An Essential Role for Tungsten in the Ecology and Evolution of a Previously Uncultivated Lineage of Anaerobic, Thermophilic Archaea

Authors

Steffen Buessecker, Stanford University
Marike Palmer, University of Nevada, Las Vegas
Dengxun Lai, University of Nevada, Las Vegas
Joshua Dimapilis, California State University, San Bernardino
Xavier Mayali, Lawrence Livermore National Laboratory, Livermore
Damon Mosier, California State University, San Bernardino
Jian-Yu Jiao, Sun Yat-Sen University, Guangzhou
Daniel R. Colman, Montana State University-Bozeman
Anna-Louise Reysenbach, Portland State UniversityFollow
multiple additional authors

Sponsor

Funding was provided by the U.S. National Science Foundation (DEB 1557042 and EAR-1820658), NASA (80NNSC17KO548 and 80NSSC19M0150), and the National Natural Science Foundation of China (No. 91951205).

Published In

Nature Communications

Document Type

Article

Publication Date

6-30-2022

Subjects

Genes -- Research, Microorganisms -- Genetic aspects

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.

Rights

Copyright (c) 2022 The Authors

This work is licensed under a Creative Commons Attribution 4.0 International License.

Locate the Document

https://doi.org/10.1038/s41467-022-31452-8

DOI

10.1038/s41467-022-31452-8

Persistent Identifier

https://archives.pdx.edu/ds/psu/38063

Citation Details

Buessecker, S., Palmer, M., Lai, D., Dimapilis, J., Mayali, X., Mosier, D., ... & Dodsworth, J. A. (2022). An essential role for tungsten in the ecology and evolution of a previously uncultivated lineage of anaerobic, thermophilic Archaea. Nature Communications, 13(1), 1-13.