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Rapid Phenotypic and Metabolomic Domestication of Wild Penicillium Molds on Cheese

Summary

This research shows how wild molds can rapidly evolve and adapt when growing on cheese, becoming more like the domesticated molds used in cheese production. Within just a few weeks, wild molds lost their blue-green color, produced fewer spores, stopped making toxins, and started producing pleasant cheese-like aromas instead of musty smells. This process happens naturally in cheese aging environments. Impacts on everyday life: • Demonstrates how safe, flavorful cheese cultures can develop naturally from wild molds • Suggests new ways to develop novel cheese cultures for unique flavors and textures • Helps explain how traditional cheese-making practices led to the development of modern cheese cultures • Shows how changing an organism’s environment can rapidly alter its characteristics • Provides insights into making fermented foods safer by understanding how harmful traits can be eliminated

Background

Fermented foods provide novel ecological opportunities for natural populations of microbes to evolve through successive recolonization of resource-rich substrates. While comparative genomic data have reconstructed the evolutionary histories of microbes adapted to food environments, experimental studies directly demonstrating the process of domestication are lacking for most fermented food microbes.

Objective

To experimentally demonstrate how wild Penicillium molds may be unintentionally domesticated in the cheese aging environment, specifically determining how quickly Penicillium could evolve new phenotypes on cheese, how Penicillium traits change during domestication on cheese, and what properties of the cheese environment promote domestication of Penicillium.

Results

Over a period of just a few weeks, populations of wild Penicillium strains serially passaged on cheese showed reduced pigment, spore, and mycotoxin production. Domesticated strains exhibited a dramatic shift in volatile metabolite production, changing from earthy/musty compounds to fatty and cheesy volatiles. RNA sequencing revealed significant decreases in expression of 356 genes in domesticated strains, with enrichment of many secondary metabolite production pathways among downregulated genes. Limited competition and high nutrient availability in the cheese environment promoted rapid trait evolution.

Conclusion

The study demonstrates that cheese aging environments can promote rapid domestication of wild Penicillium molds through loss of energetically costly traits like spore production, pigmentation, and mycotoxin production. The findings suggest that new strains of Penicillium for cheese production could potentially be generated through intentional and controlled domestication processes, though further work is needed to confirm stability and safety.
  • Published in:mBio,
  • Study Type:Experimental Evolution Study,
  • Source: 10.1128/mBio.02445-19
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