A methylotrophic origin of methanogenesis and early divergence of anaerobic multicarbon alkane metabolism

Yinzhao Wang; Gunter Wegener; Tom A Williams; Ruize Xie; Jialin Hou; Chen Tian; Yu Zhang; Fengping Wang; Xiang Xiao

doi:10.1126/sciadv.abj1453

A methylotrophic origin of methanogenesis and early divergence of anaerobic multicarbon alkane metabolism

Sci Adv. 2021 Jul 2;7(27):eabj1453. doi: 10.1126/sciadv.abj1453. Print 2021 Jul.

Authors

Yinzhao Wang¹, Gunter Wegener^{2

3}, Tom A Williams⁴, Ruize Xie⁵, Jialin Hou⁶, Chen Tian⁵, Yu Zhang⁵, Fengping Wang^{6

5

7}, Xiang Xiao^{1

8}

Affiliations

¹ State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China. wyz@sjtu.edu.cn zjxiao2018@sjtu.edu.cn.
² Max Planck Institute for Marine Microbiology, 28359 Bremen, Germany.
³ MARUM, Center for Marine Environmental Sciences, University of Bremen, 28359 Bremen, Germany.
⁴ School of Biological Sciences, University of Bristol, BS8 1TH Bristol, UK.
⁵ School of Oceanography, Shanghai Jiao Tong University, Shanghai 200240, China.
⁶ State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China.
⁷ Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, Guangdong, China.
⁸ State Key Laboratory of Ocean Engineering, School of Naval Architecture, Ocean and Civil Engineering, Shanghai Jiao Tong University, Shanghai 200240, China.

Abstract

Methanogens are considered as one of the earliest life forms on Earth, and together with anaerobic methane-oxidizing archaea, they have crucial effects on climate stability. However, the origin and evolution of anaerobic alkane metabolism in the domain Archaea remain controversial. Here, we present evidence that methylotrophic methanogenesis was the ancestral form of this metabolism. Carbon dioxide-reducing methanogenesis developed later through the evolution of tetrahydromethanopterin S-methyltransferase, which linked methanogenesis to the Wood-Ljungdahl pathway for energy conservation. Anaerobic multicarbon alkane metabolisms in Archaea also originated early, with genes coding for the activation of short-chain or even long-chain alkanes likely evolving from an ethane-metabolizing ancestor. These genes were likely horizontally transferred to multiple archaeal clades including Candidatus (Ca) Bathyarchaeia, Ca. Lokiarchaeia, Ca. Hadarchaeia, and the methanogenic Ca. Methanoliparia.

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