Proteomic Responses to Ocean Acidification in the Brain of Juvenile Coral Reef Fish

Hin Hung Tsang,Megan J Welch,Timothy Ravasi,Celia Schunter,Philip L Munday

doi:10.3389/fmars.2020.00605

Abstract

Elevated CO2 levels predicted to occur by the end of the century can affect the physiology and behaviour of marine fishes. For one important survival mechanism, the response to chemical alarm cues from conspecifics, substantial among-individual variation in the extent of behavioural impairment when exposed to elevated CO2 has been observed in previous studies. Whole brain transcriptomic data has further emphasized the importance of parental phenotypic variation in the response of juvenile fish to elevated CO2. In this study, we investigate the genome-wide proteomic responses of this variation in the brain of 5-week old spiny damselfish, Acanthochromis polyacanthus. We compared the accumulation of proteins in the brains of juvenile A. polyacanthus from two different parental behavioural phenotypes (sensitive and tolerant) that had been experimentally exposed to short-term, long-term and inter-generational elevated CO2. Our results show differential accumulation of key proteins related to stress response and epigenetic markers with elevated CO2 exposure. Proteins related to neurological development and glucose metabolism were also differentially accumulated particularly in the long-term developmental treatment, which might be critical for juvenile development. By contrast, exposure to elevated CO2 in the parental generation resulted in only three differentially accumulated proteins in the offspring, revealing potential for inter-generational acclimation. Lastly, we found a distinct proteomic pattern in juveniles due to the behavioural sensitivity of parents to elevated CO2, even though the behaviour of the juvenile fish was impaired regardless of parental phenotype. Our data shows that developing juveniles are affected in their brain protein accumulation by elevated CO2, but the effect varies with the length of exposure as well as due to variation of parental phenotypes in the population.

Highlights

Rising CO2 levels in the ocean are anticipated to affect the physiology and behavior of marine organisms, with possible impacts on the structure and function of marine ecosystems (Wittmann and Pörtner, 2013; Cattano et al, 2018; Pörtner et al, 2019)
Offspring clutches from each breeding pair were placed into different experimental conditions resulting in a total of four treatment groups for each parental behavioral phenotype (T and S) (Figure 1): (1) Parents and offspring were kept at a CO2 level of 414 ± 46 μatm (Control treatment); (2) Parents and offspring were kept at control condition, and offspring were exposed to elevated CO2 (754 ± 92 μatm) for five days before dissection (Acute treatment); (3) Parents were kept at control condition and offspring were exposed to elevated CO2 immediately after hatching for their entire developmental period (Developmental treatment); and (4) both parents as well as offspring were exposed to elevated CO2 for the entire duration of the study (Inter-generational treatment)
Three down-regulated proteins are involved in histone modifications. This includes the non-histone chromosomal protein HMG-14A-like isoform X2 (HMGN2) which is involved in phosphorylation inhibition of nucleosomal histones H3 and H2A; chromobox protein homolog 1-like (CBX1) which is associated with histone binding; and prothymosin alpha-B-like (PTMAB) which plays a role in histone methylation

Summary

Introduction

Rising CO2 levels in the ocean are anticipated to affect the physiology and behavior of marine organisms, with possible impacts on the structure and function of marine ecosystems (Wittmann and Pörtner, 2013; Cattano et al, 2018; Pörtner et al, 2019). Exposure to elevated CO2 impairs the natural avoidance behavior of chemical alarm cues (CAC) in some fishes (Ferrari et al, 2011; Chivers et al, 2014; Welch et al, 2014; Ou et al, 2015; Welch and Munday, 2017; Laubenstein et al, 2019). When exposed to elevated CO2, some fish fail to exhibit behaviors that reduce their risk of predation This impaired behavior is hypothesized to be caused by the self-amplifying alteration in the chloride-bicarbonate current in the GABAA receptor in the brain, following acid-base regulation in reaction to elevated environmental CO2 (Nilsson et al, 2012; Chivers et al, 2014; Heuer et al, 2016; Schunter et al, 2019)

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