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Between Roquefort and Camembert: multiple recent gene transfers

16 May 2014 INRA-France

In the paste of Roquefort and on the surface of Camembert, the microscopic filamentous fungi Penicillium roqueforti and Penicillium camembertii are responsible for the formation of a greenish-blue mould in the former case and a so-called "bloom" in the latter.  Sequencing of the genomes of these two fungi, performed by research scientists from INRA, the Natural History Museum (MNHN), CNRS, Université d’Orsay and the company Genomic Vision, has recently, and surprisingly, shown that these genomes contain more than 250 strictly identical genes, thus indicating a transfer of genes between these two species.  This type of event, until now little described in eukaryotes, may therefore be much more common than previously thought.  This work was published in the journal Nature Communications on 10 January 2014.

Selection pressure exerted by humans

The fermented foods that have developed over successive millennia have produced very rich and specific food environments that have led to strong selection pressures on the micro-organisms involved, these having adapted rapidly to these new environments. This is the case for bacteria (the prokaryote1 micro-organisms classically involved in fermentation), and also for microscopic fungi such as Saccharomyces yeasts (used to make bread, beer or wine), Aspergillus filamentous fungi (Asiatic fermented foods) and Penicillium, used to manufacture cheeses and smoked and fermented meats.

A recent and massive transfer of genes

So-called horizontal gene transfers between species are well documented in bacteria, but much less so in fungi and other eukaryote organisms, although examples of such transfers in wine-making yeasts have been described in recent years. It therefore appeared that these transfers were rare, sporadic and had little impact in eukaroytes. However, the sequencing of several Penicillium species has suggested that the contrary might be true. Indeed, a comparison of the genomes of two important cheese fungi, Penicillium roqueforti and Penicillium camembertii has revealed the presence of numerous totally identical sequence fragments, while other genomic regions were only 85-90% similar. A molecular combing technique, which has markedly improved the final quality of the assembly of DNA sequences in Penicillium roqueforti, has shown that these fragments are assembled within a large DNA fragment of 575,000 base pairs called Wallaby, which contains around 250 genes. As well as all the Penicillium camembertii strains tested, large portions of this element were detected in some strains of Penicillium rubens (a penicillin-producing strain) and in other Penicillium strains from cheese environments. These different elements indicate the existence of a gene transfer that is recent (several thousands of years) and massive (in view of the number of strains and species concerned).

A competitive advantage

This Wallaby fragment bears genes that give the fungi a competitive advantage over other micro-organisms present in the environment. The research scientists estimated that it may have originated from Penicillium roqueforti and was then transferred to other species used to ferment cheeses within this new environment created by humans. This example reveals the extent to which horizontal gene transfers may be involved in the rapid evolution of microscopic fungi when driven by selection pressures.

Bacteria are prokaryotes; in other words, their DNA is not packaged in a nucleus.  Yeasts (single-cell fungi) and filamentous fungi (moulds) are eukaryote micro-organisms; in other words their DNA is contained in a nucleus isolated from the cytoplasm by a membrane. 

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