Abstract
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 worm’s 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.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
The manuscript has been revised following two rounds of revision in G3. The text has been greatly shortened. We applied a singleton correction to our sequence datasets in order to compare alignments obtained from direct sequencing and the Mark-Cloning-Recapture method, redrawn figures dealing with the allele relationship and the distribution of the genetic diversity over the gene with a sliding window, performed additional analyses on recombination with the Software Phase and simulated structured coalescents with asymmetric migration using the software msms taking into account alternative selection models.