Acidic, metal-contaminated environments harbour specialized microbial consortia adapted to extreme stress. We examined an environmental Euglena mutabilis culture naturally associated with Talaromyces and Acidiphilium acidophilum and exposed it to cadmium (Cd). Integrated transcriptomic, hormonal, structural and taxonomic analyses revealed a coordinated Cd-tolerance strategy. RNA sequencing showed differential regulation of metal transporters consistent with a shift from Cd uptake to intracellular sequestration. Transmission electron microscopy confirmed Cd compartmentalization within chloroplasts and increased paramylon granules. Cd exposure suppressed light-harvesting complex genes and formate/nitrite transporters while maintaining core photosynthetic function. Hormone profiling indicated strong repression of bioactive auxin and cytokinin (CK) free bases, alongside accumulation of CK nucleotides and downregulation of CK biosynthetic and activation genes. Metagenomics revealed Cd-driven enrichment of Talaromyces and Acidiphilium, implicating them in detoxification and stress support. Together, these responses highlight early Cd uptake followed by chloroplast-based detoxification, metabolic buffering via paramylon, hormonal downregulation of growth and community-mediated resilience.