Oral Presentation Society for Molecular Biology and Evolution Conference 2016

What makes the fungi cheesy: the adaptive genomic toolbox of Penicillium molds revealed by between- and within-species comparisons (#138)

Ricardo C Rodríguez de la Vega 1 , Emilie Dumas 1 , Jeanne Ropars 2 , Manuela Lopez-Villavicencio 3 , Sandrine Lacoste 3 , Stephanie Le Prieur 1 , Robert Debuchy 4 , Sophie Siguenza 5 , Jerome Gouzy 5 , Joelle Dupont 3 , Antoine Branca 1 , Tatiana Giraud 1
  1. Ecologie Systematique et Evolution, Univ. Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, Orsay, France
  2. Fungal Biology and Pathogenicity, Institut Pasteur, Paris, France
  3. ISEB, Museum National d'Histoire Naturelle, Paris, France
  4. IGM, Univ. Paris-Sud, Orsay, France
  5. LIPM, Institut National de la Recherche Agronomique, Toulouse, France

Studying parallel evolution on the same environment is a powerful approach for understanding the genomic processes of adaptation. Several species of the ubiquitous Penicillium molds have been independently domesticated for the maturing of cheese since at least the 18th century. Two key Penicillium species used for cheese-making are P. roqueforti for blue cheeses and P. camemberti for soft surface-ripened cheeses. These distantly related species have been independently selected for optimal growth and enzymatic activities in a human-made nutrient-rich environment containing numerous bacterial and fungal competitors. Domestication is an excellent model for studies of adaptation because it involves recent and strong selection on a few, identified traits, here we present part of our studies on the genomic footprints of domestication in chese-making fungi. First, by comparing the genomes of 29 Penicillium species, we found that adaptation to the cheese medium was associated with parallel gains, losses and positive selection on genes involved in the utilization of the cheese nutrients and competition with other microorganisms. A substantial part of the gene family expansions correspond to previously identified horizontally-transferred regions recently acquired by the cheese-making fungi1. Second, by focusing on the intraspecific genetic diversity at the whole genome level in 30 P. roqueforti strains and 3 closely related species from different sources (used for chese-making and growing in the wild), we reveal two independently domesticated groups of P. roqueforti, thus giving yet another example of the ease of Penicillium species to adapt on a short evolutionary timescale. Experiments validated fitness differences between the genetic groups. Overall, we show that adaptation can occur rapidly in eukaryotes, through the acquisition of a novel genomic metabolic toolbox. These findings contribute to improve our understanding of the genomic processes of adaptation to rapid environmental changes.

  1. Ropars, Rodríguez de la Vega, et al. (2015). Adaptive horizontal gene transfers between multiple cheese-associated fungi. Current Biology 25(19):2562-2569 http://dx.doi.org/10.1016/j.cub.2015.08.025.