Balanced polymorphism at the Pgm-1 locus of the Pompeii worm Alvinella pompejana and its variant adaptability is only governed by two QE mutations at linked sites

The polychaete Alvinella pompejana lives exclusively on the walls of deep-sea hydrothermal chimneys along the East Pacific Rise and, display specific adaptations to withstand high temperature and hypoxia associated with this highly variable habitat. Previous studies revealed the existence of a balanced polymorphism on the enzyme phosphoglucomutase associated with thermal variations where allozymes 90 and 100 exhibited different optimal activities and thermostabilities. The exploration of the mutational landscape of the phosphoglucomutase1 revealed the maintenance of four highly divergent allelic lineages encoding the three most frequent electromorphs over the worms geographic range. This polymorphism is only governed by two linked amino-acid replacements located in exon 3 (E155Q and E190Q). A two-niches model of selection with cold and hot conditions represents the most likely way for the long-term persistence of these isoforms. Using directed mutagenesis, overexpression of the three recombinant variants allowed us to test the additive effect of these two mutations on the biochemical properties of this enzyme. Results are coherent with those previously obtained from native proteins and reveal a thermodynamic trade-off between the protein thermostability and catalysis, which is likely to have maintained these functional phenotypes prior to the geographic separation of populations across the Equator, about 1.2 Mya.