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

Buessecker et al. (2022). Nature Communications 13 (1)
Names (16)
Wolframiiraptor gerlachensis Ts Wolframiiraptor Wolframiiraptoraceae Benthortus lauensis Ts Geocrenenecus dongiae Ts Geocrenenecus arthurdayi Geocrenenecus huangii Terraquivivens ruidianensis Terraquivivens tengchongensis Terraquivivens yellowstonensis Benthortus Geocrenenecus Terraquivivens Terraquivivens tikiterensis Ts Wolframiiraptor sinensis Wolframiiraptor allenii
General Biochemistry, Genetics and Molecular Biology General Chemistry General Physics and Astronomy Multidisciplinary
AbstractTrace 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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