Coupling municipal anaerobic digestate (MAD) treatments with microalgal cultivation can concomitantly achieve nutrient removal and microalgal bioenergy production. However, the high cost caused by dilution water and microalgal harvesting is a great challenge. In this study, Scenedesmus quadricauda was screened as the most appropriate algae strain due to its potential for growth and auto-flocculation, and the MAD diluted 5-fold with WWTP effluent was demonstrated as an ideal medium for S. quadricauda growth. Moreover, inspired by naturally generated silica shells of diatoms, a low-cost and biomimetic auto-flocculation strategy that combined high light intensity induction and microalgal silicification was proposed to accelerate the auto-flocculation process. Compared with low light intensity groups, this strategy imparted diatom-like features to S. quadricauda cells, and contributed to 3.07-fold higher auto-flocculation efficiency within 30 min. It was attributed to the fact that the high light intensity of 150 μmol·m ^− 2·s ^− 1 stimulated the extracellular polymeric substances (EPS) secretion and induced the variation in property and composition of EPS, especially the protein secondary structures, which allowed silica nanoparticles to spontaneously attach onto S. quadricauda cells in the presence of viscous EPS. Furthermore, this strategy significantly increased microalgal biomass yield to a dry weight of 1.37 g·L ^− 1, accompanied by 93.78%, 96.39% and 91.36% removals of NH₄⁺-N, TP, and COD, respectively. The productivity of valuable by-products, including lipid, carbohydrate, protein, and pigment, reached 56.30, 101.35, 30.39 and 11.28 mg·L ^− 1·d ^− 1, respectively. Overall, this study supplies a novel approach for low-cost microalgal bioenergy production from MAD and energy-efficient microalgae harvest by auto-flocculation.