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A laboratory-scale sulfur autotrophic reactor (SAR) was first constructed for treating tellurite [Te(IV)] wastewater. The SAR had excellent Te(IV) bioreduction efficiency (90-96%) at 5-30 mg/L and conformed to the First-order kinetic model. The Te(IV) bioreduction was elaborated deeply from extracellular polymeric substances (EPS) functions, microbial metabolic activity, key enzyme activity, microbial community succession and quorum sensing. Te(IV) stimulated the increase of redox substances in EPS and the improved cell membrane permeability led to the increase of electron transport system activity. Catalase and reduced nicotinamide adenine dinucleotide (NADH) alleviated the oxidative stress caused by Te(IV) toxicity to maintain metabolic activity. The increase of sulfur dioxygenase activity (SDO) suggested that more ATP produced by sulfur oxidation might provide energy for various physiological activities. Meanwhile, nitrate reductase (NAR), nitrite reductase (NIR) and sulfide: quinone oxidoreductase (SQR) played an active role in sulfur oxidation and Te(IV) bioreduction. Combined with the above results and dynamic succession of three functional microbial communities, a synergistic mechanism was proposed to explain the excellent performance of SAR. This work provided a promising strategy for Te(IV) wastewater treatment process and Te(IV) bioreduction mechanism.