Age-dependent patterns of antioxidants in Arctica islandica from six regionally separate populations with different lifespans

Abstract

Environmental factors such as temperature and salinity regimes shape lifespan in marine ectotherms. We investigated whether the effect occurs through modification of metabolic reactive oxygen species (ROS)-producing processes and is thus in line with the rate of living-free radical theory of aging. We compared 6 biogeographically and climatically distinct populations of the extremely long-lived ocean quahog Arctica islandica for age-dependent differences in metabolic rates and antioxidant capacities (superoxide dismutase, catalase activity and total glutathione concentration). The temperature and salinity ranges covered by the sampling locations (Norwegian coast, White Sea, Iceland, Kattegat, Kiel Bay and German Bight) were 3.7 to 9.3°C and 20 to 35 ppt. Bivalve shells were used as age recorders by counting annual growth bands. Maximum determined age in different populations varied between 29 and 192 yr. Extreme longevity observed in some North Atlantic A. islandica populations seems to be based on their very low lifetime mass-specific respiration, in combination with stable maintenance of antioxidant protection throughout life in mature specimens. While the antioxidant capacity was similar among all populations, the shorter-lived populations exhibited the highest metabolic rates and showed no metabolic response (Q 10 ) when warmed to higher temperature. Low and fluctuating salinity in the Baltic may further exert stress, which enhances respiration rates and reduces longevity in the Baltic Sea population. The exceptionally long lifespan of A. islandica cannot be exclusively explained by a well-established antioxidant defense system, and the long lifespan of some populations may rather be a function of low ROS formation (low metabolic rate) and high damage repair/removal capacities.

Age-related cellular changes in the long-lived bivalve A. islandica

“…The Baltic Sea environment is characterized by large environmental fluctuations, while the Icelandic environment is relatively stable (Basova et al 2012). For example, Baltic Sea animals must adapt their metabolic behavior to recurring hypoxic and anoxic events, which can induce changes in gene expression levels that potentially lower protein stability (Conley et al 2007(Conley et al , 2009Philipp et al 2012).…”

“…Long-lived ocean quahogs show little decline in telomere maintenance, protein carbonylation, and antioxidant capacities with age; they also have low susceptibility to genotoxic stresses, including topoisomerase inhibitors (Strahl et al 2007;Abele et al 2008;Ungvari et al 2011Ungvari et al , 2013Gruber et al 2014). The short-lived Baltic Sea population experiences high environmental stress throughout the year (e.g., fluctuations in temperature, oxygen availability, salinity), while the long-lived Icelandic population lives in a relatively constant environment (Basova et al 2012). Stressful conditions may harm the shorter-lived population and lead to higher mortality rates (Begum et al 2010).…”

Telomere-independent ageing in the longest-lived non-colonial animal, Arctica islandica

“…The Irish Sea (IS) population has an estimated maximum lifespan (MLSP) of 220 years and individuals of the BS population reach an age of approximately 40 years (Begum et al, 2010). Thus MLSP of this species varies extremely between populations and seems to depend on the respective environmental conditions (Basova et al, 2012). The extreme difference in MLSP in A. islandica populations offers a promising opportunity for ageing research, such as the examination of the telomere dynamics with age.…”

“…A. islandica can be found in the northern hemisphere and lives on continental shelves across the North Atlantic down to Virginia at the western Atlantic coast and to the Barents Sea in the east , where it can tolerate a wide range of different environmental factors (salinity, temperature, oxygen availability) (Basova et al, 2012). Their distribution into the Baltic Sea (BS) and the White Sea seems to be limited by ecological attributes of brackish environment like salinity, temperature, and oxygen gradients .…”

“…Further, the species demonstrates indeterminate growth with very low growth rates compared to other bivalves (Begum et al, 2010;Strahl et al, 2007;Witbaard, 1996) and a constant rate of cell proliferation in many different tissues (Strahl and Abele, 2010). A. islandica is found in habitats with extremely different environmental conditions and populations exhibit large variations in maximum lifespans (Basova et al, 2012). Recent studies in marine bivalve molluscs have revealed an association between longevity and resistance to multiplex stressors (oxidative, genotoxic stress) as well as between longevity and proteostasis in several species including A. islandica (Treaster et al, 2013;Ungvari et al, 2013a;Ungvari et al, 2011;Ungvari et al, 2013b).…”