The impact of acute temperature stress on hemocytes of invasive and native mussels (Mytilus galloprovincialisandM. californianus): DNA damage, membrane integrity, apoptosis and signalling pathways

Abstract

SUMMARYWe investigated the effects of acute heat stress and cold stress on cell viability, lysosome membrane stability, double-and singlestranded DNA breakage, and signaling mechanisms involved in cellular homeostasis and apoptosis in hemocytes of native and invasive mussels, Mytilus californianus and Mytilus galloprovincialis, respectively. Both heat stress (28, 32°C) and cold stress (2, 6°C) led to significant double-and single-stranded breaks in DNA. The type and extent of DNA damage were temperature and time dependent, as was caspase-3 activation, an indicator of apoptosis, which may occur in response to DNA damage. Hemocyte viability and lysosomal membrane stability decreased significantly under heat stress. Western blot analyses of hemocyte extracts with antibodies for proteins associated with cell signaling and stress responses [including members of the phospho-specific mitogen-activated protein kinase (MAPK) family c-JUN NH 2 -terminal kinase (JNK) and p38-MAPK, and apoptosis executor caspase-3] revealed that heat and cold stress induced a time-dependent activation of JNK, p38-MAPK and caspase-3 and that these signaling and stress responses differed between species. The thermal limits for activation of cell signaling processes linked to the repair of stress-induced damage may help determine cellular thermal tolerance limits. Our results show similarities in responses to cold and heat stress and suggest causal linkages between levels of DNA damage at both extremes of temperature and downstream regulatory responses, including induction of apoptosis. Compared with M. californianus, M. galloprovincialis might have a wider temperature tolerance due to a lower amount of single-and double-stranded DNA damage, faster signaling activation and transduction, and stronger repair ability against temperature stress.

Behavior and survival ofMytiluscongeners following episodes of elevated body temperature in air and seawater

“…Specifically, valve gaping during recovery would permit more efficient aerobic ATP generation to fuel macromolecular repair. This prediction corresponds well with gene and protein expression data indicative of damage to proteins (induction of heat shock proteins and proteasome constituents) (Buckley et al, 2001;Gracey et al, 2008;Lockwood et al, 2010;Tomanek and Zuzow, 2010), and it is further supported by the discovery that thermal stress leads to significant increases in single-and double-stranded DNA breakage (Yao and Somero, 2012). Other gene expression studies have indicated alternating phases of oxidative and reductive metabolism in M. californianus (Connor and Gracey, 2011;Gracey et al, 2008).…”

Moderately lower temperatures greatly extend the lifespan of Brachionus manjavacas (Rotifera): Thermodynamics or gene regulation?

“…This suggests disruption of the membrane integrity of the gut, allowing algae to leak into the pseudocoelom. This is consistent with the finding that heat and cold stress caused a decrease in membrane stability in mussels (Yao & Somero 2012). …”

Temperature and population density: interactional effects of environmental factors on phenotypic plasticity, immune defenses, and disease resistance in an insect pest

“…While some studies show this component of the immune function can be increased at warmer environmental temperatures (Truscott and White 1990; Chu and Lapeyre 1993), the decrease in hemocyte numbers found here may be related to its viability or stress‐induced damage (such as apoptosis) in a warmer environment (Yao and Somero 2012; Diaz et al. 2013).…”