Gene loss, repression, amplification, and horizontal acquisition shape galactose/melibiose metabolism in fission yeast.

Abstract

Natural variation in metabolism is a key driver of microbial adaptation. While galactose utilization is well studied in budding yeasts, it remains poorly understood in the fission yeast <i>Schizosaccharomyces pombe</i>. Here, we reveal extensive natural variation in galactose utilization across <i>S. pombe</i> isolates-from complete deficiency (Gal^-) to exceptionally fast growth (Gal^F). Gal^- strains fall into two classes: one with deletions of the <i>gal</i> gene cluster (via three distinct mechanisms) and another with intact but repressed <i>gal</i> genes. In contrast, Gal^F is driven by an amplified gene cluster absent from the reference genome-the <i>gal</i>-<i>mel</i> cluster (GMC)-which also confers melibiose utilization (Mel⁺). Mel⁺ is exclusively linked to the GMC, except in one strain harboring a standalone melibiase gene. Phylogenetic analyses indicate that horizontal gene transfer may underlie these adaptive traits. Together, our work demonstrates how diverse mechanisms-gene loss, repression, amplification, and horizontal acquisition-shape metabolic diversity and ecological specialization in fission yeast.