Cold-stable eye lens crystallins of the Antarctic nototheniid toothfishDissostichus mawsoniNorman

Abstract

SUMMARY The eye lenses of the Antarctic nototheniid fishes that inhabit the perennially freezing Antarctic seawater are transparent at –2°C,whereas the cold-sensitive mammalian and tropical fish lenses display cold-induced cataract at 20°C and 7°C, respectively. No cold-cataract occurs in the giant Antarctic toothfish Dissostichus mawsoni lens when cooled to temperatures as low as –12°C, indicating highly cold-stable lens proteins. To investigate this cold stability, we characterised the lens crystallin proteins of the Antarctic toothfish, in parallel with those of the sub-tropical bigeye tuna Thunnus obesusand the endothermic cow Bos taurus, representing three disparate thermal climes (–2°C, 18°C and 37°C, respectively). Sizing chromatography resolved their lens crystallins into three groups,α/βH, β and γ, with γ crystallins being the most abundant (>40%) lens proteins in fish, in contrast to the cow lens where they comprise only 19%. The upper thermal stability of these crystallin components correlated with the body temperature of the species. In vitro chaperone assays showed that fish α crystallin can protect same-species γ crystallins from heat denaturation, as well as lysozyme from DTT-induced unfolding, and therefore are small Heat Shock Proteins (sHSP)like their mammalian counterparts. Dynamic light scattering measured an increase in size of αγ crystallin mixtures upon heating, which supports formation of the αγ complex as an integral part of the chaperone process. Surprisingly, in cross-species chaperone assays, tunaα crystallins only partly protected toothfish γ crystallins, while cow α crystallins completely failed to protect, indicating partial and no αγ interaction, respectively. Toothfish γ was likely to be the component that failed to interact, as the supernatant from a cowα plus toothfish γ incubation could chaperone cow γcrystallins in a subsequent heat incubation, indicating the presence of uncomplexed cow α. This suggests that the inability of toothfish γcrystallins to fully complex with tuna α, and not at all with the cowα crystallins, may have its basis in adaptive changes in the protein that relate to the extreme cold-stability of the toothfish lens.

Structure and Dynamics of the Fish Eye Lens Protein, γM7-Crystallin

“…Consistently, other γ M-crystallins from Antarctic toothfish and bigeye tuna also showed substantially lower temperature stability than the γ -crystallins from B. Taurus . 40 …”

“…41 It is plausible that missing such an interaction may contribute to the decreased protein stability of zebrafish γ M7 and other γ M-crystallins, as shown in this study and for several examples from other fish. 40 …”

“…The observed lower heat stability of γ M7-, γ M2b-, and some other γ M-crystallins indicates that high methionine content does not itself increase protein stability as speculated previously. 10 In general, the thermal stability of γ -crystallins appears to correlate with the body temperature, 40 with higher stability in mammalian crystallins. Alternatively, the flexibility of methionine side chains could facilitate intermolecular interactions.…”

Model of gene expression in extreme cold - reference transcriptome for the high-Antarctic cryopelagic notothenioid fish Pagothenia borchgrevinki

“…The evolution of these species in the freezing Southern Ocean waters has led to many shared adaptations to their ice-laden environment. These include newly minted genes with novel functions such as the blood borne antifreeze glycoproteins that prevent ice expansion in their body fluids and preserve life [2], as well as adaptive modifications of pre-existing genes to effectively allow optimal function at low temperatures [3-5]. The evolutionary history of these species in the world’s coldest marine waters makes them excellent models for functional and molecular studies of evolutionary adaptations to extreme environment, however, genomic or transcriptomic level resources for the Antarctic notothenioids, while emerging, currently exist for only a few species [6,7], and are entirely missing for species endemic to the highest latitude and harshest Antarctic marine environment.…”

Adaptations to an extreme environment: retinal organisation and spectral properties of photoreceptors in Antarctic notothenioid fish

“…Therefore, notothenioid fish are exposed to a light environment that is quite different from other aquatic species. A recent study has detailed the cold adaptation of the eye lens of these fish (Kiss et al, 2004), but so far very little information is available on the visual system of these fish in terms of the spectral sensitivity of their photoreceptors.…”