Analysis of nearly 3000 archaeal genomes from terrestrial geothermal springs sheds light on interconnected biogeochemical processes

Yan-Ling Qi, Ya-Ting Chen, Yuan-Guo Xie, Yu-Xian Li, Yang-Zhi Rao, Meng-Meng Li, Qi-Jun Xie, Xing-Ru Cao, Lei Chen, Yan-Ni Qu, Zhen-Xuan Yuan, Zhi-Chao Xiao, Lu Lu, Jian-Yu Jiao, Wen-Sheng Shu, Wen-Jun Li (), Brian P. Hedlund () and Zheng-Shuang Hua ()
Additional contact information
Yan-Ling Qi: University of Science and Technology of China
Ya-Ting Chen: Sichuan University–Hong Kong Polytechnic University
Yuan-Guo Xie: University of Science and Technology of China
Yu-Xian Li: University of Science and Technology of China
Yang-Zhi Rao: University of Science and Technology of China
Meng-Meng Li: Sun Yat-Sen University
Qi-Jun Xie: University of Science and Technology of China
Xing-Ru Cao: University of Science and Technology of China
Lei Chen: University of Science and Technology of China
Yan-Ni Qu: University of Science and Technology of China
Zhen-Xuan Yuan: University of Science and Technology of China
Zhi-Chao Xiao: University of Science and Technology of China
Lu Lu: China West Normal University
Jian-Yu Jiao: Sun Yat-Sen University
Wen-Sheng Shu: South China Normal University
Wen-Jun Li: Sun Yat-Sen University
Brian P. Hedlund: University of Nevada Las Vegas
Zheng-Shuang Hua: University of Science and Technology of China

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Terrestrial geothermal springs are physicochemically diverse and host abundant populations of Archaea. However, the diversity, functionality, and geological influences of these Archaea are not well understood. Here we explore the genomic diversity of Archaea in 152 metagenomes from 48 geothermal springs in Tengchong, China, collected from 2016 to 2021. Our dataset is comprised of 2949 archaeal metagenome-assembled genomes spanning 12 phyla and 392 newly identified species, which increases the known species diversity of Archaea by ~48.6%. The structures and potential functions of the archaeal communities are strongly influenced by temperature and pH, with high-temperature acidic and alkaline springs favoring archaeal abundance over Bacteria. Genome-resolved metagenomics and metatranscriptomics provide insights into the potential ecological niches of these Archaea and their potential roles in carbon, sulfur, nitrogen, and hydrogen metabolism. Furthermore, our findings illustrate the interplay of competition and cooperation among Archaea in biogeochemical cycles, possibly arising from overlapping functional niches and metabolic handoffs. Taken together, our study expands the genomic diversity of Archaea inhabiting geothermal springs and provides a foundation for more incisive study of biogeochemical processes mediated by Archaea in geothermal ecosystems.

Date: 2024
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DOI: 10.1038/s41467-024-48498-5

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