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

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.

Anaerobic methane oxidation in a coastal oxygen minimum zone: spatial and temporal dynamics

“…In Illumina‐based datasets from 2018 and 2020 containing archaea, we additionally searched for methanogen‐related 16S rRNA gene sequences and detected sequences belonging to the methanogenic Euryarchaeal class ‘ Candidatus Methanofastidiosa’, which based on metagenomic and transcriptomic analyses have been indicated to perform methanogenesis through reduction of methylated compounds (Nobu et al ., 2016; Zhang et al ., 2020; Wang et al ., 2021) (Fig. S3).…”

Editorial: Ecology, Metabolism and Evolution of Archaea-Perspectives From Proceedings of the International Workshop on Geo-Omics of Archaea

“…Two other studies focused on sediment cores collected from the Pearl River Estuary in southeastern China. The first established strong vertical stratification of dissolved organic matter (DOM) consistent with increases in recalcitrant DOM with depth, and corresponding stratification of microbial communities (Wang et al, 2021b). Lignin and carboxyl-rich alicyclic molecules were strongly correlated with Bathyarchaeia in deeper sediments; correspondingly, Bathyarchaeia MAGs were enriched with genes predicted to encode enzymes for the reductive dearomatization and carboxylation of aromatic compounds.…”

“…Eukaryogenesis will continue to be a major research frontier in this area, but other important insights into archaeal evolution await. For example, recent progress on the genomic evolution of diverse archaea in the context of Earth history provide better ties between genome-based evolutionary models and the sedimentary record (e.g., Colman et al, 2018;Wang et al, 2021b;Yang et al, 2021). The fast-increasing volume and diversity of high-quality environmental genomes should lead to fruitful new ground in archaeal evolutionary studies along geological time scales, which has been hampered by the lack of physical fossils of microorganisms.…”

Ancient electrogenic survival metabolism of β -proteobacterial ammonia oxidizers for oxygen deficiency

“…Few modern anaerobic methane-oxidizing clades (ANME) are capable of performing direct electron transfer between species using MHCs (6). The deeply rooted phylogeny of archaeal ANME clades in time (21, 22) suggests MHCs may have a long evolutionary history before the Proterozoic eon.…”