The heat shock protein (Hsp) superfamily has received accumulated attention because it is ubiquitous and conserved in almost all living organisms and is involved in a wide spectrum of cellular responses against diverse environmental stresses. However, our knowledge about the Hsp co-chaperon network is still limited in non-model organisms. In this study, we provided the systematic analysis of 95 Hsp genes (LmHsps) in the genome of spotted sea bass (Lateolabrax maculatus), an important aquaculture species in China that can widely adapt to diverse salinities from fresh to sea water, and moderately adapt to high alkaline water. Through in silico analysis using transcriptome and genome database, we determined the expression profiles of LmHsps in response to salinity change and alkalinity stress in L. maculatus gills. The results revealed that LmHsps were sensitive in response to alkalinity stress, and the LmHsp40-70-90 members were more actively regulated than other LmHsps and may also be coordinately interacted as co-chaperons. This was in accordance with the fact that members of LmHsp40, LmHsp70, and LmHsp90 evolved more rapidly in L. maculatus than other teleost lineages with positively selected sites detected in their functional domains. Our results revealed the diverse and cooperated regulation of LmHsps under alkaline stress, which may have arisen through the functional divergence and adaptive recruitment of the Hsp40-70-90 co-chaperons and will provide vital insights for the development of L. maculatus cultivation in alkaline water.

Salinity and alkalinity are among the important factors affecting the distribution, survival, growth and physiology of aquatic animals. Chinese sea bass (Lateolabrax maculatus) is an important aquaculture fish species in China that can widely adapt to diverse salinities from freshwater (FW) to seawater (SW) but moderately adapt to highly alkaline water (AW). In this study, juvenile L. maculatus were exposed to salinity change (SW to FW) and alkalinity stress (FW to AW). Coordinated transcriptomic responses in L. maculatus gills were investigated and based on the weighted gene co-expression network analysis (WGCNA), 8 and 11 stress-responsive modules (SRMs) were identified for salinity change and alkalinity stress, respectively, which revealed a cascade of cellular responses to oxidative and osmotic stress in L. maculatus gills. Specifically, four upregulated SRMs were enriched with induced differentially expressed genes (DEGs) for alkalinity stress, mainly corresponding to the functions of “extracellular matrix” and “anatomical structure”, indicating a strong cellular response to alkaline water. Both “antioxidative activity” and “immune response” functions were enriched in the downregulated alkaline SRMs, which comprised inhibited alkaline specific DEGs, revealing the severely disrupted immune and antioxidative functions under alkalinity stress. These alkaline-specific responses were not revealed in the salinity change groups with only moderately inhibited osmoregulation and induced antioxidative response in L. maculatus gills. Therefore, the results revealed the diverse and correlated regulation of the cellular process and stress response in saline-alkaline water, which may have arisen through the functional divergence and adaptive recruitment of the co-expression genes and will provide vital insights for the development of L. maculatus cultivation in alkaline water.

As lower vertebrates, teleost species could be affected by dynamic aquatic environments and may respond to environmental changes through the hypothalamus–pituitary–gonad (HPG) axis to ensure their normal growth and sexual development. Chinese sea bass (Lateolabrax maculatus), euryhaline marine teleosts, have an extraordinary ability to deal with a wide range of salinity changes, whereas the salinity decrease during their sex-maturation season may interfere with the HPG axis and affect their steroid hormone metabolism, resulting in abnormal reproductive functioning. To this end, in this study, 40 HPG axis genes in the L. maculatus genome were systematically characterized and their copy numbers, phylogenies, gene structures, and expression patterns were investigated, revealing the conservation of the HPG axis among teleost lineages. In addition, freshwater acclimation was carried out with maturing male L. maculatus, and their serum cortisol and 11-ketotestosterone (11-KT) levels were both increased significantly after the salinity change, while their testes were found to be partially degraded. After salinity reduction, the expression of genes involved in cortisol and 11-KT synthesis (cyp17a, hsd3b1, cyp21a, cyp11c, hsd11b2, and hsd17b3) showed generally upregulated expression in the head kidneys and testes, respectively. Moreover, cyp11c and hsd11b2 were involved in the synthesis and metabolism of both cortisol and 11-KT, and after salinity change their putative interaction may contribute to steroid hormone homeostasis. Our results proved the effects of salinity change on the HPG axis and steroidogenic pathway in L. maculatus and revealed the gene interactions involved in the regulation of steroid hormone levels. The coordinated interaction of steroidogenic genes provides comprehensive insights into steroidogenic pathway regulation, as well as sexual development, in teleost species.