Evolution under pressure and the adaptation of visual pigment compressibility in deep-sea environments

Abstract

Understanding the link between how proteins function in animals that live in extreme environments and selection on specific properties of amino acids has proved extremely challenging. Here we present the discovery of how the compressibility of opsin proteins in two evolutionarily distinct animal groups, teleosts and cephalopods, appears to be adapted to the high-pressure environment of the deep-sea. We report how in both groups, opsins in deeper living species are calculated to be less compressible. This is largely due to a common set of amino acid sites (bovRH#159, 196, 213, 275) undergoing positive destabilizing selection in six of the twelve amino acid physiochemical properties that determine protein compressibility. This suggests a common evolutionary mechanism to reduce the adiabatic compressibility of opsin proteins. Intriguingly, the sites under selection are on the proteins' outer faces at locations known to be involved in opsin-opsin dimer interactions.

Evolution of the visual sensory system in cichlid fishes from crater lake Barombi Mbo in Cameroon

“…Amino acid position 214 of RH2Aα, which is not among the known key spectral tuning sites (Yokoyama, ), is located in the transmembrane region of the protein, but is not part of the chromophore‐binding pocket (Spady et al, ). However, this position is located in close proximity of an amino acid site responsible for protein stability under higher pressure (position 213; Porter, Roberts, & Partridge, ), and a mutation at the same site (S214P) is known to cause tritanopia in human (i.e., malfunction of the blue cones; Weitz et al, ), suggesting that this position in the RH2Aα protein is of functional relevance.…”

Organic acids under pressure: elastic properties, negative mechanical phenomena and pressure induced phase transitions in the lactic, maleic, succinic and citric acids

“…The interest in the research of the effect of high pressure on living systems was originated by the discovery of piezophile organisms in the deep marine environments. [134][135][136][137][138][139] The corresponding studies involved not only the investigation of the pressure adaptation mechanisms of these organisms but also the possible role of high pressure in the origin of life. [140][141][142] In the research of organic materials under pressure, the main purpose is generally the study of the modification of the molecular structure and properties of the material under study associated to changes in the noncovalent interactions present in the system, although the production and analysis of drastic structural changes and the detection of phase transitions is also extremely interesting.…”

Evolution of nonspectral rhodopsin function at high altitudes

“…This is likely in part because of the caveat that investigating rhodopsin cold adaptation in natural systems may be confounded by differences in environment. Naturally occurring habitat transitions may also be accompanied by other, concurrent, selective pressures on rhodopsin function, such as changes in light spectra (12,13,28), pressure (39,40), and temperature (34). To disentangle such effects from other aspects of rhodopsin function, we selected a system that maximized consistency across ambient spectral environments.…”