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"archaea"
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The growing tree of Archaea: new perspectives on their diversity, evolution and ecology
The Archaea occupy a key position in the Tree of Life, and are a major fraction of microbial diversity. Abundant in soils, ocean sediments and the water column, they have crucial roles in processes mediating global carbon and nutrient fluxes. Moreover, they represent an important component of the human microbiome, where their role in health and disease is still unclear. The development of culture-independent sequencing techniques has provided unprecedented access to genomic data from a large number of so far inaccessible archaeal lineages. This is revolutionizing our view of the diversity and metabolic potential of the Archaea in a wide variety of environments, an important step toward understanding their ecological role. The archaeal tree is being rapidly filled up with new branches constituting phyla, classes and orders, generating novel challenges for high-rank systematics, and providing key information for dissecting the origin of this domain, the evolutionary trajectories that have shaped its current diversity, and its relationships with Bacteria and Eukarya. The present picture is that of a huge diversity of the Archaea, which we are only starting to explore.
Journal Article
Sulfate-reducing bacteria and methanogens are involved in arsenic methylation and demethylation in paddy soils
Microbial arsenic (As) methylation and demethylation are important components of the As biogeochemical cycle. Arsenic methylation is enhanced under flooded conditions in paddy soils, producing mainly phytotoxic dimethylarsenate (DMAs) that can cause rice straighthead disease, a physiological disorder occurring widely in some rice growing regions. The key microbial groups responsible for As methylation and demethylation in paddy soils are unknown. Three paddy soils were incubated under flooded conditions. DMAs initially accumulated in the soil porewater, followed by a rapid disappearance coinciding with the production of methane. The soil from a rice straighthead disease paddy field produced a much larger amount of DMAs than the other two soils. Using metabolic inhibition, quantification of functional gene transcripts, microbial enrichment cultures and
13
C-labeled DMAs, we show that sulfate-reducing bacteria (SRB) and methanogenic archaea are involved in As methylation and demethylation, respectively, controlling the dynamics of DMAs in paddy soils. We present a model of As biogeochemical cycle in paddy soils, linking the dynamics of changing soil redox potential with arsenite mobilization, arsenite methylation and subsequent demethylation driven by different microbial groups. The model provides a basis for controlling DMAs accumulation and incidence of straighthead disease in rice.
Journal Article
Dynamic RNA acetylation revealed by quantitative cross-evolutionary mapping
N
4
-acetylcytidine (ac
4
C) is an ancient and highly conserved RNA modification that is present on tRNA and rRNA and has recently been investigated in eukaryotic mRNA
1
–
3
. However, the distribution, dynamics and functions of cytidine acetylation have yet to be fully elucidated. Here we report ac
4
C-seq, a chemical genomic method for the transcriptome-wide quantitative mapping of ac
4
C at single-nucleotide resolution. In human and yeast mRNAs, ac
4
C sites are not detected but can be induced—at a conserved sequence motif—via the ectopic overexpression of eukaryotic acetyltransferase complexes. By contrast, cross-evolutionary profiling revealed unprecedented levels of ac
4
C across hundreds of residues in rRNA, tRNA, non-coding RNA and mRNA from hyperthermophilic archaea. Ac
4
C is markedly induced in response to increases in temperature, and acetyltransferase-deficient archaeal strains exhibit temperature-dependent growth defects. Visualization of wild-type and acetyltransferase-deficient archaeal ribosomes by cryo-electron microscopy provided structural insights into the temperature-dependent distribution of ac
4
C and its potential thermoadaptive role. Our studies quantitatively define the ac
4
C landscape, providing a technical and conceptual foundation for elucidating the role of this modification in biology and disease
4
–
6
.
A method termed ac
4
C-seq is introduced for the transcriptome-wide mapping of the RNA modification
N
4
-acetylcytidine, revealing widespread temperature-dependent acetylation that facilitates thermoadaptation in hyperthermophilic archaea.
Journal Article
The effect of temperature and moisture on the source of N sub(2)O and contributions from ammonia oxidizers in an agricultural soil
In recent years, identification of the microbial sources responsible for soil N sub(2)O production has substantially advanced with the development of isotope enrichment techniques, selective inhibitors, mathematical models and the discoveries of specific N-cycling functional genes. However, little information is available to effectively quantify the N sub(2)O produced from different microbial pathways (e.g. nitrification and denitrification). Here, a super(15)N-tracing incubation experiment was conducted under controlled laboratory conditions (50, 70 and 85% water-filled pore space (WFPS) at 25 and 35 degree C). Nitrification was the main contributor to N sub(2)O production. At 50, 70 and 85% WFPS, nitrification contributed 87, 80 and 53% of total N sub(2)O production, respectively, at 25 degree C, and 86, 74 and 33% at 35 degree C. The proportion of nitrified N as N sub(2)O (P sub(N2O)) increased with temperature and moisture, except for 85% WFPS, when P sub(N2O) was lower at 35 degree C than at 25 degree C. Ammonia-oxidizing archaea (AOA) were the dominant ammonia oxidizers, but both AOA and ammonia-oxidizing bacteria (AOB) were related to N sub(2)O emitted from nitrification. AOA and AOB abundance was significantly influenced by soil moisture, more so than temperature, and decreased with increasing moisture content. These findings can be used to develop better models for simulating N sub(2)O from nitrification to inform soil management practises for improving N use efficiency.
Journal Article
Diverse hydrogen production and consumption pathways influence methane production in ruminants
Farmed ruminants are the largest source of anthropogenic methane emissions globally. The methanogenic archaea responsible for these emissions use molecular hydrogen (H
2
), produced during bacterial and eukaryotic carbohydrate fermentation, as their primary energy source. In this work, we used comparative genomic, metatranscriptomic and co-culture-based approaches to gain a system-wide understanding of the organisms and pathways responsible for ruminal H
2
metabolism. Two-thirds of sequenced rumen bacterial and archaeal genomes encode enzymes that catalyse H
2
production or consumption, including 26 distinct hydrogenase subgroups. Metatranscriptomic analysis confirmed that these hydrogenases are differentially expressed in sheep rumen. Electron-bifurcating [FeFe]-hydrogenases from carbohydrate-fermenting Clostridia (e.g.,
Ruminococcus
) accounted for half of all hydrogenase transcripts. Various H
2
uptake pathways were also expressed, including methanogenesis (
Methanobrevibacter
), fumarate and nitrite reduction (
Selenomonas
), and acetogenesis (
Blautia
). Whereas methanogenesis-related transcripts predominated in high methane yield sheep, alternative uptake pathways were significantly upregulated in low methane yield sheep. Complementing these findings, we observed significant differential expression and activity of the hydrogenases of the hydrogenogenic cellulose fermenter
Ruminococcus albus
and the hydrogenotrophic fumarate reducer
Wolinella succinogenes
in co-culture compared with pure culture. We conclude that H
2
metabolism is a more complex and widespread trait among rumen microorganisms than previously recognised. There is evidence that alternative hydrogenotrophs, including acetogenic and respiratory bacteria, can prosper in the rumen and effectively compete with methanogens for H
2
. These findings may help to inform ongoing strategies to mitigate methane emissions by increasing flux through alternative H
2
uptake pathways, including through animal selection, dietary supplementation and methanogenesis inhibitors.
Journal Article
Confounding effects of oxygen and temperature on the TEX sub( 86) signature of marine Thaumarchaeota
Marine ammonia-oxidizing archaea (AOA) are among the most abundant of marine microorganisms, spanning nearly the entire water column of diverse oceanic provinces. Historical patterns of abundance are preserved in sediments in the form of their distinctive glycerol dibiphytanyl glycerol tetraether (GDGT) membrane lipids. The correlation between the composition of GDGTs in surface sediment and the overlying annual average sea surface temperature forms the basis for a paleotemperature proxy (TEX...) that is used to reconstruct surface ocean temperature as far back as the Middle Jurassic. However, mounting evidence suggests that factors other than temperature could also play an important role in determining GDGT distributions. We here use a study set of four marine AOA isolates to demonstrate that these closely related strains generate different TEX...-temperature relationships and that oxygen (O...) concentration is at least as important as temperature in controlling TEX... values in culture. All of the four strains characterized showed a unique membrane compositional response to temperature, with TEX...-inferred temperatures varying as much as 12 ...C from the incubation temperatures. In addition, both linear and nonlinear TEX...-temperature relationships were characteristic of individual strains. Increasing relative abundance of GDGT-2 and GDGT-3 with increasing O... limitation, at the expense of GDGT-1, led to significant elevations in TEX...-derived temperature. Although the adaptive significance of GDGT compositional changes in response to both temperature and O... is unclear, this observation necessitates a reassessment of archaeal lipid-based paleotemperature proxies, particularly in records that span low-oxygen events or underlie oxygen minimum zones. (ProQuest: ... denotes formulae/symbols omitted.)
Journal Article
Insight into the symbiotic lifestyle of DPANN archaea revealed by cultivation and genome analyses
Decades of culture-independent analyses have resulted in proposals of many tentative archaeal phyla with no cultivable representative. Members of DPANN (an acronym of the names of the first included phyla Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanohaloarchaeota, and Nanoarchaeota), an archaeal superphylum composed of at least 10 of these tentative phyla, are generally considered obligate symbionts dependent on other microorganisms. While many draft/complete genome sequences of DPANN archaea are available and their biological functions have been considerably predicted, only a few examples of their successful laboratory cultivation have been reported, limiting our knowledge of their symbiotic lifestyles. Here, we investigated physiology, morphology, and host specificity of an archaeon of the phylum “Candidatus Micrarchaeota” (ARM-1) belonging to the DPANN superphylum by cultivation. We constructed a stable coculture system composed of ARM-1 and its original host Metallosphaera sp. AS-7 belonging to the order Sulfolobales. Further host-switching experiments confirmed that ARM-1 grew on five different archaeal species from three genera—Metallosphaera, Acidianus, and Saccharolobus—originating from geologically distinct hot, acidic environments. The results suggested the existence of DPANN archaea that can grow by relying on a range of hosts. Genomic analyses showed inferred metabolic capabilities, common/unique genetic contents of ARM-1 among cultivated micrarchaeal representatives, and the possibility of horizontal gene transfer between ARM-1 and members of the order Sulfolobales. Our report sheds light on the symbiotic lifestyles of DPANN archaea and will contribute to the elucidation of their biological/ecological functions.
Journal Article
Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface
Subsurface microbial life contributes significantly to biogeochemical cycling, yet it remains largely uncharacterized, especially its archaeal members. This 'microbial dark matter' has been explored by recent studies that were, however, mostly based on DNA sequence information only. Here, we use diverse techniques including ultrastuctural analyses to link genomics to biology for the SM1 Euryarchaeon lineage, an uncultivated group of subsurface archaea. Phylogenomic analyses reveal this lineage to belong to a widespread group of archaea that we propose to classify as a new euryarchaeal order (‘
Candidatus
Altiarchaeales’). The representative, double-membraned species ‘
Candidatus
Altiarchaeum hamiconexum’ has an autotrophic metabolism that uses a not-yet-reported Factor
420
-free reductive acetyl-CoA pathway, confirmed by stable carbon isotopic measurements of archaeal lipids. Our results indicate that this lineage has evolved specific metabolic and structural features like nano-grappling hooks empowering this widely distributed archaeon to predominate anaerobic groundwater, where it may represent an important carbon dioxide sink.
Research on microbes that inhabit the Earth's subsurface is mostly based on metagenomic information only. Here, Probst
et al
. combine metagenomics with ultrastructural and functional analyses to study the biology of a group of uncultivated subsurface archaea, the SM1 Euryarchaeon lineage.
Journal Article
Isolation of an archaeon at the prokaryote–eukaryote interface
The origin of eukaryotes remains unclear
1
–
4
. Current data suggest that eukaryotes may have emerged from an archaeal lineage known as ‘Asgard’ archaea
5
,
6
. Despite the eukaryote-like genomic features that are found in these archaea, the evolutionary transition from archaea to eukaryotes remains unclear, owing to the lack of cultured representatives and corresponding physiological insights. Here we report the decade-long isolation of an Asgard archaeon related to Lokiarchaeota from deep marine sediment. The archaeon—‘
Candidatus
Prometheoarchaeum syntrophicum’ strain MK-D1—is an anaerobic, extremely slow-growing, small coccus (around 550 nm in diameter) that degrades amino acids through syntrophy. Although eukaryote-like intracellular complexes have been proposed for Asgard archaea
6
, the isolate has no visible organelle-like structure. Instead,
Ca
. P. syntrophicum is morphologically complex and has unique protrusions that are long and often branching. On the basis of the available data obtained from cultivation and genomics, and reasoned interpretations of the existing literature, we propose a hypothetical model for eukaryogenesis, termed the entangle–engulf–endogenize (also known as E
3
) model.
Isolation and characterization of an archaeon that is most closely related to eukaryotes reveals insights into how eukaryotes may have evolved from prokaryotes.
Journal Article