Ocean acidification induces distinct transcriptomic responses across life history stages of the sea urchin <i>Heliocidaris erythrogramma</i>

Devens, Hannah R.; Davidson, Phillip L.; Deaker, Dione J.; Smith, Kathryn E.; Wray, Gregory A.; Byrne, Maria

doi:10.1111/mec.15664

Cited by 15 publications

(17 citation statements)

References 135 publications

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“…For example, gene expression studies of early developmental stages in coral identified a number of genes affected by OA (Moya et al, 2012;Rivest et al, 2018). Studies on sea urchins also revealed the overall molecular responses of sea urchin larvae exposed to CO 2 (Todgham and Hofmann, 2009;Devens et al, 2020). OA is known to interfere with several key physiological process in marine organisms, transcriptomics has proven to be effective method to elucidate the molecular level response and when coupled with phenotypic data confers a better understanding of whole organismal response (Davies et al, 2016;Melzner et al, 2020;Strader et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Ocean Acidification Triggers Cell Signaling, Suppress Immune and Calcification in the Pacific Oyster Larvae

Dineshram

Xiao

et al. 2021

Front. Mar. Sci.

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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.

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Section: Introductionmentioning

confidence: 99%

Ocean Acidification Triggers Cell Signaling, Suppress Immune and Calcification in the Pacific Oyster Larvae

Dineshram

Xiao

et al. 2021

Front. Mar. Sci.

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“…However, this reduction could potentially be an issue for differential gene expression studies where gene variants (i.e., isoforms) are removed from the samples via the reduction of transcripts. Nevertheless, performing a reduction step before a gene expression analysis is a common practice (DeLeo & Bracken‐Grissom, 2020; Devens et al, 2020; Guo et al, 2017; Kashyap et al, 2020; Perez et al, 2021). Therefore, the nonredundant transcriptome generated by TransPi could be utilized for gene expression studies (Deshpande et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

TransPi—a comprehensive TRanscriptome ANalysiS PIpeline for de novo transcriptome assembly

Rivera‐Vicéns

Garcia-Escudero

Conci

et al. 2022

Molecular Ecology Resources

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The use of RNA sequencing (RNA‐Seq) data and the generation of de novo transcriptome assemblies have been pivotal for studies in ecology and evolution. This is especially true for nonmodel organisms, where no genome information is available. In such organisms, studies of differential gene expression, DNA enrichment bait design and phylogenetics can all be accomplished with de novo transcriptome assemblies. Multiple tools are available for transcriptome assembly, but no single tool can provide the best assembly for all data sets. Therefore, a multi‐assembler approach, followed by a reduction step, is often sought to generate an improved representation of the assembly. To reduce errors in these complex analyses while at the same time attaining reproducibility and scalability, automated workflows have been essential in the analysis of RNA‐Seq data. However, most of these tools are designed for species where genome data are used as reference for the assembly process, limiting their use in nonmodel organisms. We present TransPi, a comprehensive pipeline for de novo transcriptome assembly, with minimum user input but without losing the ability of a thorough analysis. A combination of different model organisms, k‐mer sets, read lengths and read quantities was used for assessing the tool. Furthermore, a total of 49 nonmodel organisms, spanning different phyla, were also analysed. Compared to approaches using single assemblers only, TransPi produces higher BUSCO completeness percentages, and a concurrent significant reduction in duplication rates. TransPi is easy to configure and can be deployed seamlessly using Conda, Docker and Singularity.

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“…However, thousands of genes were exclusively responsive in a single life stage with only ∼20% DEGs consistently responding to salinity stress in this earlier study, reinforcing a largely stage-specific stress response (Aguilar et al, 2019b). Although sparse, there is also evidence for development modulating the stress response in plants (Garg et al, 2016; Liu et al, 2021) and other invertebrates (Devens et al, 2020; Schneweis et al, 2017), suggesting complex life cycles can decouple the molecular response to stress. The lack of consistency in the stress response across life stages has major implications for the evolutionary trajectory of these corals.…”

Section: Discussionmentioning

confidence: 99%

“…In a meta-analysis of expression response to stress in Acroporid corals, Dixon et al (2020) found life stage to be the major factor differentiating transcriptional variation, but most studies were limited to a single life stage, precluding any formal investigation of life-stage differences. However, developmental stage has been found to modulate the transcriptional response to stress in other systems, including water and salinity stress in plants (Garg et al, 2016; Liu et al, 2021), viral infection in insects (Schneweis et al, 2017), and pH stress in sea urchins (Devens et al, 2020). It is therefore necessary to explore how functional variation is regulated across different developmental stages to inform understanding of coral adaptive capacity.…”

Section: Introductionmentioning

confidence: 99%

Divergent transcriptional response to thermal stress among life stages could constrain coral adaptation to climate change

Ruggeri

Zhang

Aglyamova

et al. 2022

Preprint

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The ability for adaptation to keep pace with environmental change largely depends on how efficiently selection can act on heritable genetic variation. Complex life cycles may either promote or constrain adaptation depending on the integration or independence of fitness-related traits over development. Reef-building corals exhibit complex life cycles and are sensitive to increasing temperatures, highlighting the need to understand the heritable potential of the thermal stress response and how it is regulated over development. Here we used tag-based RNA-seq to profile global gene expression in inshore and offshore P. astreoides adults and their offspring recruits in response to a 16-day heat stress, and larvae from separate families in response to a 4-day heat stress, to test whether gene expression patterns differentiating adult populations, and potentially underlying differences in thermal tolerance, persist in thermally naive life stages. Host developmental stage had a major effect on both host and symbiont expression, despite symbionts being directly inherited from parent colonies, and modulated the response to thermal stress, suggesting the holobiont response to selection varies across life stages. Populations also exhibited origin-specific treatment responses, but the magnitude of the response differed among populations and life stages. Inshore parents and their juvenile offspring exhibited a more robust response to heat stress compared to offshore-origin corals, indicating expression plasticity may be heritable. However, larval populations exhibited the opposite response, possibly due to stage-specific differences or exposure duration. Overall, this study shows that putatively adaptive regulatory variation can be heritable, but the identity of thermally responsive genes are stage-specific, which will have major implications for predicting the evolutionary response of corals in a changing environment.

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Ocean acidification induces distinct transcriptomic responses across life history stages of the sea urchin Heliocidaris erythrogramma

Cited by 15 publications

References 135 publications

Ocean Acidification Triggers Cell Signaling, Suppress Immune and Calcification in the Pacific Oyster Larvae

Ocean Acidification Triggers Cell Signaling, Suppress Immune and Calcification in the Pacific Oyster Larvae

TransPi—a comprehensive TRanscriptome ANalysiS PIpeline for de novo transcriptome assembly

Divergent transcriptional response to thermal stress among life stages could constrain coral adaptation to climate change

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