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Research article
Juliet M. Wong
Florida International University College of Arts Sciences and Education
Corresponding Author
ORCiD: https://orcid.org/0000-0001-9279-3113
License:
This work is licensed under a CC BY 4.0 License. Read Full License
Background: The red sea urchin Mesocentrotus franciscanus is an ecologically important kelp forest herbivore and an economically valuable wild fishery species. To examine how M. franciscanus responds to its environment on a molecular level, differences in gene expression patterns were observed in embryos raised under combinations of two temperatures (13 °C or 17 °C) and two pCO2 levels (475 matm or 1050 matm). These combinations mimic various present-day conditions measured during and between upwelling events in the highly dynamic California Current System with the exception of the 17 °C and 1050 matm combination, which does not currently occur. However, as ocean warming and acidification continues, warmer temperatures and higher pCO2 conditions are expected to increase in frequency and to occur simultaneously. The transcriptomic responses of the embryos were assessed at two developmental stages (gastrula and prism) in light of previously described plasticity in body size and thermotolerance under these temperature and pCO2 treatments.
Results: Although transcriptomic patterns primarily varied by developmental stage, there were pronounced differences in gene expression as a result of the treatment conditions. Temperature and pCO2 treatments led to the differential expression of genes related to the cellular stress response, transmembrane transport, metabolic processes, and the regulation of gene expression. At each developmental stage, temperature contributed significantly to the observed variance in gene expression, which was also correlated to the phenotypic attributes of the embryos. On the other hand, the transcriptomic response to pCO2 was relatively muted, particularly at the prism stage.
Conclusions: M. franciscanus exhibited transcriptomic plasticity under different temperatures, indicating their capacity for a molecular-level response that may facilitate red sea urchins facing ocean warming as climate change continues. In contrast, the lack of a robust transcriptomic response, in combination with observations of decreased body size, under elevated pCO2 levels suggest that this species may be negatively affected by ocean acidification. High present-day pCO2 conditions that occur due to coastal upwelling may already be influencing populations of M. franciscanus.
Keywords
red sea urchin, Mesocentrotus franciscanus, RNA-seq, transcriptomics, early development, climate change, warming, ocean acidification
Figure 1
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Figure 3
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Figure 5
This is a list of supplementary files associated with this preprint. Click to download.
- Additionalfile1Samplesummarystats.xls
Additional file 1: Summary RNA-seq statistics of all samples.
- Additionalfile2Allstagesanalyses.pdf
Additional file 2: Differential expression analysis of all samples independently of stage (i.e., gastrula and prism stages not analyzed separately). a Principal components that contributed >80% of the explained variation, PC1-PC7 (columns), were correlated (1 to -1; *p < 0.05, **p < 0.01, and ***p < 0.001) to metadata variables (rows) of the experiment treatments (i.e., temperature and pCO2). GO analysis determined significant enrichment within molecular function (MF), biological process (BP), and cellular component (CC) GO categories of genes that contributed variance to b PC2, c PC3, and d PC4. Font sizes of the category names indicate the level of statistical significance as noted in the legend. The fraction preceding each category name is the number of genes with loading absolute values >0.001 relative to the total number of genes belonging to the category. Genes were differentially expressed (displayed in color) due to e the temperature treatment and f the pCO2 treatment. GO analysis determined significant enrichment within GO categories of genes up-regulated (red text) and down-regulated (blue text) due to g the temperature treatment and h the pCO2 treatment. The fraction preceding each category name is the number of genes with moderated t-statistic absolute values >1 relative to the total number of genes belonging to the category.
- Additionalfile3Genelists.xls
Additional file 3: Lists of genes within each principal component that is significantly correlated to a metadata variable, and lists of genes that are significantly differentially expressed due to temperature or pCO2 experiment treatments.
- Additionalfile4PCGOresults.pdf
Additional file 4: GO results of principal component (PC) loadings. The GO analysis determined significant enrichment within molecular function (MF), biological process (BP), and cellular component (CC) GO categories of genes that contributed variance to a PC1 and b PC2 at the gastrula stage, as well as c PC1 and d PC2 at the prism stage. Font sizes of the category names indicate the level of statistical significance as noted in the legend. The fraction preceding each category name is the number of genes with loading absolute values >0.001 relative to the total number of genes belonging to the category.
- Additionalfile5CellularComponentDEGOresults.pdf
Additional file 5: Additional GO results of differential expression (DE) analyses. The GO analysis determined significant enrichment within the cellular component (CC) category of genes up-regulated (red text) and down-regulated (blue text) due to a the temperature treatment in gastrula embryos, b the pCO2 treatment in gastrula embryos, c the temperature treatment in prism embryos, and d the pCO2 treatment in prism embryos. Font sizes of the category names indicate the level of statistical significance as noted in the legend. The fraction preceding each category name is the number of genes with moderated t-statistic absolute values >1 relative to the total number of genes belonging to the category.
- Additionalfile6PCAgeneticdiversity.pdf
Additional file 6: Principal component analysis (PCA) plot of all samples as well as samples from a previous study that examined gene expression patterns during the early development of M. franciscanus [48].
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View the published article at BMC Genomics.
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See the published version of this preprint at BMC Genomics.
This is a preprint, a preliminary version of a manuscript that has not completed peer review at a journal. Research Square does not conduct peer review prior to posting preprints. The posting of a preprint on this server should not be interpreted as an endorsement of its validity or suitability for dissemination as established information or for guiding clinical practice.
Learn more about In Review
Research article
Juliet M. Wong
Florida International University College of Arts Sciences and Education
Corresponding Author
ORCiD: https://orcid.org/0000-0001-9279-3113
Badges
Prescreen
This manuscript passed our Prescreen assessment
Complete author information
Appropriate declaration statements
Potential risks to human health
Prescreen
Peer Review Timeline
CURRENT STATUS: Published
View the published article at BMC Genomics.
Version 3
Posted 22 Dec, 2020
No community comments so far
Editorial decision: Accept
On 11 Dec, 2020
Editor assigned
On 08 Dec, 2020
Submission checks complete
On 08 Dec, 2020
Editor invited
On 08 Dec, 2020
No comments provided
Review #1 received
Received 13 Nov, 2020
Reviewer #2 agreed
On 10 Nov, 2020
Reviewers invited
Invitations sent on 10 Nov, 2020
Reviewer #1 agreed
On 10 Nov, 2020
Editor assigned
On 31 Oct, 2020
Submission checks complete
On 31 Oct, 2020
Editor invited
On 31 Oct, 2020
No comments provided
Editorial decision: Major revision
On 27 Jul, 2020
Review #2 received
Received 26 Jul, 2020
Reviewer #2 agreed
On 13 Jul, 2020
Review #1 received
Received 12 Jul, 2020
Reviewers invited
Invitations sent on 07 Jul, 2020
Reviewer #1 agreed
On 07 Jul, 2020
Editor assigned
On 02 Jul, 2020
Submission checks complete
On 29 Jun, 2020
Editor invited
On 29 Jun, 2020
First submitted
On 22 Jun, 2020
Metrics
Comments: 0
PDF Downloads: ...
HTML Views: ...
Subject Areas
Epigenetics & Genomics
License:
This work is licensed under a CC BY 4.0 License. Read Full License
View the published article at BMC Genomics.
Background: The red sea urchin Mesocentrotus franciscanus is an ecologically important kelp forest herbivore and an economically valuable wild fishery species. To examine how M. franciscanus responds to its environment on a molecular level, differences in gene expression patterns were observed in embryos raised under combinations of two temperatures (13 °C or 17 °C) and two pCO2 levels (475 matm or 1050 matm). These combinations mimic various present-day conditions measured during and between upwelling events in the highly dynamic California Current System with the exception of the 17 °C and 1050 matm combination, which does not currently occur. However, as ocean warming and acidification continues, warmer temperatures and higher pCO2 conditions are expected to increase in frequency and to occur simultaneously. The transcriptomic responses of the embryos were assessed at two developmental stages (gastrula and prism) in light of previously described plasticity in body size and thermotolerance under these temperature and pCO2 treatments.
Results: Although transcriptomic patterns primarily varied by developmental stage, there were pronounced differences in gene expression as a result of the treatment conditions. Temperature and pCO2 treatments led to the differential expression of genes related to the cellular stress response, transmembrane transport, metabolic processes, and the regulation of gene expression. At each developmental stage, temperature contributed significantly to the observed variance in gene expression, which was also correlated to the phenotypic attributes of the embryos. On the other hand, the transcriptomic response to pCO2 was relatively muted, particularly at the prism stage.
Conclusions: M. franciscanus exhibited transcriptomic plasticity under different temperatures, indicating their capacity for a molecular-level response that may facilitate red sea urchins facing ocean warming as climate change continues. In contrast, the lack of a robust transcriptomic response, in combination with observations of decreased body size, under elevated pCO2 levels suggest that this species may be negatively affected by ocean acidification. High present-day pCO2 conditions that occur due to coastal upwelling may already be influencing populations of M. franciscanus.
Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
This is a list of supplementary files associated with this preprint. Click to download.
- Additionalfile1Samplesummarystats.xls
Additional file 1: Summary RNA-seq statistics of all samples.
- Additionalfile2Allstagesanalyses.pdf
Additional file 2: Differential expression analysis of all samples independently of stage (i.e., gastrula and prism stages not analyzed separately). a Principal components that contributed >80% of the explained variation, PC1-PC7 (columns), were correlated (1 to -1; *p < 0.05, **p < 0.01, and ***p < 0.001) to metadata variables (rows) of the experiment treatments (i.e., temperature and pCO2). GO analysis determined significant enrichment within molecular function (MF), biological process (BP), and cellular component (CC) GO categories of genes that contributed variance to b PC2, c PC3, and d PC4. Font sizes of the category names indicate the level of statistical significance as noted in the legend. The fraction preceding each category name is the number of genes with loading absolute values >0.001 relative to the total number of genes belonging to the category. Genes were differentially expressed (displayed in color) due to e the temperature treatment and f the pCO2 treatment. GO analysis determined significant enrichment within GO categories of genes up-regulated (red text) and down-regulated (blue text) due to g the temperature treatment and h the pCO2 treatment. The fraction preceding each category name is the number of genes with moderated t-statistic absolute values >1 relative to the total number of genes belonging to the category.
- Additionalfile3Genelists.xls
Additional file 3: Lists of genes within each principal component that is significantly correlated to a metadata variable, and lists of genes that are significantly differentially expressed due to temperature or pCO2 experiment treatments.
- Additionalfile4PCGOresults.pdf
Additional file 4: GO results of principal component (PC) loadings. The GO analysis determined significant enrichment within molecular function (MF), biological process (BP), and cellular component (CC) GO categories of genes that contributed variance to a PC1 and b PC2 at the gastrula stage, as well as c PC1 and d PC2 at the prism stage. Font sizes of the category names indicate the level of statistical significance as noted in the legend. The fraction preceding each category name is the number of genes with loading absolute values >0.001 relative to the total number of genes belonging to the category.
- Additionalfile5CellularComponentDEGOresults.pdf
Additional file 5: Additional GO results of differential expression (DE) analyses. The GO analysis determined significant enrichment within the cellular component (CC) category of genes up-regulated (red text) and down-regulated (blue text) due to a the temperature treatment in gastrula embryos, b the pCO2 treatment in gastrula embryos, c the temperature treatment in prism embryos, and d the pCO2 treatment in prism embryos. Font sizes of the category names indicate the level of statistical significance as noted in the legend. The fraction preceding each category name is the number of genes with moderated t-statistic absolute values >1 relative to the total number of genes belonging to the category.
- Additionalfile6PCAgeneticdiversity.pdf
Additional file 6: Principal component analysis (PCA) plot of all samples as well as samples from a previous study that examined gene expression patterns during the early development of M. franciscanus [48].
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