Protein analysis and gene expression indicate differential vulnerability of Iberian fish species under a climate change scenario

Abstract

Current knowledge on the biological responses of freshwater fish under projected scenarios of climate change remains limited. Here, we examine differences in the protein configuration of two endemic Iberian freshwater fish species, Squalius carolitertii and the critically endangered S. torgalensis that inhabit in the Atlantic-type northern and in the Mediterranean-type southwestern regions, respectively. We performed protein structure modeling of fourteen genes linked to protein folding, energy metabolism, circadian rhythms and immune responses. Structural differences in proteins between the two species were found for HSC70, FKBP52, HIF1α and GPB1. For S. torgalensis, besides structural differences, we found higher thermostability for two proteins (HSP90 and GBP1), which can be advantageous in a warmer environment. Additionally, we investigated how these species might respond to projected scenarios of 3° climate change warming, acidification (ΔpH = -0.4), and their combined effects. Significant changes in gene expression were observed in response to all treatments, particularly under the combined warming and acidification. While S. carolitertii presented changes in gene expression for multiple proteins related to folding (hsp90aa1, hsc70, fkbp4 and stip1), only one such gene was altered in S. torgalensis (stip1). However, S. torgalensis showed a greater capacity for energy production under both the acidification and combined scenarios by increasing cs gene expression and maintaining ldha gene expression in muscle. Overall, these findings suggest that S. torgalensis is better prepared to cope with projected climate change. Worryingly, under the simulated scenarios, disturbances to circadian rhythm and immune system genes (cry1aa, per1a and gbp1) raise concerns for the persistence of both species, highlighting the need to consider multi-stressor effects when evaluating climate change impacts upon fish. This work also highlights that assessments of the potential of endangered freshwater species to cope with environmental change are crucial to help decision-makers adopt future conservation strategies.

Adaptation and convergence in circadian-related genes in Iberian freshwater fish

“…Subsequent studies with those genes reinforce the dependence on temperature for proper entrainment of the circadian system in these species by showing a response in expression of cry1aa and per1a genes in S. carolitertii when subjected to a simulated scenario of moderate climate change (Jesus et al 2017). Other studies connected the circadian system with stress response through a network involving heat-shock proteins (HSP) (Jerônimo et al 2017).…”

“…This mutation consists of a substitution of an uncharged for a positively charged amino acid with acid properties, leading to a decrease in the overall charge of the protein, and consequently a lower pI. Moreover, previous studies with S. torgalensis and S. carolitertii revealed that expression of cry1aa is affected either by water temperature and pH in these species (Jesus et al 2017). Previous studies have been conducted in fish species to understand the effects of extreme water pH on the internal homeostasis of the organisms (e.g.…”

“…Water pH is another factor that has been shown to influence several physiological aspects of fish, either at gene expression and other biochemical levels (e.g. Jesus et al 2017;Xu et al 2017;Jesus et al 2018). Thus, water pH my act as a selective pressure, specifically an increased alkalinity (i.e.…”

“…Previous studies have been conducted in fish species to understand the effects of extreme water pH on the internal homeostasis of the organisms (e.g. Xu et al 2013;Kavembe et al 2015;Jesus et al 2017;Xu et al 2017;Jesus et al 2018), but to our knowledge few studies related protein properties with changes in water pH (but see Jesus et al 2017).…”

Advances in Comparative Immunology

“…The effectiveness of the insect immune system may be heightened by heat shock (Wojda 2016), but this is different from the chronic temperature rises that are occurring now. Immune competence declined in two species of freshwater fish of the Iberian Peninsula (Jesus et al 2017). Hibernation and other survival strategies by poikilothermic animals (Storey and Storey 2017) depend heavily on ambient temperatures, which are likely to increase by global warming.…”