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Background   Akkermansia muciniphila  is a human gut microbe with a key role in the physiology of the intestinal mucus layer and reported associations with decreased body mass and increased gut barrier function and health. Despite its biomedical relevance, the genomic diversity of  A. muciniphila  remains understudied and that of closely related species, except for  A. glycaniphila , unexplored.    Results  We present a large-scale population genomics analysis of the  Akkermansia  genus using 188 isolate genomes and 2226 genomes assembled from 18,600 metagenomes from humans and other animals. While we do not detect  A. glycaniphila , the  Akkermansia  strains in the human gut can be grouped into five distinct candidate species, including  A. muciniphila , that show remarkable whole-genome divergence despite surprisingly similar 16S rRNA gene sequences. These candidate species are likely human-specific, as they are detected in mice and non-human primates almost exclusively when kept in captivity. In humans,  Akkermansia  candidate species display ecological co-exclusion, diversified functional capabilities, and distinct patterns of associations with host body mass. Analysis of CRISPR-Cas loci reveals new variants and spacers targeting newly discovered putative bacteriophages. Remarkably, we observe an increased relative abundance of  Akkermansia  when cognate predicted bacteriophages are present, suggesting ecological interactions.  A. muciniphila  further exhibits subspecies-level genetic stratification with associated functional differences such as a putative exo/lipopolysaccharide operon.    Conclusions  We uncover a large phylogenetic and functional diversity of the  Akkermansia  genus in humans. This variability should be considered in the ongoing experimental and metagenomic efforts to characterize the health-associated properties of  A. muciniphila  and related bacteria.    Supplementary Information  The online version contains supplementary material available at 10.1186/s13059-021-02427-7.

Genomic diversity and ecology of human-associated Akkermansia species in the gut microbiome revealed by extensive metagenomic assembly