Genomics and synthetic community experiments uncover the key metabolic roles of acetic acid bacteria in sourdough starter microbiomes

Abstract

While research on the sourdough microbiome has primarily focused on lactic acid bacteria (LAB) and yeast, recent studies have found that acetic acid bacteria (AAB) are also common members. However, the ecology, genomic diversity, and functional contributions of AAB in sourdough remain unknown. To address this gap, we sequenced 29 AAB genomes, including three that represent putatively novel species, from a collection of over 500 sourdough starters surveyed globally from community scientists. We found variation in metabolic traits related to carbohydrate utilization, nitrogen metabolism, and alcohol production, as well as in genes related to mobile elements and defense mechanisms. Sourdough AAB genomes did not cluster when compared to AAB isolated from other environments, although a subset of gene functions were enriched in sourdough isolates. The lack of a sourdough-specific genomic cluster may reflect a nomadic lifestyle of AAB. To assess the consequences of AAB on the emergent function of sourdough starter microbiomes, we constructed synthetic starter microbiomes, varying only the AAB strain included. All AAB strains increased acidification of synthetic sourdough starters relative to yeast and LAB by 18.5% on average. Different strains of AAB had distinct effects on the profile of synthetic starter volatiles. Taken together, our results begin to define the key ways in which AAB shape emergent properties of starters and suggest that differences in gene content resulting from intraspecies diversification can have community-wide consequences on emergent function. ImportanceThis study is the first comprehensive genomic and ecological study of acetic acid bacteria isolated from sourdough starters. By combining comparative genomics with manipulative experiments using synthetic microbiomes, we demonstrate that even strains with >97% ANI can shift important microbiome functions, underscoring the importance of species and strain diversity in microbial systems. We also show the utility of sourdough starters as a model system to understand the consequences of genomic diversity at the strain and species level on multispecies communities. These results are also relevant to industrial and home-bakers as we uncover the importance of AAB in shaping properties of sourdough starters that have direct impact on sensory notes and quality of sourdough bread.