Redox distribution of Asgard archaea and co-occurring taxa in microbial mats from an early Proterozoic ecosystem analog

Eukaryotes originated from the symbiosis of an Asgard archaeon, the alphaproteobacterial ancestor of mitochondria, and possibly additional bacterial contributions. This transition occurred in redox-transition environments such as microbial mats or shallow sediments ~2 billion years ago, when atmospheric oxygen was far lower than today. We investigated Asgard-enriched microbial mats from the low-oxygen, sulfidic Catherine volcano lake (Afar region, Ethiopia), mimicking early Proterozoic conditions. 16S rRNA gene metabarcoding, metagenomics, and metagenome-assembled genome analyses across redox-stratified layers of in situ and mesocosm-maintained mats revealed that Asgardarchaeota thrived in the sulfate-reduction zone, mainly co-occurring with Desulfurobacterota-Myxococcota, among others. Lokiarchaeia and Thorarchaeia preferred anoxic layers. Within Heimdallarchaeia, Heimdallarchaeales were enriched in upper layers, correlating with oxygen-tolerant hydrogenase and sulfate-reduction genes, and Hodarchaeales, in anoxic layers, correlating with methanogenesis. Although reactive-oxygen-species defense mechanisms were widespread, Asgardarchaeota lacked aerobic respiration. These results support the idea that Asgard archaea engaged primarily in syntrophic interactions with sulfate-reducers under early-Earth-like conditions.