Pathogenic challenge reveals immune trade-off in mussels exposed to reduced seawater pH and increased temperature

Abstract

Ocean acidification (OA) and warming pose a considerable threat to marine ecosystems. Previous studies show that these environmental co-stressors significantly impact upon a number of key physiological functions, including calcification, metabolism and growth, in many marine organisms. Yet despite the importance of the immune system, to date only a handful of studies have investigated the impact of reduced seawater pH on an organism's immune response. Furthermore, whilst temperature has received far greater attention with respect to host defence, there is a dearth of information concerning the possible synergism of these two stressors on immune defence. Here we show that a 90 day exposure to reduced seawater pH led to a reduction in the antibacterial activity of cell-free haemolymph in the blue mussel Mytilus edulis, whilst temperature led to an increase in this immune parameter. However in contrast to previous research, following this initial 90 day exposure, mussels in the current study were then exposed to the pathogenic bacterium, Vibrio tubiashii. Crucially, whilst reduced seawater pH initially appeared to impair immunological functioning, as has been interpreted previously, mussels demonstrated the ability to restore haemolymph bactericidal activity when required. This indicated that the initial reduction in antibacterial activity was in fact a reversible physiological trade-off, rather than an irreversible impairment of immune function. By demonstrating this plasticity, the current study illustrates the need to measure organism responses within a realistic natural context (i.e. measuring the immune response of an organism in the presence of a pathogen). Failure to do so may result in a misleading interpretation of the ecological relevance of experimental data, and thus the sensitivity of different species in a rapidly changing environment.

Sea urchins in a high-CO 2 world: the influence of acclimation on the immune response to ocean warming and acidification

“…In this study, H. erythrogramma exposed to both stressors over 30 days were the least effective at inhibiting growth of V. anguillarum. Similarly, reduced seawater pH decreased antibacterial activity in the mussel Mytilus edulis while elevated temperature increased antibacterial activity [49]. Our findings suggest that in H. erythrogramma, exposure to combined warming and acidification over 30 days had a greater reduction in antibacterial activity than those exposed over a similar period to a single stressor.…”

Implications of Ocean Acidification for Marine Microorganisms from the Free-Living to the Host-Associated

“…The combined effects of OA and warming on marine diseases are complex, and early evidence suggests that the effect of one stressor on disease susceptibility may counteract the effect of the other. For example, antibacterial activity in the blue mussel was reduced by around 40% at low pH (6.5), but when the temperature was increased from 12.5 to 17 • C, antibacterial activity was restored to initial levels (Ellis et al, 2015). Conversely, the progression rate of coralline fungal disease (CFD) increased in crustose coralline algae (CCA) under elevated temperatures, however this rate increase was ameliorated under low pH (Williams et al, 2014).…”

Developments since 2005 in understanding potential environmental impacts of CO2 leakage from geological storage

“…In particular, it is essential for studies not to be limited to a few traditional response variables but instead to consider the likely trade-offs and compensatory mechanisms used by marine organisms to cope with short-term variations in the levels of environmental CO 2 . This represents perhaps the biggest advance in laboratory-based CCS experiments with new studies incorporating elements of physiological plasticity (Ellis et al, 2015) and energy allocation (e.g. scope for growth or dynamic energy budget modelling (Klok et al, 2014 ).…”

“…The relevance of physiological mechanisms that allow certain species to cope with high levels of CO 2 (hypercapnia) was identified and differences between species in this respect were revealed (Kamenos et al, 2013;Hammer and Pedersen, 2013;Donohue et al, 2012;Small et al, 2010). More subtle effects of elevated CO 2 concentrations were shown in experiments with multiple stressors, such as pathogens (Ellis et al, 2015). Experimentation in more complex systems also revealed indirect impacts on marine ecosystem functions such as bioturbation and nutrient cycling (Burdett et al, 2014;Widdicombe et al, 2013b;Murray et al, 2013;Widdicombe and Needham, 2007).…”