Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota

Spang, Anja; Hatzenpichler, Roland; Brochier-Armanet, Céline; Rattei, Thomas; Tischler, Patrick; Spieck, Eva; Streit, Wolfgang R.; Stahl, David A.; Wagner, Michael; Schleper, Christa

doi:10.1016/j.tim.2010.06.003

Cited by 423 publications

(325 citation statements)

References 79 publications

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“…Both the concatenated ribosomal protein and 16S/ 23S trees are built as consensus trees using 18 and 16 phylogenetic analyses, respectively, and both approaches yield consistent phylogenetic placement of the NAG1 lineage. Several universally conserved housekeeping genes have been utilized previously for phylum-level patterning in the Archaea (Spang et al, 2010), and this same analysis of de novo NAG1 assemblies supports the conclusion that NAG1 organisms are representatives of a phylum-level lineage (Supplementary Figure S2; Supplementary Table S2). Specifically, topoisomerase and translation proteins show a distinct pattern difference in NAG1 populations compared with other Archaea.…”

Section: Metagenome Assembliessupporting

confidence: 73%

“…A fourth phylum (Nanoarchaeota) was described after the discovery and genome analysis of the symbiont species Candidatus Nanoarchaeum equitans , although placement of the Nanoarchaeota as a new phylum is still debated and is based primarily on a single genome sequence and 16S rRNA sequences (Brochier et al, 2005). More recently, the candidate phylum Thaumarchaeota was proposed (Brochier-Armanet et al, 2008), and detailed analysis of genome sequence from multiple representatives of this lineage provides convincing evidence that this group of organisms is significantly different from other recognized phyla within the Archaea (Spang et al, 2010). Specifically, phylogenetic analysis of housekeeping genes (that is, ribosomal proteins and enzymes involved in translation, replication, cell division and repair) from Nitrosopumilus maritimus, Nitrososphaera gargensis and Candidatus Cenarchaeum symbiosum provides strong evidence for the unique and distinguishing genetic features of members of this phylum.…”

Section: Introductionmentioning

confidence: 99%

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Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park

et al. 2012

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Geothermal systems in Yellowstone National Park (YNP) provide an outstanding opportunity to understand the origin and evolution of metabolic processes necessary for life in extreme environments including low pH, high temperature, low oxygen and elevated concentrations of reduced iron. Previous phylogenetic studies of acidic ferric iron mats from YNP have revealed considerable diversity of uncultivated and undescribed archaea. The goal of this study was to obtain replicate de novo genome assemblies for a dominant archaeal population inhabiting acidic ironoxide mats in YNP. Detailed analysis of conserved ribosomal and informational processing genes indicates that the replicate assemblies represent a new candidate phylum within the domain Archaea referred to here as 'Geoarchaeota' or 'novel archaeal group 1 (NAG1)'. The NAG1 organisms contain pathways necessary for the catabolism of peptides and complex carbohydrates as well as a bacterial-like Form I carbon monoxide dehydrogenase complex likely used for energy conservation. Moreover, this novel population contains genes involved in the metabolism of oxygen including a Type A heme copper oxidase, a bd-type terminal oxidase and a putative oxygen-sensing protoglobin. NAG1 has a variety of unique bacterial-like cofactor biosynthesis and transport genes and a Type3-like CRISPR system. Discovery of NAG1 is critical to our understanding of microbial community structure and function in extant thermophilic iron-oxide mats of YNP, and will provide insight regarding the evolution of Archaea in early Earth environments that may have important analogs active in YNP today.

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Section: Metagenome Assembliessupporting

confidence: 73%

Section: Introductionmentioning

confidence: 99%

Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park

et al. 2012

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“…One sequence from CN25 and two sequences from CN75 contained single nucleotide changes (all at different positions) from this consensus sequence. Isotope fractionation by ammonia-oxidizing archaea AE Santoro and KL Casciotti Phylogenetic analyses place all three sequences within the Marine Group I archaea, now proposed as a new archaeal kingdom-the Thaumarchaeota (Brochier-Armanet et al, 2008;Spang et al, 2010;Walker et al, 2010) (Figure 2a). The 16S rRNA gene sequences from CN25 and CN75 are 100% identical to each other, and 92% identical to N. maritimus.…”

Section: Phylogeny and Physiologymentioning

confidence: 98%

Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation

2011

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Archaeal genes for ammonia oxidation are widespread in the marine environment, but direct physiological evidence for ammonia oxidation by marine archaea is limited. We report the enrichment and characterization of three strains of pelagic ammonia-oxidizing archaea (AOA) from the North Pacific Ocean that have been maintained in laboratory culture for over 3 years. Phylogenetic analyses indicate the three strains belong to a previously identified clade of water column-associated AOA and possess 16S ribosomal RNA genes and ammonia monooxygenase subunit a (amoA) genes highly similar (98-99% identity) to those recovered in DNA and complementary DNA clone libraries from the open ocean. The strains grow in natural seawaterbased liquid medium while stoichiometrically converting ammonia (NH 3 ) to nitrite (NO 2 À ). Ammonia oxidation by the enrichments is only partially inhibited by allylthiourea at concentrations known to completely inhibit cultivated ammonia-oxidizing bacteria. The three strains were used to determine the nitrogen stable isotope effect ( 15 e NH3 ) during archaeal ammonia oxidation, an important parameter for interpreting stable isotope ratios in the environment. Archaeal 15 e NH3 ranged from 13% to 41%, within the range of that previously reported for ammonia-oxidizing bacteria. Despite low amino acid identity between the archaeal and bacterial Amo proteins, their functional diversity as captured by 15 e NH3 is similar.

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“…The domain of Archaea consists of four kingdoms, the Eury-, Cren-and Nanoarchaeota as well as the recently, on the basis of genome analysis of enriched Archaea, proposed Thaumarchaeota (Brochier-Armanet et al, 2008;Spang et al, 2010), formerly classified as Group I Crenarchaeota. All Thaumarchaeota known so far are capable of ammonia oxidation (Kö nneke et al, 2005;de la Torre et al, 2008;Hatzenpichler et al, 2008;Park et al, 2010) and are widespread in non-extreme environments (DeLong, 1992;Fuhrman et al, 1992;DeLong et al, 1998;Schouten et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids in the Arabian Sea oxygen minimum zone. Part II: Selective preservation and degradation in sediments and consequences for the TEX86

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Hopmans

Reichart

et al. 2012

Geochimica et Cosmochimica Acta

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The TEX 86 is a proxy based on a ratio of pelagic archaeal glycerol dibiphytanyl glycerol tetraether lipids (GDGTs), and used for estimating past sea water temperatures. Concerns exist that in situ production of GDGTs lipids by sedimentary Archaea may affect its validity. In this study, we investigated the influence of benthic GDGT production on the TEX 86 by analyzing the concentrations and distributions of GDGTs present as intact polar lipids (IPLs) and as core lipids (CLs) in three sediment cores deposited under contrasting redox conditions across a depth range from 900 to 3000 m below sea level in and below the Arabian Sea oxygen minimum zone (OMZ). Direct analysis of IPLs with crenarchaeol as CL via HPLC/ESI-MS 2 revealed that surface sediments in the OMZ were relatively depleted in the phospholipid hexose, phosphohexose (HPH)-crenarchaeol compared to suspended particulate matter from the water column, suggesting preferential and rapid degradation of this IPL. In sediment cores recovered from deeper, more oxic environments, concentrations of HPH-crenarchaeol peaked at the surface, probably due to in situ production by ammonia-oxidizing Archaea, followed by a rapid decrease with increasing depth. No surface maximum was observed in the sediment core from within the OMZ. In contrast, the glycolipids, monohexose-crenarchaeol and dihexose-crenarchaeol, did not change in concentration with depth in the sediment, indicating that they were relatively well preserved and likely mostly derived from fossil pelagic GDGTs. These results suggest that phospholipids are more sensitive to degradation, while glycolipids might be preserved over longer time scales, in line with previous incubation and modeling studies. Furthermore, in situ produced IPL-GDGTs did not accumulate as IPLs, and did not influence the CL-TEX 86 . This suggests that in-situ produced GDGT lipids were more susceptible to degradation than fossil CL and IPL and did not accumulate as CL. In agreement, no significant changes of TEX 86 with sediment depth in the core lipids were observed. However, consistent differences between IPL-derived TEX 86 and CL-TEX 86 were found. These could be explained by a different composition of CL-GDGT of the glyco-and phospholipids, in combination with dissimilar degradation rates of phospholipids vs. glycolipids. We also observed consistent differences in both IPL-derived and CL-TEX 86 between the different cores, equivalent to 3°C when converted to temperature, despite the proximity of the core locations. These differences may potentially be due to a larger addition of GDGTs produced in deeper, colder waters to the (sub)surface-derived GDGTs for the deeper core sites.

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Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota

Cited by 423 publications

References 79 publications

Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park

Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park

Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation

Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids in the Arabian Sea oxygen minimum zone. Part II: Selective preservation and degradation in sediments and consequences for the TEX86

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