Thorarchaeota are a new archaeal phylum within the Asgard superphylum, whose ancestors have been proposed to play possible ecological roles in cellular evolution. However, little is known about the lifestyles of these uncultured archaea. To provide a better resolution of the ecological roles and metabolic capacity of Thorarchaeota, we obtained Thorarchaeota genomes reconstructed from metagenomes of different depth layers in mangrove and mudflat sediments. These genomes from deep anoxic layers suggest the presence of Thorarchaeota with the potential to degrade organic matter, fix inorganic carbon, reduce sulfur/sulfate and produce acetate. In particular, Thorarchaeota may be involved in ethanol production, nitrogen fixation, nitrite reduction, and arsenic detoxification. Interestingly, these Thorarchaeotal genomes are inferred to contain the tetrahydromethanopterin and tetrahydrofolate Wood-Ljungdahl (WL) pathways for CO2 reduction, and the latter WL pathway appears to have originated from bacteria. These archaea are predicted to be able to use various inorganic and organic carbon sources, possessing genes inferred to encode ribulose bisphosphate carboxylase-like proteins (normally without RuBisCO activity) and a near-complete Calvin-Benson-Bassham cycle. The existence of eukaryotic selenocysteine insertion sequences and many genes for proteins previously considered eukaryote-specific in Thorarchaeota genomes provide new insights into their evolutionary roles in the origin of eukaryotic cellular complexity. Resolving the metabolic capacities of these enigmatic archaea and their origins will enhance our understanding of the origins of eukaryotes and their roles in ecosystems.