The polychaete Alvinella pompejana lives exclusively on the walls of deep-sea hydrothermal chimneys along the East Pacific Rise (EPR), and displays specific adaptations to withstand the high temperatures and hypoxia associated with this highly variable habitat. Previous studies have revealed the existence of a balanced polymorphism on the enzyme phosphoglucomutase associated with thermal variations, where allozymes 90 and 100 exhibit different optimal activities and thermostabilities. Exploration of the mutational landscape of phosphoglucomutase 1 revealed the maintenance of four highly divergent allelic lineages encoding the three most frequent electromorphs over the geographic range of A. pompejana. This polymorphism is only governed by two linked amino acid replacements, located in exon 3 (E155Q and E190Q). A two-niche model of selection, including ‘cold’ and ‘hot’ conditions, represents the most likely scenario for the long-term persistence of these isoforms. Using directed mutagenesis and the expression of the three recombinant variants allowed us to test the additive effect of these two mutations on the biochemical properties of this enzyme. Our results are coherent with those previously obtained from native proteins, and reveal a thermodynamic trade-off between 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 million years ago.

No abstract

The polychaete Alvinella pompejana lives exclusively on the walls of deep-sea hydrothermal vents along the East Pacific Rise. This environment is considered as extreme and highly variable and the worm displays specific adaptations to withstand high temperature and hypoxia. Previous studies revealed the existence of a balanced polymorphism on the enzyme phosphoglucomutase associated with differences in the thermal habitat of the worm. Allozymes 90 and 100 exhibited different optimal enzyme activities and thermostabilities.The exploration of the mutational landscape for allozyme variation of the phosphoglucomutase1 revealed the maintenance of four highly divergent allelic lineages that encode the three most frequent electromorphs, these alleles occurring at different frequencies in populations over the worm's geographic range. Enzyme polymorphism is only governed by two linked amino-acid replacements located in exon 3 (E155Q and E190Q). Unlike other studies dealing with the non-synonymous variations of the Pgm genes, these substitutions are not linked to other cryptic amino-acid polymorphisms. Overdominance under specific environmental 'hot' conditions should represent 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 explain the long-term selection of these functional phenotypes before their geographic separation across the Equator with the emergence of a barrier to dispersal, about 1.2 Mya.