Acclimatory gene expression of primed clams enhances robustness to elevated <scp><i>p</i>CO<sub>2</sub></scp>

Gurr, Samuel J.; Trigg, Shelly A.; Vadopalas, Brent; Roberts, Susan Jo; Putnam, Hollie M.

doi:10.1111/mec.16644

Cited by 9 publications

(8 citation statements)

References 157 publications

(255 reference statements)

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“…After trimming, any fragment that was less than 20 base pairs were removed (minimum read length). Trimmed reads were aligned to the Roslin Institute’s Crassostrea gigas genome assembly with mitochondrial genes added (Peñaloza et al, 2021) using Hisat2 v.2.2.1 (D. Kim et al, 2019), a splice aware aligner that has previously been used effectively with Tag-Seq data generated from bivalves (Gurr et al, 2022). Aligned reads were assembled against the mRNA genome feature track of the Roslin genome, merged using StringTie v2.2.0, and compiled using prepDE.py (Kovaka et al, 2019).…”

Section: Methodsmentioning

confidence: 99%

Triploid Pacific oysters exhibit stress response dysregulation and elevated mortality following marine heatwaves

George

Cattau

Middleton

et al. 2023

Preprint

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Polyploidy has been shown to negatively impact environmental stress tolerance, resulting in increased susceptibility to extreme climate events such as marine heatwaves (MHWs). In this study, we used the response of the Pacific oysterCrassostrea gigasto MHWs as a model system to identify key ploidy-specific differences in the physiological and transcriptomic response of oysters to environmental stress. In this study, adult diploid (2n) and triploid (3n) oysters were exposed to elevated seawater temperature (single stressor; 30°C), elevated temperature followed by acute desiccation stress (multiple stressor; 30°C + emersion at an aerial temperature of 44°C for 4h), or a control (17°C) within a hatchery setting. Oyster mortality rate was elevated within stress treatments with respect to the control and was significantly higher in triploids than diploids following multiple stress exposure (36.4% vs. 14.8%). Triploids within the multiple stressor treatment exhibited signs of energetic limitation, including metabolic depression, a significant reduction in ctenidium Na+/K+ATPase activity, and the dysregulated expression of key genes associated with heat tolerance, the inhibition of apoptosis, and mitochondrial function. Functional enrichment analysis of ploidy-specific gene sets identified that biological processes associated with metabolism, stress tolerance, and immune function were overrepresented within triploids across stress treatments. Our results demonstrate that triploidy impacts the transcriptional regulation of key metabolic processes that underly the environmental stress response of Pacific oysters, resulting in downstream shifts in physiological tolerance limits that may be detrimental to survival. The impact of chromosome set manipulation on the climate resilience of marine populations has important implications for the adaptability of marine populations and domestic food security within future climate scenarios, especially as triploidy induction becomes an increasingly popular tool to elicit reproductive control across a wide range of marine organisms used within marine aquaculture.

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Section: Methodsmentioning

confidence: 99%

Triploid Pacific oysters exhibit stress response dysregulation and elevated mortality following marine heatwaves

George

Cattau

Middleton

et al. 2023

Preprint

Self Cite

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“…After trimming, any fragment that was less than 20 base pairs were removed (minimum read length). Trimmed reads were aligned to the C. gigas genome assembly with mitochondrial genes added (Peñaloza et al, 2021) using Hisat2 v.2.2.1 (Kim et al, 2019), a splice aware aligner that has previously been used effectively with Tag‐Seq data generated from bivalves (Gurr et al, 2022). Aligned reads were assembled against the mRNA genome feature track, merged using StringTie v2.2.0, and compiled using prepDE.py (Kovaka et al, 2019).…”

Section: Methodsmentioning

confidence: 99%

“…Bioinformatic workflows were performed using bash v. (Gurr et al, 2022). Aligned reads were assembled against the mRNA genome feature track, merged using StringTie v2.2.0, and compiled using prepDE.py (Kovaka et al, 2019).…”

Section: Differential Gene Expression Analysismentioning

confidence: 99%

Triploid Pacific oysters exhibit stress response dysregulation and elevated mortality following heatwaves

George

Cattau

Middleton

et al. 2023

Global Change Biology

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Polyploidy has been suggested to negatively impact environmental stress tolerance, resulting in increased susceptibility to extreme climate events. In this study, we compared the genomic and physiological response of diploid (2n) and triploid (3n) Pacific oysters (Crassostrea gigas) to conditions present during an atmospheric heatwave that impacted the Pacific Northwestern region of the United States in the summer of 2021. Climate stressors were applied either singly (single stressor; elevated seawater temperature, 30°C) or in succession (multiple stressor; elevated seawater temperature followed by aerial emersion at 44°C), replicating conditions present within the intertidal over a tidal cycle during the event. Oyster mortality rate was elevated within stress treatments with respect to the control and was significantly higher in triploids than diploids following multiple stress exposure (36.4% vs. 14.8%). Triploids within the multiple stressor treatment exhibited signs of energetic limitation, including metabolic depression, a significant reduction in ctenidium Na+/K+ ATPase activity, and the dysregulated expression of genes associated with stress response, innate immunity, glucose metabolism, and mitochondrial function. Functional enrichment analysis of ploidy‐specific gene sets identified that biological processes associated with metabolism, stress tolerance, and immune function were overrepresented within triploids across stress treatments. Our results suggest that triploidy impacts the transcriptional regulation of key processes that underly the stress response of Pacific oysters, resulting in downstream shifts in physiological tolerance limits that may increase susceptibility to extreme climate events that present multiple environmental stressors. The impact of chromosome set manipulation on the climate resilience of marine organisms has important implications for domestic food security within future climate scenarios, especially as triploidy induction becomes an increasingly popular tool to elicit reproductive control across a wide range of species used within marine aquaculture.

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“…For example, reef-building corals ( Acropora hyacinthus ) from thermally variable environments show a frontloading of genes involved in thermal stress and exhibit a greater tolerance to bleaching compared to conspecifics from deeper, more thermally stable environments (Barshis et al, 2013). Likewise, Juvenile Pacific geoduck clams ( Panopea Generosa ) that were exposed to elevated p CO 2 during early development showed a frontloading of genes involved in maintain homeostatic functions under acidification and consequently were more tolerant of repeated exposures later in life (Gurr et al, 2022). However, this framework has not yet been widely applied in detecting transcriptional effects associated with cross-generational plasticity.…”

Section: Introductionmentioning

confidence: 99%

Cross-generational plasticity in Atlantic silversides (Menidia menidia) under the combined effects of hypoxia and acidification

Murray,

Mays,

Long

et al. 2024

Preprint

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We investigated the potential for cross-generational plasticity to influence how offspring respond to hypoxia and ocean acidification (hereafter HypOA) in the coastal forage fish Atlantic silverside (Menidia menidia). Mature wild silversides were treated with a control [dissolved oxygen (DO):100% air saturation (a.s.) /pCO2: 650 μatm] or HypOA conditions [DO: 40% a.s. /pCO2: 2300 μatm] for 10 days prior to spawning. Their offspring were reared under both treatments in factorial experimental design. Parental acclimation to HypOA altered several offspring traits, including increased embryo survival under HypOA and an overall reduction in post-hatch growth rate. Offspring from HypOA-treated parents that were reared under control conditions had larger eyes across the developmental period. When compared against the overall control group, larvae directly exposed to HypOA exhibited 2,416 differentially expressed transcripts (DETs). Although most of these DETs were specific to individual parental treatments, the most enriched Gene Ontology terms were conserved across parental treatments, including terms related to neurotransmitter secretion, nervous system development, axon pathfinding, calcium channel activity, proteolysis, and extracellular matrix organization. Larvae from HypOA-treated parents that were reared under control conditions exhibited a shift in constitutive gene expression similar to that seen in larvae directly exposed to HypOA. This highly consistent finding indicates that parental acclimation before fertilization promotes the transcriptional frontloading of genes in offspring that are responsive to direct HypOA exposure. This highly consistent finding indicates that parental acclimation before fertilization promotes the transcriptional frontloading of genes in offspring. This effect may have primed regulatory functions in offspring that sense and respond to low DO and elevatedpCO2conditions. Though, our results suggest that this altered developmental phenotype may have some negative fitness consequences for offspring.

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Acclimatory gene expression of primed clams enhances robustness to elevated pCO₂

Cited by 9 publications

References 157 publications

Triploid Pacific oysters exhibit stress response dysregulation and elevated mortality following marine heatwaves

Triploid Pacific oysters exhibit stress response dysregulation and elevated mortality following marine heatwaves

Triploid Pacific oysters exhibit stress response dysregulation and elevated mortality following heatwaves

Cross-generational plasticity in Atlantic silversides (Menidia menidia) under the combined effects of hypoxia and acidification

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Acclimatory gene expression of primed clams enhances robustness to elevated pCO2

Cited by 9 publications

References 157 publications

Triploid Pacific oysters exhibit stress response dysregulation and elevated mortality following marine heatwaves

Triploid Pacific oysters exhibit stress response dysregulation and elevated mortality following marine heatwaves

Triploid Pacific oysters exhibit stress response dysregulation and elevated mortality following heatwaves

Cross-generational plasticity in Atlantic silversides (Menidia menidia) under the combined effects of hypoxia and acidification

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Acclimatory gene expression of primed clams enhances robustness to elevated pCO₂