An essential role for tungsten in the ecology and evolution of a previously uncultivated lineage of anaerobic, thermophilic Archaea
Steffen Buessecker, Marike Palmer, Dengxun Lai, Joshua Dimapilis, Xavier Mayali, Damon Mosier, Jian‐Yu Jiao, Daniel R. Colman, Lisa M. Keller, Emily St. John, Michelle D. Miranda, Cristina González, Lizett Gonzalez, Christian Sam, Christopher Villa, Madeline Zhuo, Nicholas Bodman, Fernando Robles, Eric S. Boyd, Alysia Cox, Brian St. Clair, Zheng‐Shuang Hua, Wen‐Jun Li, Anna‐Louise Reysenbach, Matthew B. Stott, Peter Weber, Jennifer Pett‐Ridge, Anne Dekas, Brian P. Hedlund, Jeremy A. Dodsworth
Abstract
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.