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Meta-analysis of studies using suppression subtractive hybridization and microarrays to investigate the effects of environmental stress on gene transcription in oysters.

Anderson K, Taylor DA, Thompson EL, Melwani AR, Nair SV, Raftos DA - PLoS ONE (2015)

Bottom Line: To address this shortfall, we conducted a meta-analysis of 14 studies that investigated the effects of different environmental stressors on gene expression in oysters.We found that the expression of over 400 genes in a range of oyster species changed significantly after exposure to environmental stress.In light of these findings, we put forward a consensus model of sub-cellular stress responses in oysters.

View Article: PubMed Central - PubMed

Affiliation: Sydney Institute of Marine Science, Chowder Bay, NSW, Australia; Department of Biological Sciences, Macquarie University, North Ryde, NSW, Australia.

ABSTRACT
Many microarray and suppression subtractive hybridization (SSH) studies have analyzed the effects of environmental stress on gene transcription in marine species. However, there have been no unifying analyses of these data to identify common stress response pathways. To address this shortfall, we conducted a meta-analysis of 14 studies that investigated the effects of different environmental stressors on gene expression in oysters. The stressors tested included chemical contamination, hypoxia and infection, as well as extremes of temperature, pH and turbidity. We found that the expression of over 400 genes in a range of oyster species changed significantly after exposure to environmental stress. A repeating pattern was evident in these transcriptional responses, regardless of the type of stress applied. Many of the genes that responded to environmental stress encoded proteins involved in translation and protein processing (including molecular chaperones), the mitochondrial electron transport chain, anti-oxidant activity and the cytoskeleton. In light of these findings, we put forward a consensus model of sub-cellular stress responses in oysters.

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A consensus model of intracellular responses to stress in oysters based on the genes and/or biological processes that were found in our analysis to be differentially regulated in response to environmental stress.In this model, adaptive intracellular responses to stress lead to increased energy production (ATP) via the mitochondrial electron transport chain. Reactive oxygen species (ROS) are produced as by-products of ATP synthesis. Unless controlled by molecular chaperones (HSPs) and the anti-oxidant system, excessive ROS can disrupt the actin cytoskeleton and mitochondrial membranes leading to apoptotic cell death.
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pone.0118839.g007: A consensus model of intracellular responses to stress in oysters based on the genes and/or biological processes that were found in our analysis to be differentially regulated in response to environmental stress.In this model, adaptive intracellular responses to stress lead to increased energy production (ATP) via the mitochondrial electron transport chain. Reactive oxygen species (ROS) are produced as by-products of ATP synthesis. Unless controlled by molecular chaperones (HSPs) and the anti-oxidant system, excessive ROS can disrupt the actin cytoskeleton and mitochondrial membranes leading to apoptotic cell death.

Mentions: This meta-analysis has compiled data from 14 different transcriptomic studies of oysters exposed to a range of environmental conditions. It has shown that a number of key sub-cellular systems are consistently involved in transcriptional responses to a broad range of environmental stresses. The data support a consensus model that describes a generic intracellular stress response in oysters (Fig. 7). Elements of this model, as it pertains to oysters and other organisms, have been discussed in detail by other authors [30–31]. The model highlights the importance of the mitochondrial electron transport chain, antioxidant enzymes, molecular chaperones and cytoskeletal proteins. Our meta-analysis has shown that the mitochondrial electron transport chain is the primary cellular system impacted by environmental stress and so it is central to the consensus model. Even though enhanced energy production in the mitochondria may be beneficial in terms of powering adaptive cellular processes, it is also known to elevate the production of cytotoxic reactive oxygen species (ROS), with consequent impacts on mitochondrial and cytoskeletal integrity. The failure of anti-oxidant enzymes such as SOD and molecular chaperones to limit damage caused by ROS is likely to result in cellular dysfunction and ultimately apoptotic cell death. All of these effects have been demonstrated in numerous studies of cellular function in oysters responding to stress [32–49]. Modulation of the mitochondrial electron transport chain and its downstream consequences, as depicted in this consensus model, may explain many of the impacts that environmental stress exerts at levels of biological organization from cells to ecosystems [32].


Meta-analysis of studies using suppression subtractive hybridization and microarrays to investigate the effects of environmental stress on gene transcription in oysters.

Anderson K, Taylor DA, Thompson EL, Melwani AR, Nair SV, Raftos DA - PLoS ONE (2015)

A consensus model of intracellular responses to stress in oysters based on the genes and/or biological processes that were found in our analysis to be differentially regulated in response to environmental stress.In this model, adaptive intracellular responses to stress lead to increased energy production (ATP) via the mitochondrial electron transport chain. Reactive oxygen species (ROS) are produced as by-products of ATP synthesis. Unless controlled by molecular chaperones (HSPs) and the anti-oxidant system, excessive ROS can disrupt the actin cytoskeleton and mitochondrial membranes leading to apoptotic cell death.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4358831&req=5

pone.0118839.g007: A consensus model of intracellular responses to stress in oysters based on the genes and/or biological processes that were found in our analysis to be differentially regulated in response to environmental stress.In this model, adaptive intracellular responses to stress lead to increased energy production (ATP) via the mitochondrial electron transport chain. Reactive oxygen species (ROS) are produced as by-products of ATP synthesis. Unless controlled by molecular chaperones (HSPs) and the anti-oxidant system, excessive ROS can disrupt the actin cytoskeleton and mitochondrial membranes leading to apoptotic cell death.
Mentions: This meta-analysis has compiled data from 14 different transcriptomic studies of oysters exposed to a range of environmental conditions. It has shown that a number of key sub-cellular systems are consistently involved in transcriptional responses to a broad range of environmental stresses. The data support a consensus model that describes a generic intracellular stress response in oysters (Fig. 7). Elements of this model, as it pertains to oysters and other organisms, have been discussed in detail by other authors [30–31]. The model highlights the importance of the mitochondrial electron transport chain, antioxidant enzymes, molecular chaperones and cytoskeletal proteins. Our meta-analysis has shown that the mitochondrial electron transport chain is the primary cellular system impacted by environmental stress and so it is central to the consensus model. Even though enhanced energy production in the mitochondria may be beneficial in terms of powering adaptive cellular processes, it is also known to elevate the production of cytotoxic reactive oxygen species (ROS), with consequent impacts on mitochondrial and cytoskeletal integrity. The failure of anti-oxidant enzymes such as SOD and molecular chaperones to limit damage caused by ROS is likely to result in cellular dysfunction and ultimately apoptotic cell death. All of these effects have been demonstrated in numerous studies of cellular function in oysters responding to stress [32–49]. Modulation of the mitochondrial electron transport chain and its downstream consequences, as depicted in this consensus model, may explain many of the impacts that environmental stress exerts at levels of biological organization from cells to ecosystems [32].

Bottom Line: To address this shortfall, we conducted a meta-analysis of 14 studies that investigated the effects of different environmental stressors on gene expression in oysters.We found that the expression of over 400 genes in a range of oyster species changed significantly after exposure to environmental stress.In light of these findings, we put forward a consensus model of sub-cellular stress responses in oysters.

View Article: PubMed Central - PubMed

Affiliation: Sydney Institute of Marine Science, Chowder Bay, NSW, Australia; Department of Biological Sciences, Macquarie University, North Ryde, NSW, Australia.

ABSTRACT
Many microarray and suppression subtractive hybridization (SSH) studies have analyzed the effects of environmental stress on gene transcription in marine species. However, there have been no unifying analyses of these data to identify common stress response pathways. To address this shortfall, we conducted a meta-analysis of 14 studies that investigated the effects of different environmental stressors on gene expression in oysters. The stressors tested included chemical contamination, hypoxia and infection, as well as extremes of temperature, pH and turbidity. We found that the expression of over 400 genes in a range of oyster species changed significantly after exposure to environmental stress. A repeating pattern was evident in these transcriptional responses, regardless of the type of stress applied. Many of the genes that responded to environmental stress encoded proteins involved in translation and protein processing (including molecular chaperones), the mitochondrial electron transport chain, anti-oxidant activity and the cytoskeleton. In light of these findings, we put forward a consensus model of sub-cellular stress responses in oysters.

Show MeSH
Related in: MedlinePlus