A moderately thermophilic origin of a novel family of marine group II euryarchaeota from deep ocean

Haodong Liu; Wei-Wei Liu; Jose M Haro-Moreno; Bu Xu; Yanfen Zheng; Jiwen Liu; Jiwei Tian; Xiao-Hua Zhang; Ning-Yi Zhou; Liping Qin; Yuanqing Zhu; Francisco Rodriguez-Valera; Chuanlun Zhang

doi:10.1016/j.isci.2023.107664

A moderately thermophilic origin of a novel family of marine group II euryarchaeota from deep ocean

iScience. 2023 Aug 17;26(9):107664. doi: 10.1016/j.isci.2023.107664. eCollection 2023 Sep 15.

Authors

Haodong Liu^{1

2

3

4}, Wei-Wei Liu⁵, Jose M Haro-Moreno⁶, Bu Xu^{1

2}, Yanfen Zheng^{7

8}, Jiwen Liu⁷, Jiwei Tian⁹, Xiao-Hua Zhang⁷, Ning-Yi Zhou⁵, Liping Qin³, Yuanqing Zhu^{1

10}, Francisco Rodriguez-Valera^{6

11}, Chuanlun Zhang^{1

2

10}

Affiliations

¹ Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science & Engineering, Southern University of Science and Technology, Shenzhen 518055, China.
² Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 510000, China.
³ CAS Key Laboratory of Crust-Mantle Materials and Environments, University of Science and Technology of China, Hefei 230026, China.
⁴ School of Global Health, Chinese Centre for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China.
⁵ State Key Laboratory of Microbial Metabolism & School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China.
⁶ Evolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel Hernández, 03550 Alicante, Spain.
⁷ College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China.
⁸ Marine Agriculture Research Center, Tobacco Research Institute of Chinese Academy of Agricultural Sciences, Qingdao 266101, China.
⁹ Key Laboratory of Physical Oceanography, Ocean University of China, Qingdao 266100, China.
¹⁰ Shanghai Sheshan National Geophysical Observatory, Shanghai Earthquake Agency, Shanghai 200062, China.
¹¹ Laboratory for Theoretical and Computer Studies of Biological Macromolecules and Genomes, Moscow Institute of Physics and Technology, Dolgoprudny, Russia.

Abstract

Marine group II (MGII) is the most abundant planktonic heterotrophic archaea in the ocean. The evolutionary history of MGII archaea is elusive. In this study, 13 new MGII metagenome-assembled genomes were recovered from surface to the hadal zone in Challenger Deep of the Mariana Trench; four of them from the deep ocean represent a novel group. The optimal growth temperature (OGT) of the common ancestor of MGII has been estimated to be at about 60°C and OGTs of MGIIc, MGIIb, and MGIIa at 47°C-50ºC, 37°C-44ºC, and 30°C-37ºC, respectively, suggesting the adaptation of these species to different temperatures during evolution. The estimated OGT range of MGIIc was supported by experimental measurements of cloned β-galactosidase that showed optimal enzyme activity around 50°C. These results indicate that MGIIc may have originated from a common ancestor that lived in warm or even hot marine environment, such as hydrothermal vents.

Keywords: Aquatic biology; Geomicrobiology; Microbiology.