The candidate phyla radiation is a large monophyletic lineage comprising unculturable bacterial taxa with small cell and genome sizes, mostly known from genomes obtained from environmental sources without cultivation. Here, we present the closed complete genome of a member of the superphylum Microgenomates obtained from the metagenome of a deep subsurface thermal aquifer. Phylogenetic analysis indicates that the new bacterium, designated Ch65, represents a novel phylum-level lineage within the Microgenomates group, sibling to the candidate phylum Collierbacteria. The Ch65 genome has a highly unusual nucleotide composition with one strand of highly enriched in cytosine versus guanine throughout the whole length. Such nucleotide composition asymmetry, also detected in the members of Ca. Collierbacteria and Ca. Beckwithbacteria, suggests that most of the Ch65 chromosome is replicated in one direction. A genome analysis predicted that the Ch65 bacterium has fermentative metabolism and could produce acetate and lactate. It lacks respiratory capacity, as well as complete pathways for the biosynthesis of lipids, amino acids, and nucleotides. The Embden–Meyerhof glycolytic pathway and nonoxidative pentose phosphate pathway are mostly complete, although glucokinase, 6-phosphofructokinase, and transaldolase were not found. The Ch65 bacterium lacks secreted glycoside hydrolases and conventional transporters for importing sugars and amino acids. Overall, the metabolic predictions imply that Ch65 adopts the lifestyle of a symbiont/parasite, or a scavenger, obtaining resources from the lysed microbial biomass. We propose the provisional taxonomic assignment ‘Candidatus Chazhemtobacterium aquaticus’, genus ‘Chazhemtobacterium‘, family ‘Chazhemtobacteraceae‘ in the Microgenomates group.