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Sourdough bread is an ancient fermented food that has sustained humans around the world for thousands of years. It is made from a sourdough ‘starter culture’ which is maintained, portioned, and shared among bread bakers around the world. The starter culture contains a community of microbes made up of yeasts and bacteria, which ferment the carbohydrates in flour and produce the carbon dioxide gas that makes the bread dough rise before baking. The different acids and enzymes produced by the microbial culture affect the bread’s flavor, texture and shelf life. However, for such a dependable staple, sourdough bread cultures and the mixture of microbes they contain have scarcely been characterized. Previous studies have looked at the composition of starter cultures from regions within Europe. But there has never been a comprehensive study of how the microbial diversity of sourdough starters varies across and between continents. To investigate this, Landis, Oliverio et al. used genetic sequencing to characterize the microbial communities of sourdough starters from the homes of 500 bread bakers in North America, Europe and Australasia. Bread makers often think their bread’s unique qualities are due to the local environment of where the sourdough starter was made. However, Landis, Oliverio et al. found that geographical location did not correlate with the diversity of the starter cultures studied. The data revealed that a group of microbes called acetic acid bacteria, which had been overlooked in past research, were relatively common in starter cultures. Moreover, starters with a greater abundance of this group of bacteria produced bread with a strong vinegar aroma and caused dough to rise at a slower rate. This research demonstrates which species of bacteria and yeast are most commonly found in sourdough starters, and suggests geographical location has little influence on the microbial diversity of these cultures. Instead, the diversity of microbes likely depends more on how the starter culture was made and how it is maintained over time. 

ABSTRACT Fermented foods provide novel ecological opportunities for natural populations of microbes to evolve through successive recolonization of resource-rich substrates. Comparative genomic data have reconstructed the evolutionary histories of microbes adapted to food environments, but experimental studies directly demonstrating the process of domestication are lacking for most fermented food microbes. Here, we show that during adaptation to cheese, phenotypic and metabolomic traits of wild Penicillium molds rapidly change to produce domesticated phenotypes with properties similar to those of the industrial cultures used to make Camembert and other bloomy rind cheeses. Over a period of just a few weeks, populations of wild Penicillium strains serially passaged on cheese had reduced pigment, spore, and mycotoxin production. Domesticated strains also had a striking change in volatile metabolite production, shifting from production of earthy or musty volatile compounds (e.g., geosmin) to fatty and cheesy volatiles (e.g., 2-nonanone, 2-undecanone). RNA sequencing demonstrated a significant decrease in expression of 356 genes in domesticated strains, with an enrichment of many secondary metabolite production pathways in these downregulated genes. By manipulating the presence of neighboring microbial species and overall resource availability, we demonstrate that the limited competition and high nutrient availability of the cheese environment promote rapid trait evolution of Penicillium molds. IMPORTANCE Industrial cultures of filamentous fungi are used to add unique aesthetics and flavors to cheeses and other microbial foods. How these microbes adapted to live in food environments is generally unknown as most microbial domestication is unintentional. Our work demonstrates that wild molds closely related to the starter culture Penicillium camemberti can readily lose traits and quickly shift toward producing desirable aroma compounds. In addition to experimentally demonstrating a putative domestication pathway for P. camemberti , our work suggests that wild Penicillium isolates could be rapidly domesticated to produce new flavors and aesthetics in fermented foods.