Casting Light on the Adaptation Mechanisms and Evolutionary History of the Widespread Sumerlaeota

Sumerlaeota is a mysterious, putative phylum-level lineage distributed globally but rarely reported. As such, their physiology, ecology, and evolutionary history remain unknown. The 16S rRNA gene survey reveals that Sumerlaeota is frequently detected in diverse environments globally, especially cold arid desert soils and deep-sea basin surface sediments, where it is one dominant microbial group. Here, we retrieved four Sumerlaeota metagenome-assembled genomes (MAGs) from two hot springs and one saline lake. Including another 12 publicly available MAGs, they represent six of the nine putative Sumerlaeota subgroups/orders, as indicated by 16S rRNA gene-based phylogeny. These elusive organisms likely obtain carbon mainly through utilization of refractory organics (e.g., chitin and cellulose) and proteinaceous compounds, suggesting that Sumerlaeota act as scavengers in nature. The presence of key bidirectional enzymes involved in acetate and hydrogen metabolisms in these MAGs suggests that they are acetogenic bacteria capable of both the production and consumption of hydrogen. The capabilities of dissimilatory nitrate and sulfate reduction, nitrogen fixation, phosphate solubilization, and organic phosphorus mineralization may confer these heterotrophs great advantages to thrive under diverse harsh conditions. Ancestral state reconstruction indicated that Sumerlaeota originated from chemotrophic and facultatively anaerobic ancestors, and their smaller and variably sized genomes evolved along dynamic pathways from a sizeable common ancestor (2,342 genes), leading to their physiological divergence. Notably, large gene gain and larger loss events occurred at the branch to the last common ancestor of the order subgroup 1, likely due to niche expansion and population size effects.IMPORTANCE In recent years, the tree of life has expanded substantially. Despite this, many abundant yet uncultivated microbial groups remain to be explored. The candidate phylum Sumerlaeota is widely distributed in various harsh environments. However, their physiology, adaptation mechanisms, and evolution remain elusive due to a lack of pure cultures and limited available genomes. Here, we used genomes from uncultivated members of Sumerlaeota to disclose why these taxa can thrive under diverse harsh conditions and how they evolved from a chemotrophic and facultatively anaerobic common ancestor. This study deeply explored the biology of Sumerlaeota and provided novel insights into their possible roles in global biogeochemical cycles, adaptation mechanisms, ecological significance, and evolutionary history.