Lokiarchaeon exhibits homoacetogenesis

Abstract The proposed Asgard superphylum of Archaea comprises the closest archaeal relatives of eukaryotes, whose genomes hold clues pertaining to the nature host cell that acquired the mitochondrion at the origin of eukaryotes1-4. Genomes of the Asgard candidate Phylum ‘Candidatus Lokiarchaeota’ [Lokiarchaeon] suggest an acetogenic H2 –dependent lifestyle5 and mixotrophic capabilities6. However, data on the activity of Lokiarchaeon are currently lacking, and the ecology of the host cell that acquired the mitochondrion is debated4,7. Here, we show that in anoxic marine sediments underlying highly productive waters on the Namibian continental shelf Lokiarchaeon gene expression increases with depth below the seafloor, and was significantly different across a redox gradient spanning hypoxic to sulfidic conditions. Notably, Lokiarchaeon increased expression of genes involved in growth, carbohydrate metabolism, and the H2-dependent Wood-Ljungdahl (WLP) carbon fixation pathway under the most reducing (sulfidic) conditions. Quantitative stable isotope probing experiments revealed multiple populations of Lokiarchaeota utilizing both CO2 and diatomaceous extracellular polymeric substances (dEPS) as carbon sources over a 10-day incubation under anoxic conditions. This apparent anaerobic mixotrophic metabolism was consistent with the expression of Lokiarchaeon genes involved in transport and fermentation of sugars and amino acids. Remarkably, several Asgard populations were more enriched with 13C-dEPS compared to the community average, indicating a preference for dEPS as a growth substrate. The qSIP and gene expression data indicate a metabolism of “Candidatus Lokiarchaeota” similar to that of sugar fermenting homoacetogenic bacteria8, namely that Lokiarchaeon can couple fermentative H2 production from organic substrates with electron bifurcation and the autotrophic and H2-dependent WLP. Homoacetogenesis allows to access a wide range of substrates and relatively high ATP gain during acetogenic sugar fermentation8 thereby providing an ecological advantage for Lokiarchaeon in anoxic, energy limited settings.