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An essential role for tungsten in the ecology and evolution of a previously uncultivated lineage of anaerobic, thermophilic Archaea.

Steffen BuesseckerMarike PalmerDengxun LaiJoshua DimapilisXavier MayaliDamon MosierJian-Yu JiaoDaniel R ColmanLisa M KellerEmily St JohnMichelle MirandaCristina GonzalezLizett GonzalezChristian SamChristopher VillaMadeline ZhuoNicholas BodmanFernando RoblesEric S BoydAlysia D CoxBrian St ClairZheng-Shuang HuaWen-Jun LiAnna-Louise ReysenbachMatthew B StottPeter K WeberJennifer Pett-RidgeAnne E DekasBrian P HedlundJeremy A Dodsworth
Published in: Nature communications (2022)
Trace metals have been an important ingredient for life throughout Earth's history. Here, we describe the genome-guided cultivation of a member of the elusive archaeal lineage Caldarchaeales (syn. Aigarchaeota), Wolframiiraptor gerlachensis, and its growth dependence on tungsten. A metagenome-assembled genome (MAG) of W. gerlachensis encodes putative tungsten membrane transport systems, as well as pathways for anaerobic oxidation of sugars probably mediated by tungsten-dependent ferredoxin oxidoreductases that are expressed during growth. Catalyzed reporter deposition-fluorescence in-situ hybridization (CARD-FISH) and nanoscale secondary ion mass spectrometry (nanoSIMS) show that W. gerlachensis preferentially assimilates xylose. Phylogenetic analyses of 78 high-quality Wolframiiraptoraceae MAGs from terrestrial and marine hydrothermal systems suggest that tungsten-associated enzymes were present in the last common ancestor of extant Wolframiiraptoraceae. Our observations imply a crucial role for tungsten-dependent metabolism in the origin and evolution of this lineage, and hint at a relic metabolic dependence on this trace metal in early anaerobic thermophiles.
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