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.

Alexis Bioy,Stéphane Hourdez,Anne-Sophie Le Port,Marie Verheye,Jean Mary,Baptiste Faure,Didier Jollivet,Emeline Sabourin,Patrice Piccino

doi:10.3390/genes13020206

Abstract

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.

Highlights

A central goal in evolutionary biology is to understand the origin and maintenance of polymorphisms sculpted by natural selection and, how the mean phenotype of a population evolves under heterogeneous and/or changing conditions [1]
A few decades ago, a series of enzymes interacting in the glycolytic cycle, mostly associated with isomerase and mutase functions, such as phosphoglucose isomerase (PGI), mannose phosphate isomerase (MPI), and phosphoglucomutase (PGM), were shown to display isoforms that may be the subject of natural selection, leading to habitat-driven differentiation in populations according to temperature, wave action, or metallic pollution [2,3,4,5,6,7,8,9,10]
We explored the mutational landscape of the gene to search for traces of balancing selection in the vicinity of the amino acid substitutions that led to these isoforms and assess their long-term duration

Summary

Introduction

A central goal in evolutionary biology is to understand the origin and maintenance of polymorphisms sculpted by natural selection and, how the mean phenotype of a population evolves under heterogeneous and/or changing conditions [1]. Many studies have investigated the maintenance of enzyme polymorphisms by selective processes for species exposed to environmental gradients such as temperature, salinity, or desiccation [2]. Alleles encoding the enzyme phosphoglucomutase have been widely studied, with the aim of testing the hypothesis of differential and/or balancing selection. This was mainly achieved by looking at allele [3,4,12] and heterozygote [13] frequencies in populations, as well as assessing either the fitness of individuals carrying alleles suspected to be locally advantageous along latitudinal clines [14] or the kinetic properties of the enzyme isoforms themselves [6,12]

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Conclusion