavascurensis an ammonia oxidizing extremely thermophilic archaeon with a highly mobile genome
bioRxiv, 2017Co-Authors: Sophie S Abby, Michaela Stieglmeier, Michael Melcher, Melina Kerou, Mart Krupovic, Kevin Pfeifer, Claudia Rossel, Christa SchleperAbstract:Ammonia oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread in moderate environments but their occurrence and activity has also been demonstrated in hot springs. Here we present the first cultivated thermophilic representative with a sequenced genome, which allows to search for adaptive strategies and for traits that shape the evolution of Thaumarchaeota. Candidatus Nitrosocaldus cavascurensis has been cultivated from a hot spring in Ischia, Italy. It grows optimally at 68°C under chemolithoautotrophic conditions on ammonia or urea converting ammonia stoichiometrically into nitrite with a generation time of approximately 25h. Phylogenetic analyses based on ribosomal proteins place the organism as a sister group to all known mesophilic AOA. The 1.58 Mb genome of Ca. N. cavascurensis harbors an amoAXCB gene cluster encoding ammonia monooxygenase, genes for a 3-hydroxypropionate/4-hydroxybutyrate pathway for autotrophic carbon fixation, but also genes that indicate potential alternative energy metabolisms. Although a bona fide gene for nitrite reductase is missing, the organism is sensitive to NO-scavenging, underlining the importance of this compound for AOA metabolism. Ca. N. cavascurensis is distinct from all other AOA in its gene repertoire for replication, cell division and repair. Its genome has an impressive array of mobile genetic elements and other recently acquired gene sets, including conjugative systems, a provirus, transposons and cell appendages. Some of these elements indicate recent exchange with the environment, whereas others seem to have been domesticated and might convey crucial metabolic traits.
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pathways and key intermediates required for obligate aerobic ammonia dependent chemolithotrophy in bacteria and Thaumarchaeota
The ISME Journal, 2016Co-Authors: Jessica A Kozlowski, Michaela Stieglmeier, Christa Schleper, Martin G. Klotz, Lisa Y SteinAbstract:Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota
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26 the phylum Thaumarchaeota
2014Co-Authors: Michaela Stieglmeier, Ricardo Eloy J Alves, Christa SchleperAbstract:Thaumarchaeota represent a unique phylum within the domain Archaea that embraces ammonia-oxidizing organisms from soil, marine waters, and hot springs (currently two pure cultures and 13 enrichments), as well as many lineages represented only by environmental sequences from virtually every habitat that has been screened. All cultivated Thaumarchaeota perform the first step in nitrification, i.e., they oxidize ammonia to nitrite aerobically. They live under autotrophic conditions and fix CO2, but some are dependent on the presence of other bacteria or small amounts of organic material. Different from bacterial ammonia oxidizers, all cultivated Thaumarchaeota are adapted to comparably low amounts of substrate (ammonia) and inhabit not only moderate but also extreme environments, such as hot springs and acidic soils. All cultivated strains contain tetraether lipids with crenarchaeol, a Thaumarchaeota-specific core lipid.
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metagenomics of kamchatkan hot spring filaments reveal two new major hyper thermophilic lineages related to Thaumarchaeota
Research in Microbiology, 2013Co-Authors: Laila J Reigstad, Christa Schleper, Anja Spang, Anders Lanzen, Thomas Weinmaier, Thomas Rattei, Celine BrochierarmanetAbstract:Based on phylogenetic analyses and gene distribution patterns of a few complete genomes, a new distinct phylum within the Archaea, the Thaumarchaeota, has recently been proposed. Here we present analyses of six archaeal fosmid sequences derived from a microbial hot spring community in Kamchatka. The phylogenetic analysis of informational components (ribosomal RNAs and proteins) reveals two major (hyper-)thermophilic clades (“Hot Thaumarchaeota-related Clade” 1 and 2, HTC1 and HTC2) related to Thaumarchaeota, representing either deep branches of this phylum or a new archaeal phylum and provides information regarding the ancient evolution of Archaea and their evolutionary links with Eukaryotes.
Celine Brochierarmanet - One of the best experts on this subject based on the ideXlab platform.
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metagenomics of kamchatkan hot spring filaments reveal two new major hyper thermophilic lineages related to Thaumarchaeota
Research in Microbiology, 2013Co-Authors: Laila J Reigstad, Christa Schleper, Anja Spang, Anders Lanzen, Thomas Weinmaier, Thomas Rattei, Celine BrochierarmanetAbstract:Based on phylogenetic analyses and gene distribution patterns of a few complete genomes, a new distinct phylum within the Archaea, the Thaumarchaeota, has recently been proposed. Here we present analyses of six archaeal fosmid sequences derived from a microbial hot spring community in Kamchatka. The phylogenetic analysis of informational components (ribosomal RNAs and proteins) reveals two major (hyper-)thermophilic clades (“Hot Thaumarchaeota-related Clade” 1 and 2, HTC1 and HTC2) related to Thaumarchaeota, representing either deep branches of this phylum or a new archaeal phylum and provides information regarding the ancient evolution of Archaea and their evolutionary links with Eukaryotes.
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horizontal gene transfer of a chloroplast dnaj fer protein to Thaumarchaeota and the evolutionary history of the dnak chaperone system in archaea
BMC Evolutionary Biology, 2012Co-Authors: Celine Petitjean, David Moreira, Purificacion Lopezgarcia, Celine BrochierarmanetAbstract:Background: In 2004, we discovered an atypical protein in metagenomic data from marine Thaumarchaeotal species. This protein, referred as DnaJ-Fer, is composed of a J domain fused to a Ferredoxin (Fer) domain. Surprisingly, the same protein was also found in Viridiplantae (green algae and land plants). Because J domain-containing proteins are known to interact with the major chaperone DnaK/Hsp70, this suggested that a DnaK protein was present in Thaumarchaeota. DnaK/Hsp70, its co-chaperone DnaJ and the nucleotide exchange factor GrpE are involved, among others, in heat shocks and heavy metal cellular stress responses. Results: Using phylogenomic approaches we have investigated the evolutionary history of the DnaJ-Fer protein and of interacting proteins DnaK, DnaJ and GrpE in Thaumarchaeota. These proteins have very complex histories, involving several inter-domain horizontal gene transfers (HGTs) to explain the contemporary distribution of these proteins in archaea. These transfers include one from Cyanobacteria to Viridiplantae and one from Viridiplantae to Thaumarchaeota for the DnaJ-Fer protein, as well as independent HGTs from Bacteria to mesophilic archaea for the DnaK/DnaJ/GrpE system, followed by HGTs among mesophilic and thermophilic archaea. Conclusions: We highlight the chimerical origin of the set of proteins DnaK, DnaJ, GrpE and DnaJ-Fer in Thaumarchaeota and suggest that the HGT of these proteins has played an important role in the adaptation of several archaeal groups to mesophilic and thermophilic environments from hyperthermophilic ancestors. Finally, the evolutionary history of DnaJ-Fer provides information useful for the relative dating of the diversification of Archaeplastida and Thaumarchaeota.
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spotlight on the Thaumarchaeota
The ISME Journal, 2012Co-Authors: Celine Brochierarmanet, Simonetta Gribaldo, Patrick ForterreAbstract:Over the last two decades, many new groups of deeply branching uncultivated archaea have been unveiled by molecular screening of 16S rRNA genes. Among these, Thaumarchaeota (Brochier-Armanet et al., 2008) are now known to represent a highly diversified and ancient phylum present in a wide variety of ecosystems, including marine and fresh waters, soils and also hot environments (Pester et al., 2011). The Thaumarchaeota have rapidly gained much attention after the discovery that some of them are able to oxidize ammonia aerobically, providing the first example of nitrification in the Archaea and therefore extending the range of microorganisms capable of this important metabolism, which was previously thought to be restricted to a few proteobacterial lineages (Konneke et al., 2005). The interest raised by Thaumarchaeota is witnessed by the growing availability over the last 4 years of isolated representatives (or enrichment cultures) and of genomic data. This opens up a whole new perspective on the diversity of Archaea and on ancient evolution.
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distinct gene set in two different lineages of ammonia oxidizing archaea supports the phylum Thaumarchaeota
Trends in Microbiology, 2010Co-Authors: Anja Spang, Celine Brochierarmanet, Thomas Rattei, Eva Spieck, David A. Stahl, Roland Hatzenpichler, Patrick Tischler, Wolfgang R Streit, Michael WagnerAbstract:Globally distributed archaea comprising ammonia oxidizers of moderate terrestrial and marine environments are considered the most abundant archaeal organisms on Earth. Based on 16S rRNA phylogeny, initial assignment of these archaea was to the Crenarchaeota. By contrast, features of the first genome sequence from a member of this group suggested that they belong to a novel phylum, the Thaumarchaeota. Here, we re-investigate the Thaumarchaeota hypothesis by including two newly available genomes, that of the marine ammonia oxidizer Nitrosopumilus maritimus and that of Nitrososphaera gargensis, a representative of another evolutionary lineage within this group predominantly detected in terrestrial environments. Phylogenetic studies based on r-proteins and other core genes, as well as comparative genomics, confirm the assignment of these organisms to a separate phylum and reveal a Thaumarchaeota-specific set of core informational processing genes, as well as potentially ancestral features of the archaea.
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a dna topoisomerase ib in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of archaea and eucarya
Biology Direct, 2008Co-Authors: Celine Brochierarmanet, Simonetta Gribaldo, Patrick ForterreAbstract:DNA topoisomerase IB (TopoIB) was thought for a long time to be a eukaryotic specific enzyme. A shorter version was then found in viruses and later on in several bacteria, but not in archaea. Here, we show that a eukaryotic-like TopoIB is present in the recently sequenced genomes of two archaea of the newly proposed phylum Thaumarchaeota. Phylogenetic analyses suggest that a TopoIB was present in the last common ancestor of Archaea and Eucarya. This finding indicates that the last common ancestor of Archaea and Eucarya may have harboured a DNA genome.
Bradley B Tolar - One of the best experts on this subject based on the ideXlab platform.
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Correction: Single-cell genomics shedding light on marine Thaumarchaeota diversification.
The ISME Journal, 2019Co-Authors: Bradley B Tolar, Chuanlun L. Zhang, Mary Ann Moran, Brandon K Swan, Ramunas Stepanauskas, James T HollibaughAbstract:An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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Depth distributions of nitrite reductase (nirK) gene variants reveal spatial dynamics of thaumarchaeal ecotype populations in coastal Monterey Bay
Environmental Microbiology, 2019Co-Authors: Linta Reji, Bradley B Tolar, Jason M. Smith, Francisco P. Chavez, Christopher A. FrancisAbstract:Ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota are key players in nutrient cycling, yet large gaps remain in our understanding of their ecology and metabolism. Despite multiple lines of evidence pointing to a central role for copper-containing nitrite reductase (NirK) in AOA metabolism, the thaumarchaeal nirK gene is rarely studied in the environment. In this study, we examine the diversity of nirK in the marine pelagic environment, in light of previously described ecological patterns of pelagic thaumarchaeal populations. Phylogenetic analyses show that nirK better resolves diversification patterns of marine Thaumarchaeota, compared to the conventionally used marker gene amoA. Specifically, we demonstrate that the three major phylogenetic clusters of marine nirK correspond to the three 'ecotype' populations of pelagic Thaumarchaeota. In this context, we further examine the relative distributions of the three variant groups in metagenomes and metatranscriptomes representing two depth profiles in coastal Monterey Bay. Our results reveal that nirK effectively tracks the dynamics of thaumarchaeal ecotype populations, particularly finer-scale diversification patterns within major lineages. We also find evidence for multiple copies of nirK per genome in a fraction of thaumarchaeal cells in the water column, which must be taken into account when using it as a molecular marker.
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Differential co-occurrence relationships shaping ecotype diversification within Thaumarchaeota populations in the coastal ocean water column
The ISME Journal, 2019Co-Authors: Linta Reji, Bradley B Tolar, Jason M. Smith, Francisco P. Chavez, Christopher A. FrancisAbstract:Ecological factors contributing to depth-related diversification of marine Thaumarchaeota populations remain largely unresolved. To investigate the role of potential microbial associations in shaping thaumarchaeal ecotype diversification, we examined co-occurrence relationships in a community composition dataset (16S rRNA V4-V5 region) collected as part of a 2-year time series in coastal Monterey Bay. Ecotype groups previously defined based on functional gene diversity—water column A (WCA), water column B (WCB) and Nitrosopumilus -like clusters—were recovered in the thaumarchaeal 16S rRNA gene phylogeny. Networks systematically reflected depth-related patterns in the abundances of ecotype populations, suggesting thaumarchaeal ecotypes as keystone members of the microbial community below the euphotic zone. Differential environmental controls on the ecotype populations were further evident in subnetwork modules showing preferential co-occurrence of OTUs belonging to the same ecotype cluster. Correlated abundances of Thaumarchaeota and heterotrophic bacteria (e.g., Bacteroidetes , Marinimicrobia and Gammaproteobacteria) indicated potential reciprocal interactions via dissolved organic matter transformations. Notably, the networks recovered ecotype-specific associations between thaumarchaeal and Nitrospina OTUs. Even at depths where WCB-like Thaumarchaeota dominated, Nitrospina OTUs were found to preferentially co-occur with WCA-like and Nitrosopumilus -like thaumarchaeal OTUs, highlighting the need to investigate the ecological implications of the composition of nitrifier assemblages in marine waters.
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light and temperature control the seasonal distribution of Thaumarchaeota in the south atlantic bight
The ISME Journal, 2018Co-Authors: Bradley B Tolar, Natalie J Wallsgrove, Brian N Popp, Meredith J Ross, Jelani B Cheek, Corinne M Sweeney, James T HollibaughAbstract:Mid-summer peaks in the abundance of Thaumarchaeota and nitrite concentration observed on the Georgia, USA, coast could result from in situ activity or advection of populations from another source. We collected data on the distribution of Thaumarchaeota, ammonia-oxidizing betaproteobacteria (AOB), Nitrospina, environmental variables and rates of ammonia oxidation during six cruises in the South Atlantic Bight (SAB) from April to November 2014. These data were used to examine seasonality of nitrification in offshore waters and to test the hypothesis that the bloom was localized to inshore waters. The abundance of Thaumarchaeota marker genes (16S rRNA and amoA) increased at inshore and nearshore stations starting in July and peaked in August at >107 copies L−1. The bloom did not extend onto the mid-shelf, where Thaumarchaeota genes ranged from 103 to 105 copies L−1. Ammonia oxidation rates (AO) were highest at inshore stations during summer (to 840 nmol L−1 d−1) and were always at the limit of detection at mid-shelf stations. Nitrite concentrations were correlated with AO (R = 0.94) and were never elevated at mid-shelf stations. Gene sequences from samples collected at mid-shelf stations generated using Archaea 16S rRNA primers were dominated by Euryarchaeota; sequences from inshore and nearshore stations were dominated by Thaumarchaeota. Thaumarchaeota were also abundant at depth at the shelf-break; however, this population was phylogenetically distinct from the inshore/nearshore population. Our analysis shows that the bloom is confined to inshore waters during summer and suggests that Thaumarchaeota distributions in the SAB are controlled primarily by photoinhibition and secondarily by water temperature.
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oxidation of urea derived nitrogen by Thaumarchaeota dominated marine nitrifying communities
Environmental Microbiology, 2017Co-Authors: Bradley B Tolar, Natalie J Wallsgrove, Brian N Popp, James T HollibaughAbstract:Urea nitrogen has been proposed to contribute significantly to nitrification by marine thaumarchaeotes. These inferences are based on distributions of thaumarchaeote urease genes rather than activity measurements. We found that ammonia oxidation rates were always higher than oxidation rates of urea-derived N in samples from coastal Georgia, USA (means±SEM: 382±35 versus 73±24 nmol L−1 d−1, Mann-Whitney U-test p 0.05). Urea-derived N was relatively more important in samples from Antarctic continental shelf waters, though the difference was not statistically significant (19.4±4.8 versus 12.0±2.7 nmol L−1 d−1, p>0.05). We found only weak correlations between oxidation rates of urea-derived N and the abundance or transcription of putative Thaumarchaeota ureC genes. Dependence on urea-derived N does not appear to be directly related to pH or ammonium concentrations. Competition experiments and release of 15NH3 suggest that urea is hydrolyzed to ammonia intracellularly, then a portion is lost to the dissolved pool. The contribution of urea-derived N to nitrification appears to be minor in temperate coastal waters, but may represent a significant portion of the nitrification flux in Antarctic coastal waters. This article is protected by copyright. All rights reserved.
