Abstract

Elevated carbon dioxide levels in ocean waters, an anthropogenic stressor, can alter the chemical equilibrium of seawater through a process called ocean acidification (OA). The resultant reduction of pH can be detrimental during the early developmental stages of the commercially important edible Pacific oyster Crassostrea gigas; the ability of larvae to join a population is likely to be compromised by declining ocean pH. Given this threat, it is important to study the molecular mechanisms that these organisms use to overcome OA stress at the gene expression level. Here, we performed transcriptome profiling in oyster larvae following exposure to ambient (8.1) and reduced (7.4) pH during the pre-settlement growth period (i.e., 18 d post fertilization) using RNA-seq with Illumina sequencing technology. In total, 1,808 differentially expressed genes (DEGs) were identified, 1,410 of which were matched by BLAST against the Swiss-Prot database. Gene ontology classification showed that most of these DEGs were related to ribosomal, calcium ion binding, cell adhesion and apoptotic processes. Pathway enrichment analysis revealed that low pH (7.4) enhanced energy production and organelle biogenesis but prominently suppressed several immune response pathways. Moreover, activation of the MAPK signaling pathway was observed along with inhibition of the Wnt, VEGF, and ErbB pathways, highlighting the fact that the initiation of stress responses is given priority over larval development or shell growth when the larvae cope with low pH. In conclusion, our study demonstrated a unique gene expression profiling approach in studying oyster larval responses to OA, which not only provides comprehensive insights into the mechanisms underlying oyster tolerance to CO2-driven decreases in ocean pH but also supplies a valuable genomic resource for further studies in this species.

Highlights

  • Carbon dioxide levels in the atmosphere and oceans have been increasing at unprecedented rates, since the beginning of the industrial revolution (Falkowski et al, 2000)

  • Each larval culture tanks were mixed with air to obtain the ambient CO2 levels for the control and CO2 pre-mixed air for the low pH (7.4), which was within environmentally relevant range predicted for the Pacific oysters in the fluctuating coastal marine systems and reflects the futuristic atmospheric CO2 emission scenarios (Zeebe, 2008), for the year 2300 as predicted by the Intergovernmental Panel on Climate Change IPCC (Caldeira and Wickett, 2005)

  • After low quality reads removal and adaptor trimming, a total of 15,081,854 effective reads were produced from the control group, while 13,455,384 effective reads were obtained from the treated group, whose effective reads ratio were 90.8 and 90.9%, respectively

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Summary

Introduction

Carbon dioxide levels in the atmosphere and oceans have been increasing at unprecedented rates, since the beginning of the industrial revolution (Falkowski et al, 2000). Though some marine organisms are resilient and can acclimate to changes (Kroeker et al, 2010; Munday et al, 2011; McCulloch et al, 2012), most shell-forming invertebrates, such as sea urchins, corals and mollusks (Parker et al, 2013), find it difficult to calcify in the presence of elevated CO2 levels and reduced pH in seawater (Gazeau et al, 2007, 2010, 2013; Kurihara et al, 2007; Miller et al, 2009; Talmage and Gobler, 2009; Todgham and Hofmann, 2009; Sheppard Brennand et al, 2010; Parker et al, 2012; Doney et al, 2020). Ocean acidification impacts homeostasis and behavioral response in marine fishes (Esbaugh et al, 2012; Jutfelt et al, 2013; Hamilton et al, 2014) and leads to metabolic suppression to conserve energy for survival and immune responses in many marine organisms (Bibby et al, 2007, 2008; Lannig et al, 2010; Hernroth et al, 2011)

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