Few terrestrial animals ever experience hypoxia (when oxygen is scarce), but spells of low oxygen availability are routine for creatures clinging to life on the seashore: ‘Diurnal cycles of respiration and photosynthesis in the coastal zones commonly lead to O2 swings from near-anoxia during the night to hyperoxia during the day’, says Inna Sokolova from the University of North Carolina at Charlotte, USA. Yet, many of these creatures can withstand periods of oxygen deprivation lasting weeks and even months. Sokolova explains that several of the mechanisms that underpin the coast dwellers’ survival are already known, including the use of alternative mechanisms to generate ATP and the animals’ ability to drop their metabolic rate to conserve energy. However, Sokolova explains that little was known about how these resilient species protected the essential mitochondria – which consume oxygen to generate ATP – from the damaging effects of oxygen deprivation.
Sokolova and a team of colleagues investigated the function of mitochondria in two shoreline species: the hypoxia-tolerant hard clam (Mercenaria mercenaria), which can survive for 2 weeks with no oxygen at all, and the less robust bay scallop (Argopecten irradians), which can only survive a few hours in anoxia. Keeping the bivalves in deoxygenated water (less than 0.1% oxygen) for 18 h, the team then collected samples from the gills, hepatopancreas tissue and adductor muscles to find out how the mitochondria had responded to oxygen deprivation. In addition, the team collected tissues from molluscs that had not experienced hypoxia, and from molluscs that had been transferred back into water with normal oxygen concentrations after hypoxia to find out how they responded as damaging oxygen flooded back into their bodies.
Analysing the animals’ responses, the team saw that when the oxygen returned after an extended period of hypoxia, the scallops suffered similar experiences to those of other hypoxia-sensitive animals: the mitochondria were impaired, reducing their oxidation and phosphorylation capacities as they partially depolarized and the potential difference across the membrane reduced. In parallel, the vulnerable scallops ramped up production of heat shock proteins – which mop up proteins that have been damaged by the oxygen influx – in order to reduce the damage incurred by the mitochondria during reoxygenation. In contrast, the robust clams increased the oxidative capacity of their mitochondria during hypoxia and this also continued rising when the oxygen returned. Meanwhile, both of the molluscs reduced phosphorylation activity (which is normally responsible for ATP production via the Fo,F1-ATPase) during the extended period of hypoxia, ‘Likely to prevent ATP wastage by the reverse action of the ATPase’, say Sokolova and colleagues, although the clams regained this activity during the 1 h period of reoxygenation, when the scallops’ phosphorylation activity failed to improve. And when the team tested the bivalves’ ability to conserve energy by downregulating non-essential metabolic processes, it was clear that the clam was better able to reduce its energy expenditure than the more vulnerable scallop, although neither animal was severely energy deprived.
So, a period of hypoxia dramatically affects both the hypoxia-tolerant hard clam and the more susceptible bay scallop, but alterations in the physiology of the clam leave it better prepared to tackle extended periods of hypoxia than its scallop shore-mate.
