A novel fungal family of oligopeptide transporters identified by functional metatranscriptomics of soil eukaryotes
Functional environmental genomics has the potential to identify novel biological functions that the
systematic sequencing of microbial genomes or environmental DNA may fail to uncover. We
targeted the functions expressed by soil eukaryotes using a metatranscriptomic approach based on
the use of soil-extracted polyadenylated messenger RNA to construct environmental complementary DNA expression libraries. Functional complementation of a yeast mutant defective in
di/tripeptide uptake identified a novel family of oligopeptide transporters expressed by fungi. This
family has a patchy distribution in the Basidiomycota and Ascomycota and is present in the genome
of a Saccharomyces cerevisiae wine strain. High throughput phenotyping of yeast mutants
expressing two environmental transporters showed that they both displayed broad substrate
specificity and could transport more than 60–80 dipeptides. When expressed in Xenopus oocytes
one environmental transporter induced currents upon dipeptide addition, suggesting protoncoupled co-transport of dipeptides. This transporter was also able to transport specifically cysteine.
Deletion of the two copies of the corresponding gene family members in the genome of the wine
yeast strain severely reduced the number of dipeptides that it could assimilate. These results
demonstrate that these genes are functional and can be used by fungi to efficiently scavenge the
numerous, low concentration, oligopeptides continuously generated in soils by proteolysis.
The ISME Journal (2011) 5, 1871–1880; doi:10.1038/ismej.2011.67; published online 9 June 2011