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Life Strategies in the Long-Lived Bivalve Arctica Islandica on a Latitudinal Climate Gradient – Environmental Constraints and Evolutionary Adaptations

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Life strategies in the long-lived bivalve Arctica islandica on a latitudinal climate gradient – Environmental constraints and evolutionary adaptations Lebensstrategien der langlebigen Muschel Arctica islandica, untersucht an Populationen entlang eines Klimagradienten – Umwelteinflüsse und evolutionäre Anpassungen Dissertation zur Erlangung des Grades eines Doktors der Naturwissenschaften -Dr. rer. nat.- Fachbereich 2 Biologie/Chemie Universität Bremen vorgelegt von Julia Strahl Bremen März 2011 Prüfungsausschuss: 1. Gutachter: Prof. Dr. Ralf Dringen (Zentrum für Biomolekulare Interaktionen Bremen, Universität Bremen) 2. Gutachter: PD Dr. Doris Abele (Funktionelle Ökologie, Alfred-Wegener-Institut für Polar- und Meeresforschung, Bremerhaven) 1. Prüfer: Prof. Dr. Thomas Brey (Funktionelle Ökologie, Alfred-Wegener-Institut für Polar- und Meeresforschung, Bremerhaven) 2. Prüfer: Prof. Dr. Kai Bischof (Marine Botanik, Universität Bremen) CONTENTS FREQUENTLY USED ABBREVATIONS I SUMMARY III ZUSAMMENFASSUNG V 1. INTRODUCTION 1 1.1. Bivalves as models in aging research 1 1.2. Why is Arctica islandica an interesting model in aging research? 2 1.3. What is aging? 4 1.4. Physiological parameters involved in the aging process 5 1.5. Is the aging process in ectotherms related to reactive oxygen species formation? 6 1.6. Cellular maintenance and longevity 7 1.7. Metabolic rate depression and longevity 9 1.8. Possible role of nitric oxide in metabolic rate depression 10 1.9. Metabolic rate depression, anaerobiosis and recovery from anoxia 10 1.10. Aims of the thesis 13 2. MATERIALS AND METHODS – A GENERAL OVERVIEW 14 2.1. Investigated species and sampling locations 14 2.2. Experimental studies 15 2.2.1. Incubation experiment for the determination of cell-turnover rates 15 2.2.2. Field and laboratory studies of burrowing behavior and self-induced metabolic rate depression in Iceland and German Bight Arctica islandica 15 2.2.3. Laboratory study of forced metabolic rate depression 17 2.2.4. Measurement of ROS-formation in isolated gill tissue 18 2.2.5. Measurement of aerobic metabolic rates 18 2.2.6. Investigation of nitric oxide formation and its possible role as modulator of cellular respiration 19 2.3. Biochemical Assays 20 2.3.1. Proliferation rates 20 2.3.2. Apopotosis intensities 20 2.3.3. Mitochondrial enzyme activity 20 2.3.4. Adenylate concentrations and energy charge 20 2.3.5. Antioxidant defense parameters 20 2.3.6. Anaerobic enzyme activity and accumulation of anaerobic metabolites 20 2.3.7. Nitrite and nitrate contents 21 2.4. Individual age determination 21 3. PUBLICATIONS 23 Publication I 25 Cell turnover in tissues of the long-lived ocean quahog Arctica islandica and the short-lived scallop Aequipecten opercularis Publication II 45 Metabolic and physiological responses in tissues of the long-lived bivalve Arctica islandica to oxygen deficiency Publication III 63 Metabolic rate depression: a key to longevity in the ocean quahog Arctica islandica 4. CONTRIBUTED WORK 87 Publication IV 89 A metabolic model for the ocean quahog Arctica islandica – Effects of animal mass and age, temperature, salinity, and geography on respiration rate Publication V 107 Age dependent patterns of antioxidants in Arctica islandica from six regionally separate populations with different life spans Publication VI 127 Aging in marine animals 5. ADDITIONAL RESULTS 149 5.1. Possible functions of the signaling molecule nitric oxide in the bivalve Arctica islandica 151 5.2. Hemocyte cell cultures 169 6. DISCUSSION 173 6.1. What contributes to the long live expectancy in Arctica islandica? 173 6.2. Metabolic rate depression as life-prolonging strategy in Arctica islandica and the possible role of NO in regulating cellular respiration in this species 177 6.3. What are the reasons for the differences in maximum life span in geographically separated Arctica islandica populations? Intrinsic vs. extrinsic determinants 179 6.4. Reproduction and longevity in Arctica islandica 182 7. CONCLUSIONS AND PERSPECTIVES 185 8. REFERENCES 189 ACKNOWLEDGEMENTS 199 Abbreviations FREQUENTLY USED ABBREVIATIONS ADP Adenosine diphosphate AFDM Ash free dry mass ATP Adenosine triphosphate B Burrowed BrdU 5-Bromo-2-deoxyuridine CAT Catalase CS Citrate synthase EC Energy charge GB German Bight GSH Reduced glutathione GSSG Oxidized glutathione GSx Total glutathione (GSH + 2 x GSSG) IC Iceland LDH Lactate dehydrogenase MLSP Maximum life span potential MRD Metabolic rate depression MSR Mass specific respiration NE North East NW North West ODH Octopine dehydrogenase PO2 Oxygen partial pressure Pcrit Critical PO2 NO Nitric oxide NOS Nitric oxide synthase RLU Relative luminescence units ROS Reactive oxygen species SMR Standard metabolic rate SOD Superoxide dismutase SST Sea surface temperature VBGF Von Bertalanffy growth function I II Summary SUMMARY The ocean quahog, Arctica islandica is the longest-lived non-colonial animal known to science. A maximum individual age of this bivalve of 405 years has been found in a population off the north western coast of Iceland. Conspicuously shorter maximum lifespan potentials (MLSPs) were recorded from other populations of A. islandica in European waters (e.g. Kiel Bay: 30 years, German Bight: 150 years) which experience wider temperature and salinity fluctuations than the clams from Iceland. The aim of my thesis was to identify possible life-prolonging physiological strategies in A. islandica and to examine the modulating effects of extrinsic factors (e.g. seawater temperature, food availa- bility) and intrinsic factors (e.g. species-specific behavior) on these strategies. Burrowing behavior and metabolic rate depression (MRD), tissue-specific antioxidant and anaerobic capacities as well as cell-turnover (= apoptosis and proliferation) rates were investigated in A. islandica from Iceland and the German Bight. An inter-species comparison of the quahog with the epibenthic scallop Aequipecten opercularis (MLSP = 8-10 years) was carried out in order to determine whether bivalves with short lifespans and different lifestyles also feature a different pattern in cellular maintenance and repair. The combined effects of a low-metabolic lifestyle, low oxidative damage accumulation, and constant investment into cellular protection and tissue maintenance, appear to slow-down the process of physiological aging in A. islandica and to afford the extraordinarily long MLSP in this species. Standard metabolic rates were lower in A. islandica when compared to the shorter-lived A. opercularis. Furthermore, A. islandica regulate mantle cavity water PO2 to mean values < 5 kPa, a PO2 at which the formation of reactive oxygen species (ROS) in isolated gill tissues of the clams was found to be 10 times lower than at normoxic conditions (21 kPa). Burrowing and metabolic rate depression (MRD) in Icelandic specimens were more pronounced in winter, possibly supported by low seawater temperature and food availability, and seem to be key energy-saving and life-prolonging parameters in A. islandica. The signaling molecule nitric oxide (NO) may play an important role during the onset of MRD in the ocean quahog by directly inhibiting cytochome-c-oxidase at low internal oxygenation upon shell closure. In laboratory experiments, respiration of isolated A. islandica gills was completely inhibited by chemically produced NO at low experimental PO2 ≤ 10 kPa. During shell closure, mantle cavity water PO2 decreased to 0 kPa for longer than 24 h, a state in which ROS production is supposed to subside. Compared to other mollusk species, onset of anaerobic metabolism is late in A. islandica in the metabolically reduced state. Increased accumulation of the anaerobic metabolite succinate was initially detected in the adductor muscle of the clams after 3.5 days under anoxic incubation or in burrowed specimens. A ROS-burst was absent in isolated gill tissue of the clams following hypoxia (5 kPa)-reoxygenation (21 kPa). Accordingly, neither the activity of antioxidant enzymes superoxide dismutase (SOD) and catalase (CAT), nor the specific content of the ROS-scavenger glutathione (GSH) was enhanced in different tissues of the ocean quahog after 3.5 days of self-induced or forced hypoxia/anoxia to prepare for an oxidative burst. III Summary While reduced ROS formation compared to routine levels lowers oxidative stress during MRD and also during surfacing, the general preservation of high cellular defense and the efficient removal and replacement of damaged cells over lifetime seem to be of crucial importance in decelerating the senescent decline in tissues of A. islandica. Along with stable antioxidant protection over 200 years of age, proliferation rates and apoptosis intensities in most investigated tissues of the ocean quahog were low, but constant over 140 years of age. Accordingly, age-dependent accumu- lations of protein and lipid oxidation products are lower in A. islandica tissues when compared to the shorter-lived bivalve A. opercularis. The short-lived swimming scallop is a model bivalve species representing the opposite life and aging strategy to A. islandica. In this species permanently high energy throughput, reduced invest- ment into antioxidant defense with age, and higher accumulation of oxidation products are met by higher cell turnover rates than in the ocean quahog. The only symptoms of physiological change over age ever found in A. islandica were decreasing cell turnover rates in the heart muscle over a lifetime of 140 years. This may either indicate higher damage levels and
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