Proteomic responses of blue mussel (Mytilus) congeners to temperature acclimation

Abstract

SUMMARYThe ability to acclimate to variable environmental conditions affects the biogeographic range of species, their success at colonizing new habitats, and their likelihood of surviving rapid anthropogenic climate change. Here we compared responses to temperature acclimation (4weeks at 7, 13 and 19°C) in gill tissue of the warm-adapted intertidal blue mussel Mytilus galloprovincialis, an invasive species in the northeastern Pacific, and the cold-adapted M. trossulus, the native congener in the region, to better understand the physiological differences underlying the ongoing competition. Using two-dimensional gel electrophoresis and tandem mass spectrometry, we showed that warm acclimation caused changes in cytoskeletal composition and proteins of energy metabolism in both species, consistent with increasing rates of filtration and respiration due to increased ciliary activity. During cold acclimation, changes in cytoskeletal proteins were accompanied by increasing abundances of oxidative stress proteins and molecular chaperones, possibly because of the increased production of aldehydes as indicated by the upregulation of aldehyde dehydrogenase. The cold-adapted M. trossulus showed increased abundances of molecular chaperones at 19°C, but M. galloprovincialis did not, suggesting that the two species differ in their long-term upper thermal limits. In contrast, the warm-adapted M. galloprovincialis showed a stronger response to cold acclimation than M. trossulus, including changes in abundance in more proteins and differing protein expression profiles between 7 and 13°C, a pattern absent in M. trossulus. In general, increasing levels of oxidative stress proteins inversely correlate with modifications in Krebs cycle and electron transport chain proteins, indicating a trade-off between oxidative stress resistance and energy production. Overall, our results help explain why M. galloprovincialis has replaced M. trossulus in southern California over the last century, but also suggest that M. trossulus may maintain a competitive advantage at colder temperatures. Anthropogenic global warming may reinforce the advantage M. galloprovincialis has over M. trossulus in the warmer parts of the latterʼs historical range. Supplementary material available online at

Proteomic responses to environmentally induced oxidative stress

“…Finally, acclimation to cold (7°C), moderate (13°C) and warm (19°C) temperatures for 4 weeks increased Prx at cold to moderate temperatures in gill of the warm-adapted M. galloprovincialis for which 7 and 13°C are at the low end of the temperature range it prefers (Fields et al, 2012b). In contrast, cold to moderate temperatures in comparison to warm temperatures caused a change in abundance in an opposite fashion of two isoforms of DyP-type peroxidase in the cold-adapted M. trossulus, indicating a PTM as the reason for this change of abundance from cold and moderate to warm temperatures.…”

“…The reason for a decrease in SDH might be to counteract the potentially pro-oxidant effects of succinate accumulation (Chouchani et al, 2014). SDH also decreased in abundance in an opposite fashion to some antioxidant proteins during chronic temperature stress in M. trossulus (Fields et al, 2012b). However, highlighting the multiple roles of this enzyme, it increased in gill in response to hypoxia in Geukensia (Fields et al, 2014), most likely as part of an anaerobic metabolic pathway typical of bivalves (Muller et al, 2012 Fig.…”

“…However, if this hypothesis is correct, it is still unclear whether protein denaturation and the proposed subsequent reduction in protein synthesis cause an overall lower demand for (ER and cytosolic) antioxidant proteins, or whether environmental stress caused an increase in overall ROS production throughout the cell, requiring a decrease in protein maturation generating H 2 O 2 and thereby also a localized decrease in antioxidant proteins. Furthermore, while acute heat stress did not activate changes in ER chaperones in Mytilus congeners, chronic cold and warm temperature stress changed the abundance of Grp78 and DyP-peroxidase in M. trossulus (Fields et al, 2012b;Tomanek and Zuzow, 2010). A comparison of the proteomic responses of gill of five populations of the mussel G. demissa from different latitudes along the Atlantic coast of North America in response to acute heat stress showed changes in two Grp78 and one PPIase isoform (Fields et al, 2012a).…”

“…A number of recent proteomic studies indeed showed changes in the abundance of either NADH dehydrogenase or cytochrome c reductase isoforms, or both, in gill of several marine invertebrate species in response to acute and chronic temperature and hyposalinity stress (Dilly et al, 2012;Fields et al, 2012b;Tomanek and Zuzow, 2010;Tomanek et al, 2012), suggesting that decreasing abundance, composition or PTM of both complex I and III of the ETS are potential sites for regulation.…”

“…Acute and chronic heat stress, as well as hyposaline stress also showed (most frequently) an increase in abundance in additional proteins generating NADPH, specifically NADP-ICDH and ALDH in Mytilus congeners (Fields et al, 2012b;Tomanek and Zuzow, 2010;Tomanek et al, 2012). Part of the variation in how these proteins changed is due to a shift in the abundance of PTMs due to changes in the redox status of the cell, e.g.…”