Commensal protists and gut bacterial communities exhibit complex relationships, mediated at least in part through host immunity. To improve our understanding of this tripartite interplay, we investigated community and functional dynamics between the murine protist Tritrichomonas musculus (T. mu) and intestinal bacteria in healthy and B cell-deficient mice. We identified dramatic, T. mu-dependent remodeling of resident bacterial composition and metabolism in parallel to increases in T. mu metabolism and the expression of putative virulence factors, responses accelerated in the absence of B cells. Upregulation of iron acquisition and tryptophan consumption revealed competition between bacteria and the protist. Single cell transcriptomics identified distinct T. mu life stages, providing evidence for active growth, sexual replication and the formation of pseudocysts. Unique cell states were validated in situ, and appeared modulated by constituent bacteria, suggesting their role in protist development. Our results reveal complex microbial dynamics during the establishment of a commensal protist.