The proteomic response of cheliped myofibril tissue in the eurythermal porcelain crab Petrolisthes cinctipes to heat shock following acclimation to daily temperature fluctuations

Abstract

The porcelain crab Petrolisthes cinctipes lives under rocks and in mussel beds in the mid-intertidal zone where it experiences immersion during high tide and saturating humid conditions in air during low tide, which can increase habitat temperature by up to 20°C. To identify the biochemical changes affected by increasing temperature fluctuations and subsequent heat shock, we acclimated P. cinctipes for 30 days to one of three temperature regimes: (1) constant 10°C, (2) daily temperature fluctuations between 10 and 20°C (5 h up-ramp to 20°C, 1 h down-ramp to 10°C) and (3) 10-30°C (up-ramp to 30°C). After acclimation, animals were exposed to either 10°C or a 30°C heat shock to analyze the proteomic changes in claw muscle tissue. Following acclimation to 10-30°C (measured at 10°C), enolase and ATP synthase increased in abundance. Following heat shock, isoforms of arginine kinase and glycolytic enzymes such as aldolase, triose phosphate isomerase and glyceraldehyde 3-phosphate dehydrogenase increased across all acclimation regimes. Full-length isoforms of hemocyanin increased abundance following acclimation to 10-30°C, but hemocyanin fragments increased after heat shock following constant 10°C and fluctuating 10-20°C, possibly playing a role as antimicrobial peptides. Following constant 10°C and fluctuating 10-20°C, paramyosin and myosin heavy chain type-B increased in abundance, respectively, whereas myosin light and heavy chain decreased with heat shock. Actin-binding proteins, which stabilize actin filaments (filamin and tropomyosin), increased during heat shock following 10-30°C; however, actin severing and depolymerization proteins (gelsolin and cofilin) increased during heat shock following 10-20°C, possibly promoting muscle fiber restructuring. RAF kinase inhibitor protein and prostaglandin reductase increased during heat shock following constant 10°C and fluctuating 10-20°C, possibly inhibiting an immune response during heat shock. The results suggest that ATP supply, muscle fiber restructuring and immune responses are all affected by temperature fluctuations and subsequent acute heat shock in muscle tissue. Furthermore, although heat shock after acclimation to constant 10°C and fluctuating 10-30°C showed the greatest effects on the proteome, moderately fluctuating temperatures (10-20°C) broadened the temperature range over which claw muscle was able to respond to an acute heat shock with limited changes in the muscle proteome. INTRODUCTIONEnvironmental temperature has a ubiquitous effect on rates of biochemical reactions and cellular structures in ectothermic organisms, which have adapted their cellular processes and structures to cope with the specific thermal properties of their habitat (Somero, 2012;Tomanek, 2010). An organism's ability to adjust biochemical processes to different body temperatures is in large part determined by the rate and amplitude of temperature change and its evolutionary history, e.g. the thermal environment it occupies and recent thermal history, e.g. acclimatization. For...

Temperature gradient affects differentiation of gene expression and SNP allele frequencies in the dominant Lake Baikal zooplankton species

“…More strait. The observed differential expression and possible genetic differentiation of cytoskeleton-related transcripts are, therefore, in agreement with similar results found in heat-or hypoxiarelated stress proteomics studies in a variety of aquatic poikilothermic organisms including marine bivalves (Haslbeck, Franzmann, Weinfurtner, & Buchner, 2005), marine crabs (Garland, Stillman, & Tomanek, 2015), marine tunicates (Serafini, Hann, K€ ultz, & Tomanek, 2011) and freshwater fish (Chen, Cole, & Rees, 2013). Finally, the downregulation of numerous cuticle proteins in warmer areas of the lake and in the laboratory experiment (Supporting information Table S4) is consistent with similar observations for their orthologs in a parasitic copepod Lepeophtheirus salmonis larvae (Sutherland et al, 2012;) and with the previously hypothesized role of cuticle proteins in swimming efficiency in Cyclops (Alcaraz & Strickler, 1988).…”

Antimicrobial proteins: From old proteins, new tricks

“…As yet, it has still to be clarified how these fragments are cleaved from haemocyanin in vivo. It could be via proteases liberated from haemocytes, as suggested originally by Destoumieux-Garzon et al (2001), but it could occur non-proteolytically as a recent paper has found that in the porcelain crab, Petrolisthes cinctipes, haemocyanin fragmentation occurs after non-lethal heat-shock (Garland et al, 2015). Interestingly, heatshock enhances haemocyanin mRNA expression in L. vannamei (Loc et al, 2013) possibly to replenish the haemocyanin pool depleted by fragmentation.…”

Proteomic analysis of cardiac response to thermal acclimation in the eurythermal goby fish Gillichthys mirabilis

“…Based on the role of the cytosolic isoform of CK within the PCr circuit, it is possible that the increase in the abundance of this protein in cardiac muscle of cold-acclimated G. mirabilis contributes to maintaining higher ATP:ADP ratios during periods of high ATP turnover (Dzeja and Terzic, 2003) and, thereby, compensates for reduced reaction rates in cold temperatures (Christensen et al, 1994). Its invertebrate analog, arginine kinase, has been shown to play an important role during temperature acclimation in the cheliped myofibril tissue of porcelain crabs (Garland et al, 2015).…”