The time course of molecular acclimation to seawater in a euryhaline fish

Lucrezia C Bonzi,Alison A Monroe,Robert Lehmann,Michael L Berumen,Celia Schunter,Timothy Ravasi

doi:10.1038/s41598-021-97295-3

Abstract

The Arabian pupfish, Aphanius dispar, is a euryhaline fish inhabiting both inland nearly-freshwater desert ponds and highly saline Red Sea coastal lagoons of the Arabian Peninsula. Desert ponds and coastal lagoons, located respectively upstream and at the mouths of dry riverbeds (“wadies”), have been found to potentially become connected during periods of intense rainfall, which could allow the fish to migrate between these different habitats. Flash floods would therefore flush Arabian pupfish out to sea, requiring a rapid acclimation to a greater than 40 ppt change in salinity. To investigate the molecular pathways of salinity acclimation during such events, a Red Sea coastal lagoon and a desert pond population were sampled, with the latter exposed to a rapid increase in water salinity. Changes in branchial gene expression were investigated via genome-wide transcriptome measurements over time from 6 h to 21 days. The two natural populations displayed basal differences in genes related to ion transport, osmoregulation and immune system functions. These mechanisms were also differentially regulated in seawater transferred fish, revealing their crucial role in long-term adaptation. Other processes were only transiently activated shortly after the salinity exposure, including cellular stress response mechanisms, such as molecular chaperone synthesis and apoptosis. Tissue remodelling processes were also identified as transient, but took place later in the timeline, suggesting their importance to long-term acclimation as they likely equip the fish with lasting adaptations to their new environment. The alterations in branchial functional pathways displayed by Arabian pupfish in response to salinity increases are diverse. These reveal a large toolkit of molecular processes important for adaptation to hyperosmolarity that allow for successful colonization to a wide variety of different habitats.

Highlights

Markers for an evolutionarily conserved cellular stress response (CSR) triggered by macromolecular damage have been identified in gene expression and transcriptomic studies in fish exposed to changes in salinity[25,26,27]
In October 2016, the osmotic challenge experiment started: fish from the desert pond population were directly transferred to seawater, in order to mimic the change in salinity they might experience during potential colonization of coastal lagoons of the Red Sea (Fig. 2)
The first de novo transcriptome assembly for Aphanius dispar was created from a total of 1.38 billion raw reads with an average of 24.5 million reads per sample after trimming and error correction steps

Summary

Introduction

While salinity changes have been observed to influence Arabian pupfish osmotic pressure, body ion content, and gill permeability[46,47], no differences in performance indicators, such as resting metabolic rate, swimming speed and activity level, were caused by up to 70 ppt increases in water s alinity[48]. For these reasons, the Arabian pupfish represents an excellent system to investigate the mechanisms underlying the plasticity of euryhaline fish gills during salt stress events, and the processes that allow them to acclimate long-term and colonize novel habitats.

Methods

Results

Conclusion