A decrease in pH can affect the biochemical properties of a sulfate reduction system, but the stress responses to such pH fluctuations and acid-adaptive mechanisms of the microorganisms remain incompletely understood. Here, we compared the sulfate (SO₄²⁻) reduction performance of a sulfate-reducing consortium (SRB system) and a pure Desulfovibrio sp. system (Des. system, control) under pH 7.0, 5.5, and 5.0 via batch experiments. A key novelty is the integration of microbial physiology and metagenomics to reveal adaptive mechanisms: the Des. system showed significant inhibition of growth and sulfate reduction with decreasing pH, while the SRB system maintained superior SO₄²⁻ removal efficiency through three synergistic adjustments: (1) physiological regulation (enhanced H⁺-ATPase activity, stress protein production, and cell membrane cyclopropane fatty acid content); (2) microbial community restructuring (enrichment of acid-resistant Bacillus and Clostridium); and (3) functional gene upregulation (sulfate import, dissimilar sulfate reduction, sulfide oxidation, and SO_x system-related genes, p < 0.05). This study links physiological responses to metagenomic functional shifts under acid stress, providing critical theoretical support for applying sulfate-reducing consortia in acidic sulfate-containing wastewater remediation.