Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis

Sorokin, Dimitry Y.; Makarova, Kira S.; Abbas, Ben; Ferrer, Manuel; Golyshin, Peter N.; Galinski, Erwin A.; Ciordia, Sergio; Mena, Montaña; Merkel, Alexander Y.; Wolf, Yuri I.; Loosdrecht, Mark C.M. van; Koonin, Eugene V.

doi:10.1038/nmicrobiol.2017.81

Cited by 215 publications

(251 citation statements)

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“…9). The existence of a CTD that is catalytically active in vivo adds credence to the bioinformatic and proteomic discovery of isolated pylSc genes in diverse archaeal species 1,27 .…”

Section: Resultsmentioning

confidence: 97%

Crystal structures reveal an elusive functional domain of pyrrolysyl-tRNA synthetase

et al. 2017

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Pyrrolysyl-tRNA synthetase (PylRS) is a major tool in genetic code expansion with non-canonical amino acids, yet understanding of its structure and activity is incomplete. Here we describe the crystal structure of the previously uncharacterized essential N-terminal domain of this unique enzyme in complex with tRNAPyl. This structure explains why PylRS remains orthogonal in a broad range of organisms, from bacteria to humans. The structure also illustrates why tRNAPyl recognition by PylRS is anticodon-independent; the anticodon does not contact the enzyme. Using standard microbiological culture equipment, we then established a new method for laboratory evolution – a non-continuous counterpart of the previously developed phage-assisted continuous evolution. With this method, we evolved novel PylRS variants with enhanced activity and amino acid specificity. We finally employed an evolved PylRS variant to determine its N-terminal domain structure and show how its mutations improve PylRS activity in the genetic encoding of a non-canonical amino acid.

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“…9). The existence of a CTD that is catalytically active in vivo adds credence to the bioinformatic and proteomic discovery of isolated pylSc genes in diverse archaeal species 1,27 .…”

Section: Resultsmentioning

confidence: 97%

Crystal structures reveal an elusive functional domain of pyrrolysyl-tRNA synthetase

et al. 2017

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“…1e, Figs. 20 S1d and S2j-k). The fourth zone comprised the hypersaline (~30%), almost neutral (pH~6.5), Lake Assale (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…To check whether this resulted from excessively low DNA amounts in those samples (although relatively large volumes were filtered), we carried out semi-nested PCR reactions using as templates potential amplicons produced during the first PCR-amplification reaction, including first-PCR negative controls. Almost all samples produced 20 amplicons in semi-nested PCR-reactions, including the first-PCR blanks (Fig. 3a).…”

Section: Resultsmentioning

confidence: 99%

“…The rest of archaea distributed in lineages typically present in hypersaline environments, e.g. the Methanonatronoarchaeia (20,21) or Candidate Divison MSBL1, thought to encompass methanogens (22) and/or sugar-fermentors (23), but also other archaeal groups not specifically associated with salty systems. These included Thermoplasmata and Archaeoglobi within 45 Euryarchaeota, Woesearchaeota and other lineages (Aenigmarchaeota, Altiarchaeales) usually grouped as DPANN (24)(25)(26) and Thaumarchaeota and Crenarchaeota (Sulfolobales) within the TACK/Proteoarchaeota (27) ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Consistent with metabarcoding results, and despite the use of various culture media and growth conditions mimicking local environments (see Supplementary Methods), cultural approaches did not yield enrichments for any of the Dallol dome, Black and Yellow lake samples. We obtained enrichments from the canyon cave (Gt/7Gt) and salt plain (PS/PS3) 20 samples in most culture media (except on benzoate/hexadecane) and tested conditions (except at 70°C in the dark). A single isolate (PS3-A1) was obtained from serial dilutions.…”

Section: Resultsmentioning

confidence: 99%

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Hyperdiverse archaea near life limits at the polyextreme geothermal Dallol area

Belilla

Moreira

Jardillier

et al. 2019

Preprint

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Microbial life has adapted to various individual extreme conditions; yet, organisms simultaneously adapted to low pH, high salt and high temperature are unknown. We combined environmental 16S/18S rRNA-gene metabarcoding, cultural approaches, fluorescence-activated cell sorting, scanning electron microscopy and chemical analyses to study samples along such 25 unique polyextreme gradients in the Dallol-Danakil area (Ethiopia). We identify two physicochemical barriers to life in the presence of surface liquid water defined by high chaotropicity-low water activity in Mg 2+ /Ca 2+ -dominated brines and hyperacidity-salt combinations. When detected, life was dominated by highly diverse ultrasmall archaea widely distributed across phyla with and without previously known hyperhalophilic members. We detect 30 active silica encrustment/fossilization of cells but also abiotic biomorphs of varied chemistry, raising warnings for the interpretation of morphological biosignatures on Earth and beyond. One Sentence Summary:The absence of life from some polyextreme sites in the presence of liquid surface water on Earth 35 helps to circumscribe habitability Belilla et al. 2 Main Text:Microbial life has adapted to so-called extreme values of temperature, pH or salinity, but also to 5 several polyextreme, e.g. hot acidic or salty alkaline, ecosystems (1, 2). However, organisms adapted simultaneously to low pH and high salt, and eventually also high temperature, are not known (1). Are molecular adaptations to those combinations incompatible or (hot) acidic hypersaline environments simply rare and unexplored? The Dallol geothermal dome and its surroundings (Danakil Depression, Afar, Ethiopia) allow to address this question by offering 10 unique polyextreme gradients combining high salt content (20 to >50%; either Mg 2+ /Ca 2+ or Na + (/Fe 2+/3+ )-rich), high temperature (25-110°C) and low pH (≤-1.5 to 6). Dallol is an up-lifted (~40 m) dome structure located in the North of the Danakil depression (~120 m below-sea-level), a 200 km-long basin within the Afar rift, at the triple junction between the Nubian, Somalian and Arabian Plates (3). Lying only 30 km north of the hypersaline, hydrothermally-influenced, Lake 15 Assale (Karum) and the Erta Ale volcanic range, Dallol does not display volcanic outcrops but intense degassing and hydrothermal activity. These activities are observed on the salt dome and the adjacent Black Mountain and Yellow Lake (Gaet'Ale) areas (3, 4) ( Fig. 1a-b). Gas and fluid isotopic measurements indicate that meteoritic waters, notably infiltrating from the high Ethiopian plateau (>2,500 m), interact with an underlying geothermal reservoir (280-370°C) (4, 20 5). Further interaction of those fluids with the km-thick marine evaporites filling the Danakil depression results in unique combinations of polyextreme conditions and salt chemistries (3,4,6, 7), which have led some authors consider Dallol as a Mars analog (8).Here, we use environmental 16S/18S rRNA-gene metabarcoding, cultural approaches, fluorescence-activa...

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Anaerobic Haloalkaliphiles

Sorokin

2017

Encyclopedia of Life Sciences

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Halo‐alkali‐philes is a type of double extremophiles functioning optimally in saline brines of soda lakes. Soda lakes are a specific type of salt lakes with their brines consisting mostly of alkaline sodium carbonates. With rare exceptions, the haloalkaliphiles are prokaryotes, represented by four major metabolic blocks: aerobic and anoxygenic phototrophs as primary producers and aerobic and anaerobic chemotrophs mostly involved in mineral cycling and mineralisation of organic carbon. The fermentative anaerobes in soda lakes mostly include members of Clostridia involved in polymer hydrolysis and further fermentation of the monomers. The halolalkaliphilic denitrifiers are represented mostly by the members of Gammaproteobacteria from the genera Halomonas and Alkalilimnicola/Alkalispirillum group. The sulfidogens is the most active group of secondary anaerobes in soda lakes and include two major groups – sulfate/thiosulfate reducers from the Deltaproteobacteria with a prominent capacity for sulfite and thiosulfate disproportionation and sulfur/polysulfide reducers from the phylum Chrysiogenetes. Furthermore, soda lake natronoarchaea can also participate in polysulfide respiration. Methanogenesis in soda lakes is active with all three classical pathway represented by haloalkaliphilic species, but, similar to salt lakes, it is dominated by methylotrophs. So far, little is known about the specific bioenergetic features of the soda lake anaerobes allowing them to thrive at high pH. One of it, however, seems to be in common – the substantial use of sodium‐pumping, both by primary and secondary cation pumps. Key Concepts Soda lakes is not the only highly alkaline habitat on Earth, but it is the only one where the extremely high pH is stable. Not only the high pH, but also a combination of chemical parameters created by extremely high carbonate alkalinity in brines of the soda lakes makes them a unique habitat dominated by Prokaryotic life. The salinity caused by strongly electrolytic NaCl in pH‐neutral brines differs substantially from the salinity of weakly electrolytic sodium carbonates in its osmotic effect on salt‐tolerant organisms. Extreme salinity and high pH impose extra energy demands on haloalkalphilic microbes, especially anaerobes with low energy‐producing metabolism. Nevertheless, all major functional groups of anaerobic microbes are present in soda lakes. The primary organic matter in soda lakes is mostly produced by protein-rich cyanobacteria. However, the identity of haloalkaliphilic anaerobes degrading proteins in soda lake sediments is still mostly unknown. The denitrifying haloalkaliphilies in soda lakes belong to Gammaproteobacteria but the identity of dissimilatory ammonifyers remains unknown. Many haloalkaliphilic anaerobes isolated from soda lakes are capable of using toxic metal oxyanions as electron acceptors but very few can use Fe(III). The most prominent property of the soda lake sulfidogens is the ability to grow by disproportionation of inorganic sulfur compounds. The methogenesis in soda lakes is dominated by methylotrophic pathways but, in contrast to salt lakes, the other pathways are also active at haloalkaline conditions. Low sulfide toxicity and high CO 2 and H 2 S‐absorbing capacity of the soda brines makes sulfidogenesis and methanogenesis at haloalkaline conditions attractive for application.

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Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis

Cited by 215 publications

References 61 publications

Crystal structures reveal an elusive functional domain of pyrrolysyl-tRNA synthetase

Crystal structures reveal an elusive functional domain of pyrrolysyl-tRNA synthetase

Hyperdiverse archaea near life limits at the polyextreme geothermal Dallol area

Anaerobic Haloalkaliphiles

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