Evolutionary genomics reveals plant-associated origins of acetic acid bacteria in fermented food

Abstract

Humans have historically relied on acetic acid bacteria (AAB) for food fermentation, yet their origins likely trace back to free-living species outside of human environments. In nature, plants, fruit flies, and social insects host AAB. However, the evolutionary transitions of AAB from symbiotic hosts to fermented foods remain ambiguous. Here, we conduct a comprehensive phylogenomic analysis of 570 publicly available AAB genomes. Unlike other ferment-associated microbes, ferment-associated AAB appear to have exclusively evolved from clades inhabiting plants, and never social insect hosts. In particular, the sugar-rich fruits and flowers of angiosperms appear to promote diversification of AAB and transitions to fermented food habitats. Genomic features are similar in plant- and ferment-associated AAB; conversely, social insect-associated AAB have reduced genome sizes and number of genes, which may have limited their functional capability to disperse into ferments. Plant- and ferment-associated AAB share in the ability to metabolise diverse plant carbohydrates, though both produce habitat-specific carbohydrate-active enzymes. In contrast, metabolic capacity is reduced in social insect-associated AAB. By tracing the phylogenomics of this clade, we understand how evolution forged AAB capable of performing metabolic work for humans, shaping the past and potential futures of fermentation.