Metabolic framework of spontaneous and synthetic sourdough metacommunities to unravel microbial players implying resilience and performance

Background: In nature, microbial communities undergo changes in composition threatening their resilient behaviour. Here, we interrogated sourdough, a natural cereal-fermenting metacommunity, as challenging ecosystem, where players undergo continuous environmental and spatiotemporal stimuli. Results: Inspecting meta-genomes and -transcriptomes, spontaneous sourdoughs harboured dominant, sub-dominant and satellite players differently engaged in functional pathways. The highest microbial richness bared the highest number of gene copies per pathway. Merging meta-24 omics data or using the same microbiota of a spontaneous sourdough, we de novo reconstructed two synthetic microbial communities, respectively, SDG and SMC-SD43. In vitro, the KEGG number of dominant players in SDG was not affected by single player depletion; that of sub-dominants and satellites fluctuated but showed unique contributions. Compared to SMC-SD43, SDG ensured broader transcriptome redundancy. After in situ long-time back slopping, SDG kept stable, with constant volatilome. SMC-SD43 lost many members. Dominant, sub-dominant and satellite players altogether ensured gene and transcript redundancy. Conclusions: Our study demonstrates how starting from spontaneous sourdoughs and by reconstructing the synthetic community it was possible to unravel the metabolic contribution of individual players. To be resilient and performing, the sourdough metacommunity had to comprise dominant, sub-dominant and satellite players, which, only altogether, ensured gene and transcript redundancy. Overall, our study changed the paradigm and introduced theoretical foundations for steering food fermentations.