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 Miranda, Cristina Gonzalez, Lizett Gonzalez, Christian Sam, Christopher Villa, Madeline Zhuo, Nicholas Bodman, Fernando Robles, Eric S. Boyd, Alysia D. Cox, Brian St. Clair, Zheng-Shuang Hua, Wen-Jun Li, Anna-Louise Reysenbach, Matthew B. Stott, Peter K. Weber, Jennifer Pett-Ridge, Anne E. Dekas, Brian P. Hedlund and Jeremy A. Dodsworth ()
Additional contact information
Steffen Buessecker: Stanford University
Marike Palmer: University of Nevada, Las Vegas
Dengxun Lai: University of Nevada, Las Vegas
Joshua Dimapilis: California State University
Xavier Mayali: Lawrence Livermore National Laboratory
Damon Mosier: California State University
Jian-Yu Jiao: Sun Yat-Sen University
Daniel R. Colman: Montana State University
Lisa M. Keller: Montana State University
Emily St. John: Portland State University
Michelle Miranda: California State University
Cristina Gonzalez: California State University
Lizett Gonzalez: California State University
Christian Sam: California State University
Christopher Villa: California State University
Madeline Zhuo: California State University
Nicholas Bodman: California State University
Fernando Robles: California State University
Eric S. Boyd: Montana State University
Alysia D. Cox: Montana Technological University
Brian St. Clair: Montana Technological University
Zheng-Shuang Hua: University of Science and Technology of China
Wen-Jun Li: Sun Yat-Sen University
Anna-Louise Reysenbach: Portland State University
Matthew B. Stott: University of Canterbury
Peter K. Weber: Lawrence Livermore National Laboratory
Jennifer Pett-Ridge: Lawrence Livermore National Laboratory
Anne E. Dekas: Stanford University
Brian P. Hedlund: University of Nevada, Las Vegas
Jeremy A. Dodsworth: California State University

Nature Communications, 2022, vol. 13, issue 1, 1-13

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41467-022-31452-8

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