Population genomics ofAspergillus sojaeis shaped by the food environment

Abstract

AbstractTraditional fermented foods often contain specialized microorganisms adapted to the unique food environment. For example, the filamentous moldAspergillus oryzae, used in saké fermentation, has evolved to thrive in starch-rich conditions compared to its wild ancestor,Aspergillus flavus. Similarly,Aspergillus sojaeis used in soybean-based food fermentations (e.g.miso and shochu) and is closely related toAspergillus parasiticus. Here, we investigated the impact of long-termA. sojaeusage in soybean fermentation on population structure, genome variation, and phenotypic traits. We analyzed 12A. sojaeand 10A. parasiticusgenomes, along with phenotypic characteristics of 15 isolates. Our results revealed thatA. sojaeisolates formed a distinct population separate fromA. parasiticusand displayed remarkably low levels of genetic diversity, indicative of a recent clonal expansion. Genome comparisons revealed numerous loss-of-function mutations inA. sojae, notably in genes responsible for secondary metabolite production, including genes in the aflatoxin encoding gene cluster. Consequently,A. sojaelacked aflatoxin production, while it varied amongA. parasiticusisolates. No other significant differences were observed in growth rates or other measured phenotypic traits betweenA. sojaeandA. parasiticus. These findings suggest thatA. sojaemay have evolved from a population ofA. parasiticusand lost the ability to produce some secondary metabolites. To elucidate the phenotypic differences betweenA. sojaeandA. parasiticus, future work should focus on the influence of wild and food-associated strains on the sensory aspects and microbial community dynamics of fermented soy products.Significance StatementLike plants and animals, microbes were also domesticated by humans, however relatively little is known about how the process of domestication shapes microbial genomes and traits. We found that isolates ofAspergillus sojae, a mold used in the production of miso and soy sauce, makeup a less toxic group that is genetically distinct from its closely related wild ancestorAspergillus parasiticus. Our analyses shed new light on commonalities observed across filamentous molds adapted to the food environment.