Insight into the function and evolution of the Wood–Ljungdahl pathway in Actinobacteria

Jian Yu Jiao, Li Fu, Zheng Shuang Hua, Lan Liu, Nimaichand Salam, Peng Fei Liu, Ai Ping Lv, Geng Wu, Wen Dong Xian, Qiyun Zhu, En Min Zhou, Bao Zhu Fang, Aharon Oren, Brian P. Hedlund, Hong Chen Jiang, Rob Knight, Lei Cheng, Wen Jun Li

Research output: Contribution to journalArticlepeer-review

Abstract

Carbon fixation by chemoautotrophic microbes such as homoacetogens had a major impact on the transition from the inorganic to the organic world. Recent reports have shown the presence of genes for key enzymes associated with the Wood–Ljungdahl pathway (WLP) in the phylum Actinobacteria, which adds to the diversity of potential autotrophs. Here, we compiled 42 actinobacterial metagenome-assembled genomes (MAGs) from new and existing metagenomic datasets and propose three novel classes, Ca. Aquicultoria, Ca. Geothermincolia and Ca. Humimicrobiia. Most members of these classes contain genes coding for acetogenesis through the WLP, as well as a variety of hydrogenases (NiFe groups 1a and 3b–3d; FeFe group C; NiFe group 4-related hydrogenases). We show that the three classes acquired the hydrogenases independently, yet the carbon monoxide dehydrogenase/acetyl-CoA synthase complex (CODH/ACS) was apparently present in their last common ancestor and was inherited vertically. Furthermore, the Actinobacteria likely donated genes for CODH/ACS to multiple lineages within Nitrospirae, Deltaproteobacteria (Desulfobacterota), and Thermodesulfobacteria through multiple horizontal gene transfer events. Finally, we show the apparent growth of Ca. Geothermincolia and H2-dependent acetate production in hot spring enrichment cultures with or without the methanogenesis inhibitor 2-bromoethanesulfonate, which is consistent with the proposed homoacetogenic metabolism.

Original languageEnglish (US)
JournalISME Journal
DOIs
StateAccepted/In press - 2021
Externally publishedYes

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

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