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Transcriptomic responses to heat-stress in invasive and native blue mussels (genus Mytilus)

ABSTRACT: [original Title] Transcriptomic responses to heat-stress in invasive and native blue mussels (genus Mytilus): molecular correlates of invasive success. Invasive species are increasingly prevalent in marine ecosystems worldwide. Although many studies have examined the ecological effects of invasives, little is known about physiological mechanisms that might contribute to invasive success. The mussel Mytilus galloprovincialis, a native of the Mediterranean Sea, is a successful invader on the central and southern coasts of California, where it has largely displaced the native congener, Mytilus trossulus. It has been previously shown that thermal responses of several physiological traits may underlie the capacity of M. galloprovincialis to out-compete M. trossulus in warm habitats. To elucidate possible differences in stress-induced gene expression between these congeners, we developed an oligonucleotide microarray with 8,874 probes representing 4,488 different genes that recognized mRNAs of both species. In acute heat-stress experiments, 1,531 of these genes showed temperature-dependent changes in gene expression that were highly similar in the two congeners. In contrast, 96 genes showed species-specific responses to heat-stress, functionally characterized by their involvement in oxidative stress, proteolysis, energy metabolism, ion transport, cell signaling, and cytoskeletal reorganization. The gene that showed the biggest difference between the species was the gene for the molecular chaperone small heat shock protein 24, which was highly induced in M. galloprovincialis and showed only a small change in M. trossulus. These different responses to acute heat-stress may help to explain—and predict—the invasive success of M. galloprovincialis in a warming world.

OTHER RELATED OMICS DATASETS IN: PRJNA120631

ORGANISM(S): Mytilus californianus Mytilus galloprovincialis Mytilus trossulus

PROVIDER: GSE19031 | GEO | 2010/10/11

SECONDARY ACCESSION(S): PRJNA120631

REPOSITORIES: GEO

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Project description:The invasive marine mussel Mytilus galloprovincialis has displaced the native congener Mytilus trossulus from central and southern California, but the native species remains dominant at more northerly sites that have high levels of freshwater input. To determine the extent to which interspecific differences in physiological tolerance to low salinity might explain limits to the invasive species’ biogeography, we used an oligonucleotide microarray to compare the transcriptional responses of these two species to an acute decrease in salinity. Among 6,777 genes on the microarray, 117 genes showed significant changes that were similar between species, and 12 genes showed significant species-specific responses to salinity stress. Osmoregulation and cell cycle control were important aspects of the shared transcriptomic response to salinity stress, whereas the genes with species-specific expression patterns were involved in mRNA splicing, polyamine synthesis, exocytosis, translation, cell adhesion, and cell signaling. Forty-five genes that changed expression significantly during salinity stress also changed expression during heat stress, but the direction of change in expression was typically opposite for the two forms of stress. These results (i) provide insights into the role of changes in gene expression in establishing physiological tolerance to acute decreases in salinity, and (ii) indicate that transcriptomic differences between M. galloprovincialis and M. trossulus in response to salinity stress are subtle and involve only a minor fraction of the overall suite of gene regulatory responses. Two species (Mytilus galloprovincialis, Mytilus trossulus), hypo-osmotic shock for four hours (850 mOs/kg), one control group (1000 mOs/kg) sampled at the end of the treatment exposure (850 mOs/kg), one control group (1000 mOs/kg) sampled at the beginning. Biological replicates: 6 in each treatment group, 6 in each control group. Heterologous and homologous hybridization to a microarray constructed from Mytilus californianus and Mytilus galloprovincialis sequences. A reference design that used separate pools of reference RNA for each species was employed. Reference amplified RNA (aRNA) was created for each species by pooling RNA before and after amplification. The reference pool was made up of RNA from six different samples: two base-line control samples from the beginning of the experiment, two treatment samples from the end of the four-hour hypo-osmotic exposure, and two time-control samples from the end of the four-hour exposure time. To accurately compare the transcriptomes of Mytilus galloprovincialis and M. trossulus, we chose to develop a common microarray format that could be used for both species. This microarray design consisted of probe sequences generated from the out-group species, M. californianus. M. trossulus and M. galloprovincialis are approximately 7.5 million years divergent from M. californianus, yet only 3.5 million years divergent from each other (Seed, 1992). Therefore, heterologous hybridization to the microarray allowed us to compare transcriptional responses of M. galloprovincialis and M. trossulus without the inherent sequence biases that would result from a microarray that was designed from sequences of either M. galloprovincialis or M. trossulus. A limited number of sequences (556) from ESTs from M. galloprovincialis that matched M. californianus ESTs were included on the microarray to test for the effects of sequence mismatches. Only probes that performed well for both M. galloprovincialis and M. trossulus were used in our analyses. In order to determine significant changes in expression, we conducted a two-way ANOVA, in which salinity and species were modeled as fixed effects, and focused on genes that were significant for the salinity effect or the species x temperature interaction. We ignored the species term from the ANOVA as this effect could have highlighted genes that differentially bound to probes on the microarray due to differences in sequence homology, thus not reflecting true differences in gene expression. In accordance with statistical convention, all genes with a significant species x temperature interaction were deemed not to have significant temperature effects, even if the temperature term from the ANOVA had a low P-value. All genes with FDR-corrected (Benjamini and Hochberg, 1995) P-values less than 0.05 were considered significant. Analyses were conducted in the R statistical programming environment (R Development Core Team, 2009).

Project description:Transcriptional profiling of the digestive gland tissue of female mussel Mytilus galloprovincialis exposed to nickel along with a temperature gradient Background: The exposure of marine organisms to stressing agents may affect the level and pattern of gene expression. Although many studies have examined the ecological effects of heat stress on mussels, little is known about the physiological mechanisms that might be affected by co-exposure to heat stress and environmental contaminants such as nickel (Ni). In the present work we investigated the effects of simultaneous changes in temperature and Ni supply on lysosomal membrane stability (LMS) and malondialdehyde accumulation (MDA) in the digestive gland (DG) of the blue mussel Mytilus galloprovincialis (Lam.). To shed some light into how the molecular response to environmental stressors is modulated, we employed a cDNA microarray with 1,673 sequences to measure the relative transcript abundances in the DG of mussels exposed to Ni along with the temperature increase. Temperature and Ni rendered additive effects on LMS and MDA accumulation, increasing the toxic effects of metal cations. Ni loads in DG tissues was also affected by co-exposure to 26°C. In animals exposed only to heat stress, functional genomics analysis of the microarray data (171 DEGs) revealed 7 biological processes, largely dominated by the up-regulation of folding protein-related genes, and the down regulation of genes involved in cell migration and cellular component assembly. Exposure to Ni at 18°C and 26°C rendered respectively 188 and 262 DEGs showing distinct pattern in term of biological processes. In particular, the response of mussels exposed to Ni at 26°C was characterized by the up regulation of proteolysis, ribosome biogenesis, response to unfolded proteins and catabolic-related genes as well as the down-regulation of genes encoding cellular metabolic processes. Our data provide new insights on the transcriptomic response in mussels challenging temperature increases and Ni exposure and should be carefully considered in view of the biological effects of heat stress and particularly in polluted areas.

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Transcriptomic responses to heat-stress in invasive and native blue mussels (genus Mytilus)

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