Genomic Insights Into the Archaea Inhabiting an Australian Radioactive Legacy Site

During the 1960s, small quantities of radioactive materials were co-disposed with chemical waste at the Little Forest Legacy Site (LFLS, Sydney, Australia). The microbial function and population dynamics in a waste trench during a rainfall event have been previously investigated revealing a broad abundance of candidate and potentially undescribed taxa in this iron-rich, radionuclide-contaminated environment. Applying genome-based metagenomic methods, we recovered 37 refined archaeal MAGs, mainly from undescribed DPANN Archaea lineages without standing in nomenclature and ‘ Candidatus Methanoperedenaceae’ (ANME-2D). Within the undescribed DPANN, the newly proposed orders ‘ Ca. Gugararchaeales’, ‘ Ca. Burarchaeales’ and ‘ Ca. Anstonellales’, constitute distinct lineages with a more comprehensive central metabolism and anabolic capabilities within the ‘ Ca. Micrarchaeota’ phylum compared to most other DPANN. The analysis of new and extant ‘ Ca. Methanoperedens spp.’ MAGs suggests metal ions as the ancestral electron acceptors during the anaerobic oxidation of methane while the respiration of nitrate/nitrite via molybdopterin oxidoreductases would have been a secondary acquisition. The presence of genes for the biosynthesis of polyhydroxyalkanoates in most ‘ Ca. Methanoperedens’ also appears to be a widespread characteristic of the genus for carbon accumulation. This work expands our knowledge about the roles of the Archaea at the LFLS, especially, DPANN Archaea and ‘ Ca. Methanoperedens’, while exploring their diversity, uniqueness, potential role in elemental cycling, and evolutionary history.