Evolution of chaperome gene expression and regulatory elements in the antarctic notothenioid fishes

Abstract

Confined within the cold-stable Southern Ocean, Antarctic notothenioid fishes have undergone an evolutionary loss of the inducible heat shock response (HSR), while facing perpetual low-temperature challenges to cellular proteostasis. This study examines how evolution in chronic cold has affected the shared cellular apparatus that mediates proteostasis under normal and heat stressed states. To deduce Antarctic-specific changes, we compared native expression levels across the full suite of chaperome genes and assessed the structural integrity of two crucial HSR regulators – Heat Shock Factor 1 (HSF1) that activates HSR, and heat shock elements (HSEs), the binding sites for HSF1 – between Antarctic fishes and the basal temperate notothenioid Eleginops maclovinus. Native expression levels of Antarctic fish chaperomes showed very modest changes overall, contrary to the common view of constitutive upregulation in the cold. Only a few cytosolic HSP70 genes showed greater transcription, with only the ancestrally-inducible HSPA6 strongly upregulated across all Antarctic species. Additionally, the constant cold has apparently not relaxed the selective pressures on maintaining HSF1 and HSEs in Antarctic fish. Instead, we found HSF1 experienced intensified selective pressure, with conserved sequence changes in Antarctic species suggesting optimization for non-heat-stress functional roles. HSEs of the HSP70 gene family have largely remained conserved in canonical sequence motifs and copy numbers as in E. maclovinus, showing limited impact of relaxed selective pressure. This study shows that evolution in chronic cold has led to both subtle and distinctive changes in the cellular apparatus for proteostasis and HSR, with functional consequences amenable to experimental evaluation.

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Fig. 1: Profiles of differentially expressed (DE) chaperome genes in gill tissue of Antarctic notothenioids compared to E. maclovinus.
Fig. 2: Gene expression profile of the HSP70 gene family members in Antarctic notothenioids.
Fig. 3: Heat map of chaperome gene expression.
Fig. 4: Sequence alignment of HSF1 from basal E. maclovinus and representative derived Antarctic notothenioids.
Fig. 5: Tests of selective pressure change (RELAX) and occurrence of positive selection (aBSREL) on HSF1 coding sequence.
Fig. 6: Comparison of cis-regulatory regions of HSC71-like, HSPA8, HSPA6, and HSP70-like.
Fig. 7: Comparison of cis-regulatory regions of HSPA4, HSPA5, HSPA13, and HSPA14.

Data availability

Sequencing results for the genomic region upstream of the HSP70 genes have been archived on Genbank through accession numbers MN275890-MN275895. The RT-PCR verified sequence of HSF1 are similarly archived on Genbank with accession numbers MT813024-MT813026.

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Acknowledgements

The authors thank Katherine R. Murphy for her thoughtful comments on the manuscript in its in initial preparation. A special thanks to Jeffery Haas, Director of Information Technology for the Schools of Integrative Biology and Molecular and Cellular Biology at the University of Illinois, Urbana Champaign, who unfailingly helped through a near endless series of software installation requests. This work was supported by the US National Science Foundation Division of Polar Programs grant ANT-1142158 to C-HCC and AL DeVries. LV-C was supported by Fondap-IDEAL 15150003. The funding agencies of this study played no role in the design, collection, analysis, and interpretation of data and writing of this manuscript.

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Bilyk, K.T., Zhuang, X., Vargas-Chacoff, L. et al. Evolution of chaperome gene expression and regulatory elements in the antarctic notothenioid fishes. Heredity (2020). https://doi.org/10.1038/s41437-020-00382-w

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