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Diversification, evolution and sub-functionalization of 70kDa heat-shock proteins in two sister species of antarctic krill: differences in thermal habitats, responses and implications under climate change.

Cascella K, Jollivet D, Papot C, Léger N, Corre E, Ravaux J, Clark MS, Toullec JY - PLoS ONE (2015)

Bottom Line: They therefore provide a useful model system for the investigation of adaptations to thermal tolerance.Initial CTmax studies showed that E. superba was slightly more thermotolerant than E. crystallorophias.Furthermore, analyses conducted to estimate the evolutionary rates and selection strengths acting on each gene tended to support the hypothesis that diversifying selection has contributed to the diversification of this gene family, and led to the selective relaxation on the inducible C form with its possible loss of function in the two krill species.

View Article: PubMed Central - PubMed

Affiliation: Sorbonne Universités, UPMC Université Paris 06, UMR 7144 CNRS, Equipe ABICE, Station Biologique de Roscoff, 29680 Roscoff, France; CNRS, UMR 7144, Adaptation et Diversité en Milieu Marin, Station Biologique de Roscoff, 29680 Roscoff, France.

ABSTRACT

Background: A comparative thermal tolerance study was undertaken on two sister species of Euphausiids (Antarctic krills) Euphausia superba and Euphausia crystallorophias. Both are essential components of the Southern Ocean ecosystem, but occupy distinct environmental geographical locations with slightly different temperature regimes. They therefore provide a useful model system for the investigation of adaptations to thermal tolerance.

Methodology/principal finding: Initial CTmax studies showed that E. superba was slightly more thermotolerant than E. crystallorophias. Five Hsp70 mRNAs were characterized from the RNAseq data of both species and subsequent expression kinetics studies revealed notable differences in induction of each of the 5 orthologues between the two species, with E. crystallorophias reacting more rapidly than E. superba. Furthermore, analyses conducted to estimate the evolutionary rates and selection strengths acting on each gene tended to support the hypothesis that diversifying selection has contributed to the diversification of this gene family, and led to the selective relaxation on the inducible C form with its possible loss of function in the two krill species.

Conclusions: The sensitivity of the epipelagic species E. crystallorophias to temperature variations and/or its adaptation to cold is enhanced when compared with its sister species, E. superba. These results indicate that ice krill could be the first of the two species to be impacted by the warming of coastal waters of the Austral ocean in the coming years due to climate change.

No MeSH data available.


Related in: MedlinePlus

Expression levels of hsp70 genes obtained by qPCR in two krill species: E. superba (red solid line) and E. crystallorophias (blue dotted line) during a heat shock of 3°C and 6°C whereas 0h group is control at 0°C.Heat shocks were carried out during 3h and 6h, and hsp70 expressions measured at those time on n = 6 to 10 individuals per group. Hsp70 expressions for both species were normalized by the 18S gene expression. To compare values, a Kruskal-Wallis test followed by a Dunn’s test were used to compare control groups (0h) and shocked groups (3h and 6h). Significant differences between mean normalized expressions are indicated by asterisks (*).
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pone.0121642.g005: Expression levels of hsp70 genes obtained by qPCR in two krill species: E. superba (red solid line) and E. crystallorophias (blue dotted line) during a heat shock of 3°C and 6°C whereas 0h group is control at 0°C.Heat shocks were carried out during 3h and 6h, and hsp70 expressions measured at those time on n = 6 to 10 individuals per group. Hsp70 expressions for both species were normalized by the 18S gene expression. To compare values, a Kruskal-Wallis test followed by a Dunn’s test were used to compare control groups (0h) and shocked groups (3h and 6h). Significant differences between mean normalized expressions are indicated by asterisks (*).

Mentions: The kinetics of expression of the different isoforms was analysed in both species in response to moderate thermal shocks of 3°C and 6°C. These temperatures were chosen in order to be compatible with possible scenarios of global warming (Fig. 5). The level of expression in control animals for each of the isoforms was different and suggested that the basal level of expression strongly depends on each isoform, providing further evidence for the sub-functionalization hypothesis. Both the molecular and phylogenetic analyses have enabled predictions to be made with regard to the status of the different isoforms, such that Hsp70A, B and E are potentially constitutive, Hsp70C is inducible and finally Hsp70D is mitochondrial. If A and B represent the constitutive forms, their basal expression is expected to be superior to the inducible form (C), as it is the case (Fig. 5). The forms D and E are less highly expressed. These observations on basal expression levels are validated by comparison with the FPKM values from the transcriptome analysis of E. crystallorophias (Table 3).


Diversification, evolution and sub-functionalization of 70kDa heat-shock proteins in two sister species of antarctic krill: differences in thermal habitats, responses and implications under climate change.

Cascella K, Jollivet D, Papot C, Léger N, Corre E, Ravaux J, Clark MS, Toullec JY - PLoS ONE (2015)

Expression levels of hsp70 genes obtained by qPCR in two krill species: E. superba (red solid line) and E. crystallorophias (blue dotted line) during a heat shock of 3°C and 6°C whereas 0h group is control at 0°C.Heat shocks were carried out during 3h and 6h, and hsp70 expressions measured at those time on n = 6 to 10 individuals per group. Hsp70 expressions for both species were normalized by the 18S gene expression. To compare values, a Kruskal-Wallis test followed by a Dunn’s test were used to compare control groups (0h) and shocked groups (3h and 6h). Significant differences between mean normalized expressions are indicated by asterisks (*).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4383606&req=5

pone.0121642.g005: Expression levels of hsp70 genes obtained by qPCR in two krill species: E. superba (red solid line) and E. crystallorophias (blue dotted line) during a heat shock of 3°C and 6°C whereas 0h group is control at 0°C.Heat shocks were carried out during 3h and 6h, and hsp70 expressions measured at those time on n = 6 to 10 individuals per group. Hsp70 expressions for both species were normalized by the 18S gene expression. To compare values, a Kruskal-Wallis test followed by a Dunn’s test were used to compare control groups (0h) and shocked groups (3h and 6h). Significant differences between mean normalized expressions are indicated by asterisks (*).
Mentions: The kinetics of expression of the different isoforms was analysed in both species in response to moderate thermal shocks of 3°C and 6°C. These temperatures were chosen in order to be compatible with possible scenarios of global warming (Fig. 5). The level of expression in control animals for each of the isoforms was different and suggested that the basal level of expression strongly depends on each isoform, providing further evidence for the sub-functionalization hypothesis. Both the molecular and phylogenetic analyses have enabled predictions to be made with regard to the status of the different isoforms, such that Hsp70A, B and E are potentially constitutive, Hsp70C is inducible and finally Hsp70D is mitochondrial. If A and B represent the constitutive forms, their basal expression is expected to be superior to the inducible form (C), as it is the case (Fig. 5). The forms D and E are less highly expressed. These observations on basal expression levels are validated by comparison with the FPKM values from the transcriptome analysis of E. crystallorophias (Table 3).

Bottom Line: They therefore provide a useful model system for the investigation of adaptations to thermal tolerance.Initial CTmax studies showed that E. superba was slightly more thermotolerant than E. crystallorophias.Furthermore, analyses conducted to estimate the evolutionary rates and selection strengths acting on each gene tended to support the hypothesis that diversifying selection has contributed to the diversification of this gene family, and led to the selective relaxation on the inducible C form with its possible loss of function in the two krill species.

View Article: PubMed Central - PubMed

Affiliation: Sorbonne Universités, UPMC Université Paris 06, UMR 7144 CNRS, Equipe ABICE, Station Biologique de Roscoff, 29680 Roscoff, France; CNRS, UMR 7144, Adaptation et Diversité en Milieu Marin, Station Biologique de Roscoff, 29680 Roscoff, France.

ABSTRACT

Background: A comparative thermal tolerance study was undertaken on two sister species of Euphausiids (Antarctic krills) Euphausia superba and Euphausia crystallorophias. Both are essential components of the Southern Ocean ecosystem, but occupy distinct environmental geographical locations with slightly different temperature regimes. They therefore provide a useful model system for the investigation of adaptations to thermal tolerance.

Methodology/principal finding: Initial CTmax studies showed that E. superba was slightly more thermotolerant than E. crystallorophias. Five Hsp70 mRNAs were characterized from the RNAseq data of both species and subsequent expression kinetics studies revealed notable differences in induction of each of the 5 orthologues between the two species, with E. crystallorophias reacting more rapidly than E. superba. Furthermore, analyses conducted to estimate the evolutionary rates and selection strengths acting on each gene tended to support the hypothesis that diversifying selection has contributed to the diversification of this gene family, and led to the selective relaxation on the inducible C form with its possible loss of function in the two krill species.

Conclusions: The sensitivity of the epipelagic species E. crystallorophias to temperature variations and/or its adaptation to cold is enhanced when compared with its sister species, E. superba. These results indicate that ice krill could be the first of the two species to be impacted by the warming of coastal waters of the Austral ocean in the coming years due to climate change.

No MeSH data available.


Related in: MedlinePlus