Abstract Background DPANN archaea, including Woesearchaeota, encompass a large fraction of the archaeal diversity, yet their genomic diversity, lifestyle, and role in natural microbiomes remain elusive. With an archaeal assemblage naturally enriched in Woesearchaeota and steep vertical geochemical gradients, Lake Dziani Dzaha (Mayotte) provides an ideal model to decipher their in-situ activity and ecology. Results Using genome-resolved metagenomics and phylogenomics, we identified highly diversified Woesearchaeota populations and defined novel halophilic clades. Depth distribution of these populations in the water column showed an unusual double peak of abundance, located at two distinct chemoclines that are hotspots of microbial diversity in the water column. Genome-centric metatranscriptomics confirmed this vertical distribution and revealed a fermentative activity, with acetate and lactate as end products, and active cell-to-cell processes, supporting strong interactions with other community members at chemoclines. Our results also revealed distinct Woesearchaeota ecotypes, with different transcriptional patterns, contrasted lifestyles, and ecological strategies, depending on environmental/host conditions. Conclusions This work provides novel insights into Woesearchaeota in situ activity and metabolism, revealing invariant, bimodal, and adaptative lifestyles among halophilic Woesearchaeota. This challenges our precepts of an invariable host-dependent metabolism for all the members of this taxa and revises our understanding of their contributions to ecosystem functioning and microbiome assemblage. Video Abstract
