Gene Expression and Physiological Changes of Different Populations of the Long-Lived Bivalve Arctica islandica under Low Oxygen Conditions

Abstract

The bivalve Arctica islandica is extremely long lived (>400 years) and can tolerate long periods of hypoxia and anoxia. European populations differ in maximum life spans (MLSP) from 40 years in the Baltic to >400 years around Iceland. Characteristic behavior of A. islandica involves phases of metabolic rate depression (MRD) during which the animals burry into the sediment for several days. During these phases the shell water oxygen concentrations reaches hypoxic to anoxic levels, which possibly support the long life span of some populations. We investigated gene regulation in A. islandica from a long-lived (MLSP 150 years) German Bight population and the short-lived Baltic Sea population, experimentally exposed to different oxygen levels. A new A. islandica transcriptome enabled the identification of genes important during hypoxia/anoxia events and, more generally, gene mining for putative stress response and (anti-) aging genes. Expression changes of a) antioxidant defense: Catalase, Glutathione peroxidase, manganese and copper-zinc Superoxide dismutase; b) oxygen sensing and general stress response: Hypoxia inducible factor alpha, Prolyl hydroxylase and Heat-shock protein 70; and c) anaerobic capacity: Malate dehydrogenase and Octopine dehydrogenase, related transcripts were investigated. Exposed to low oxygen, German Bight individuals suppressed transcription of all investigated genes, whereas Baltic Sea bivalves enhanced gene transcription under anoxic incubation (0 kPa) and, further, decreased these transcription levels again during 6 h of re-oxygenation. Hypoxic and anoxic exposure and subsequent re-oxygenation in Baltic Sea animals did not lead to increased protein oxidation or induction of apoptosis, emphasizing considerable hypoxia/re-oxygenation tolerance in this species. The data suggest that the energy saving effect of MRD may not be an attribute of Baltic Sea A. islandica chronically exposed to high environmental variability (oxygenation, temperature, salinity). Contrary, higher physiological flexibility and stress hardening may predispose these animals to perform a pronounced stress response at the expense of life span.

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). Relatively stable proteins in Icelandic A. islandica support previous findings showing high stress resistance in A. islandica (Ungvari et al 2011(Ungvari et al , 2013.…”

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

“…Moreover, compared to the highly stable marine IC habitat the brackish BS environment is highly fluctuating not only in respect to salinity but also in ionic compositions of the water body, water temperature, oxygen content and nutrient concentrations which implies a general more stressful habitat and an impact on telomere dynamics as hypothesized by others (Hall et al, 2004;Horn et al, 2008;Jennings et al, 2000). Philipp et al (2012) for example could show that A. islandica from the Baltic Sea and Iceland were found to differ in transcriptional response towards hypoxia which was attributed to the adaptation to different environmental stability of the two populations. Stressful environments have been linked to higher levels of oxidative stress, associated to telomere shortening (Jennings et al, 2000;Von Zglinicki, 2002).…”

“…The BS population endures great fluctuations in temperature, salinity and oxygen availability (Begum et al, 2010), whereas abiotic conditions in the Northeast of Iceland are much more constant and stable (Basova et al, 2012). It is hypothesized this may greatly influence the animals' energy allocation to tissue maintenance, growth or reproduction but also the physiological response to different environmental stressors as recently reported for different A. islandica populations Basova et al, 2012;Philipp et al, 2012). The vast difference in MLSP and the environmental variables makes the two populations from the BS and IC with shortest (BS, MLSP 40 years) and longest (IC, MLSP N500 years) MLSP reported so far interesting objects for ageing studies, especially for the examination of telomere dynamics in A. islandica.…”

Environmental Control and Control of the Environment: The Basis of Longevity in Bivalves

“…In experimental hypoxia, anoxia and MRD (burrowed individuals), the bivalves kept up their antioxidant defences (enzyme activities and glutathione levels) [7,13], and antioxidant transcript levels were mostly stable in the burrowed-MRD state (catalase, glutathione peroxidase, Mn-SOD constant, whereas Cu-Zn SOD diminished) and under experimental hypoxia. In response to anoxia, antioxidant and stress gene transcript levels decreased altogether, as the individuals reduced protein synthesis as a consequence of metabolic shutdown [14]. It thus appears that long-lived A. islandica suspend the anticipatory upregulation of antioxidant/stress defence.…”

“…In this marginal, but stable and highly productive population, maximum lifespan (MLSP) is reduced to only 40 years. In Baltic Sea Arctica , the majority of stress genes were upregulated in response to anoxia (but not hypoxia) [14]. The Baltic Sea bivalves live in a highly fluctuating environment with fast and extreme changes in temperature, salinity and oxygen, whereas German Bight individuals experience more stable physical conditions.…”