A hybrid photocatalytic system enables direct glucose utilization for methanogenesis

Proc Natl Acad Sci U S A. 2024 Jan 23;121(4):e2317058121. doi: 10.1073/pnas.2317058121. Epub 2024 Jan 17.

Abstract

Integration of methanogenic archaea with photocatalysts presents a sustainable solution for solar-driven methanogenesis. However, maximizing CH4 conversion efficiency remains challenging due to the intrinsic energy conservation and strictly restricted substrates of methanogenic archaea. Here, we report a solar-driven biotic-abiotic hybrid (biohybrid) system by incorporating cadmium sulfide (CdS) nanoparticles with a rationally designed methanogenic archaeon Methanosarcina acetivorans C2A, in which the glucose synergist protein and glucose kinase, an energy-efficient route for glucose transport and phosphorylation from Zymomonas mobilis, were implemented to facilitate nonnative substrate glucose for methanogenesis. We demonstrate that the photo-excited electrons facilitate membrane-bound electron transport chain, thereby augmenting the Na+ and H+ ion gradients across membrane to enhance adenosine triphosphate (ATP) synthesis. Additionally, this biohybrid system promotes the metabolism of pyruvate to acetyl coenzyme A (AcCoA) and inhibits the flow of AcCoA to the tricarboxylic acid (TCA) cycle, resulting in a 1.26-fold augmentation in CH4 production from glucose-derived carbon. Our results provide a unique strategy for enhancing methanogenesis through rational biohybrid design and reprogramming, which gives a promising avenue for sustainably manufacturing value-added chemicals.

Keywords: biotic–abiotic hybrid; glucose-to-methane conversion; photocatalysis; reasoned reconstruction; solar-driven methanogenesis.

MeSH terms

  • Adenosine Triphosphate* / metabolism
  • Biological Transport
  • Electron Transport
  • Energy Metabolism
  • Methane* / metabolism
  • Methanosarcina / metabolism

Substances

  • Methane
  • Adenosine Triphosphate