Coping with a warming world: genetic studies on thermal adaptation and links to membrane saturation in Antarctic fish

Abstract

Stearoyl-CoA desaturase (SCD) plays a key role in thermal adaptation across organisms, allowing alteration of membranes in response to temperature change. Thermal adaptive signatures at the gene sequence level and in the primary structure of the SCD protein require investigation, especially in Antarctic fish. Owing to the stenothermal nature of Antarctic fish, it remains unclear whether they have retained capacity to modulate their membranes in response to warming temperatures. The hypothesis that membrane saturation, a major thermal adaptive mechanism, will occur at reduced capacities in Antarctic notothenioid fish in response to elevated temperatures was tested SCD sequences were isolated from 21 fish species (Antarctic and non-Antarctic notothenioids, and non-notothenioid Antarctic fish species). Phylogenetic analyses supported the ancestral SCD1 duplication into SCD1a and SCD1b. Lineage-specific duplication and loss of gene duplicates were identified for specific orders of fish. Cold adapted notothenioids (Antarctic and non-Antarctic with Antarctic ancestry) SCD isoform sequences were evolutionarily distinct from non-Antarctic sequences. SCD1a and 1b from Antarctic fish displayed more diversity with amino acid composition varying across the isoforms. SCD1a isoforms had more sites under positive selection and a higher rate of molecular evolution in Antarctic fish than SCD1b, suggesting neofunctionalisation of SCD1a. Ubiquitous tissue expression of SCD1b was seen in both the Antarctic species Trematomus bernacchii and Pagothenia borchgrevinki, while ubiquitous expression of SCD1a isoform was seen in T. bernacchii but not in P.borchgrevinki. Transcriptional response of the SCD isoforms, along with the biochemical response of membrane saturation, in T. bernacchii and P. borchgrevinki livers were determined in fish acclimated at 0°C (control temperature), 4°C and 6°C. Overall, temperature had a significant effect on the expression of SCD1a and SCD1b in T. bernacchii, while expression of SCD1a was low to be detected by qPCR in P. borchgrevinki. Membrane lipid composition of Antarctic fish species varied significantly when compared to the New Zealand Perciforme species Notolabrus celidotus. Thermal acclimation at 4°C did not result in any detectable change in membrane saturation state or membrane cholesterol in either Antarctic species. However, 6°C thermal acclimation induced a homeoviscous adaptive (HVA) response in the benthic species T. bernacchii, as shown by the significant increase in membrane saturated fatty acids, and a significant decline in unsaturated fatty acids. HVA response was not observed in P. borchgrevinki. This is the first study to determine thermal adaptive signatures in the SCD gene of Antarctic fish and provides evidence for asymmetric molecular evolution of SCD. This provides a framework for future functional work. This is also the first study to show a homeoviscous response to higher temperature in an Antarctic fish although only for one of the two species examined.