Cloacimonadota metabolisms include adaptations for engineered environments that are reflected in the evolutionary history of the phylum

Phylum Cloacimonadota (previously Cloacimonetes, WWE1) is an understudied bacterial lineage frequently associated with engineered and wastewater systems. Cloacimonadota members were abundant and diverse in metagenomic datasets from a municipal landfill, prompting an examination of phylogenetic relationships, metabolic diversity, and pangenomic dynamics across the phylum, based on 22 publicly available genomes and 24 from landfill samples. Cloacimonadota formed two discrete clades, with one clade's genomes principally deriving from engineered systems. A few more-divergent genomes were placed basal in the tree, and not associated with either clade. Metabolic reconstructions for metagenome-assembled genomes predict an anaerobic, acetogenic, and fermentative lifestyle for the majority of Cloacimonadota surveyed. Genomes from engineered ecosystems (first clade) encode a unique suite of genes not typically found in genomes from natural environments (second clade). These encoded functions include acetate kinase, the enzyme responsible for the formation of acetate from acetyl phosphate, and carbon utilization enzymes, suggesting different substrate degradation and energy generation strategies in these ecologically and phylogenetically distinct lineages.