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

Abstract

Increasing evidence supports that eukaryotes originated from the symbiosis of an Asgard archaeon, the alphaproteobacterial ancestor of mitochondria, and possibly additional bacterial contributions. Eukaryogenesis likely occurred in redox-transition environments such as microbial mats or shallow sediments [~]2 billion years ago, when atmospheric oxygen was far lower than today, and oceans were euxinic. We investigated Asgardarchaeota-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 (MAG) 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 and Myxococcota, among others. Lokiarchaeia and Thorarchaeia were more abundant in deeper, anoxic layers. Within Heimdallarchaeia, Heimdallarchaeales were enriched in upper layers, correlating with oxygen-tolerant hydrogenase and sulfate-reduction genes, whereas Hodarchaeales were more relatively abundant in anoxic layers, correlating with methanogenesis. Although reactive-oxygen-species defense mechanisms were widespread in Asgardarchaeota MAGs, they lacked genes for aerobic respiration. These results support the hypothesis that Asgard archaea engaged primarily in syntrophic interactions with sulfate-reducers under conditions prevailing on the early Earth at the onset of eukaryogenesis.