Deciphering the function of Fe3O4 in alleviating propionate inhibition during high-solids anaerobic digestion: Insights of physiological response and energy conservation

Fe3O4 is a recognized addictive to enhance low solid anaerobic digestion (AD), while for high solid AD challenged by acidity inhibition, its feasibility and mechanism remain unclear. In this study, the positive effect of Fe3O4 on high-solids AD of food waste by regulating microbial physiology and energy conservation to enhance mutualistic propionate methanation was documented. The methane yield was increased by 36.7 % with Fe3O4, which because Fe3O4 alleviated propionate stress on methane generation, along with improved propionate degradation and methanogenic metabolism. Fe3O4 facilitated the production of extracellular polymeric substances and the formation of tightly bio-aggregates, fostering an enriched microbial population (e.g., Smithella and Methanosaeta) to resist propionate stress. Also, Fe3O4 up-regulated the genes in stress defense system, cytomembrane biosynthesis/function, metal irons transporter, cell division and enzyme synthesis, verifying its superiority on cellular physiology. In addition, energy-conservation strategies related to intracellular and extracellular electron transfer were enhanced by Fe3O4. Specifically, the enzyme expressions involved in reversed electron transfer and electron bifurcation coupled with direct interspecies electron transfer (DIET) were upregulated by at least 2.2 times with Fe3O4, providing sufficient energy to drive thermodynamic adverse methanogenesis from propionate-stressed condition. Consequently, the reinforced enzyme expression in the dismutation and DIET pathway make it to be the predominant drivers for enhanced methanogenic propionate metabolism. This study fills the knowledge gaps of Fe3O4-induced microbial physiological and energetic strategies to resist environmental stress, and has remarkable practical implicated for restoring inhibited bioactivities.