Simulated microgravity confines and fragments the straw-based lignocellulose degrading microbial community

Crewed long-term and long-distance missions are the undoubted trends of human space exploration, which require a bioregenerative life support system (BLSS) and its efficient treatment of the highly lignocellulosic organic solid waste under microgravity. Under normal gravity and simulated microgravity effect (mµ-g) created by clinostats, we used the inoculum from the world's longest BLSS experiment "Lunar Palace 365" to ferment and degrade wheat straw. The straw and its lignocellulose contents' weight losses were significantly slowed down by mµ-g. By high-throughput sequencing and metabolomics on the fermentation material, we found that mµ-g largely shrank and fragmented the microbial community's phylogenetic molecular ecological network (pMEN), and enriched many reported antimicrobial metabolites, especially against fungi, the principal lignocellulose degrader (e.g., cyclohexylamine, an antifungal chemical, increased by 188 times). Inspired by the solid-media visualization experiment of Aspergillus nidulans (a representative fungus) which showed a confined hyphal expansion under mµ-g, we proposed a material-convection-based model: the degradation of complex and recalcitrant macromolecules like lignocellulose is a multistep and highly coordinative task for the microbial community, but the mµ-g physically destroyed the material convection in the fermentation material, which confined the diffusion of microbial cells, their metabolic products/substrates, and extracellular enzymes, thus fragmenting the microbial interactions needed for the degradation; the confined diffusion also caused a local resource shortage for next-step degraders, which resulted in a zonal concentration of microbes and thus intensified conflicts manifested in the release of antimicrobial metabolites, especially against fungi.IMPORTANCEThis convection-based model explains the observed phenomena and suggests proper mass-transfer-promoting methods for more "globalized" microbial interactions in such a community-based, highly coordinative, oligotrophic, mixed-phase (physically), and fungi-dominant application scenario under microgravity. The higher lignocellulose degradation efficiency thus achieved would certainly improve the bioregenerative life support system (BLSS) required for long-term space exploration missions. For non-space-exploration scenarios, this model could also serve as an additional illustration of both the biological and physical principles of such multistep bioprocesses.