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Auswirkungen Der Ozeanversauerung Auf Die Große Seespinne Hyas Araneus: Molekulare Mechanismen Und Plastizität

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Auswirkungen Der Ozeanversauerung Auf Die Große Seespinne Hyas Araneus: Molekulare Mechanismen Und Plastizität Auswirkungen der Ozeanversauerung auf die große Seespinne Hyas araneus: Molekulare Mechanismen und Plastizität Dissertation zur Erlangung des akademischen Grades – Dr. rer. nat. – Dem Fachbereich 2 Biologie/Chemie der Universität Bremen vorgelegt von Lars Harms Diplombiologe Bremen 2014 Der Einband enthält Illustrationen von Allen (1967) und Hugo Ahlenius (UNEP/GRID-Arendal) Gutachter: 1. Gutachter: Professor Dr. H.-O. Pörtner Alfred-Wegener-Institut – Helmholtz-Zentrum für Polar- und Meeresforschung Am Handelshafen 12, 27570 Bremerhaven 2. Gutachter: Associate Professor Dr. L. Tomanek California Polytechnic State University San Luis Obispo, California 93407, United States of America Inhaltsverzeichnis Inhaltsverzeichnis Abkürzungsverzeichnis III Zusammenfassung V Abstract VII 1 Einleitung 1 1.1 Das Projekt BIOACID 1 1.2 Einfluss von Ozeanversauerung auf marine Crustaceen 3 1.3 Kieme als Modelgewebe 6 1.4 Hyas araneus als Modelorganismus 8 1.5 Konzept und Fragestellung 11 2 Material und Methoden 13 2.1 Versuchstiere 13 2.2 Experimenteller Aufbau und Bestimmung der Meerwasserparameter 13 2.3 Probennahme und Hämolymph-Analytik 14 2.4 Molekulare Analytik 15 RNA Extraktion und Sequenzierung 15 Assemblierung, funktionelle Annotation und Sequenzalignierung 16 Quantitative Real-Time PCR 17 Protein-Aufbereitung 19 Zweidimensionale Gel-Elektrophorese und Gelanalyse 19 Massenspektrometrie 20 2.5 Statistik 21 Vergleichende Analyse 21 Transkriptomik 22 Proteomik 22 3 Publikationen 23 Publikation I 25 "Characterization and analysis of a transcriptome from the boreal spider crab Hyas araneus" Publikation II 47 "Gene expression profiling in gills of the great spider crab Hyas araneus in response to ocean acidification and warming" I Inhaltsverzeichnis Publikation III 77 "The proteomic responses of gill tissue in two populations of the spider crab Hyas araneus to simultaneously elevated PCO2 and temperature" 4 Diskussion 114 4.1 Effekte der Ozeanversauerung auf die Transkription und Translation spezifischer funktioneller Gruppen in der Kieme von Hyas araneus 114 Transkriptomik 114 Proteomik 115 Korrelation und Limitierung der genomweiten methodischen Ansätze Transkriptomik und Proteomik 116 Vergleich der transkriptionellen und translationalen Antwort auf eine erhöhte PCO2- Konzentration 119 4.2 Effekte von Erwärmung und erhöhtem PCO2 auf die molekulare Antwort verschiedener Hyas araneus Populationen entlang eines latitudinalen Gradienten 123 4.3 Extrapolation auf die Ganztier-Physiologie und Implikationen für Hyas araneus 125 4.4 Zusammenfassung und Implikationen für Hyas araneus 129 Referenzen 132 Anhang 143 Additional files – Publikation II 143 Additional files – Publikation III 168 Danksagung 172 Erklärung gemäß § 6 (5) der PromO der Universität Bremen 175 II Abkürzungsverzeichnis Abkürzungsverzeichnis ASB-14 Amidosulfobetain-14 BMBF Bundesministerium für Bildung und Forschung bp Basenpaare BWA Burrows-Wheeler Aligner CCO2 Gesamtmenge des Kohlendioxid cDNA komplementäre Desoxyribonukleinsäure CHAPS Cholamidopropyl-Dimethylammoniio-Propan-Sulfonat CO2 Kohlendioxid 2- CO3 Karbonat DIC Gesamtmenge des gelösten anorganischen Kohlenstoffs DTT Dithiothreitol EMBL-EBI European Molecular Biology Laboratory – European Bioinformatics Institute ENA European Nucleotide Archive EST Expressed Sequence Tag ETS Elektronen-Transport-System GFP Grün fluoreszierende Proteine GO Gene Ontology H+ Wasserstoffproton H2CO3 Kohlensäure HCCA -Cyano-hydroxy-zimtsäure HCL Chlorwasserstoff - HCO3 Bikarbonat IEP isoelektrischer Punkt IPCC Intergovernmental Panel on Climate Change IPG Immobilisierter pH Gradient MALDI TOF-TOF Matrix-unterstützten Laser-Desorption/Ionisation Massenspektrometer MCL Markov Cluster Algorithmus MOWSE Molecular Weight Search MPIMG Max-Planck-Institut für Molekulare Genetik MS Massenspektrum Mt Megatonnen Na+/K+-ATPase Natrium/Kalium-ATPase NCBI National Center for Biotechnology Information NH3 Ammoniak + NH4 Ammonium NHE Natrium/Wasserstoffprotonen-Austauscher NIST National Institute of Standards and Technology NP-40 Nonyl Phenoxylpolyethoxylethanol-40 PCO2 Kohlendioxidpartialdruck PMF Peptidmassenfingerabdruck ppt Teile von einer Billion qRT-PCR quantitative Real-Time Polymerase-Kettenreaktion RCP Representative Concentration Pathways RNA Ribonukleinsäure RNA-Seq Gesamt-Transkriptom-Shotgun Sequenzierung ROS reaktive Sauerstoffspezies SDS Natriumdodocylsulfat SDS-PAGE Natriumdodocylsulfat-Polyacrylamid-Gel-Elektrophorese SFF Standard Flowgram Format TFA Trifluressigsäure USA Vereinigte Staaten von Amerika atm Mikroatmosphären III IV Zusammenfassung Zusammenfassung Die Versauerung und Erwärmung der Ozeane, als Konsequenz des Klimawandels, und die dadurch möglicherweise nachteilige Beeinflussung von marinen Organismen ist im Laufe der letzten Jahre immer mehr in den Fokus der Wissenschaft gerückt. Während bereits eine Vielzahl von physiologischen und ökologischen Auswirkungen identifiziert wurden, sind die Einflüsse auf die molekularen Mechanismen, die den physiologischen Phänotyp einer Art und somit die Grenzen der kompensatorischen Kapazität formen, weitestgehend unverstanden. Im Zuge der vorliegenden Arbeit wurden aus diesem Grund verschiedene global angelegte Gen- und Proteinexpressionsanalysen genutzt, um in ihrer Kombination die regulatorischen Mechanismen und Prozesse an der großen Seespinne Hyas araneus ganzheitlich zu erfassen. Auf Basis verschiedener durchgeführter Sequenzierungen (454; Illumina) wurde in einem ersten Ansatz ein de novo Transkriptom assembliert. Es wurden insgesamt 20.479 Transkript-Sequenzen generiert, welche als Grundlage für die anschließenden Expressionsanalysen dienten. Darauf aufbauend wurde der neu erreichte Zustand in der Genexpression ermittelt. Dazu wurde eine differentielle Genexpressionsanalyse am Kiemengewebe der Tiere nach einem mittelfristigen Inkubationsexperiment (10 Wochen) bei unterschiedlichen Versuchsbedingungen durchgeführt. Die Analyse offenbarte von der Kontrollbedingung (390 atm) ausgehend eine Verschiebung der Genexpression bei einem mittleren (1.120 atm) und hohen PCO2 (1.960 atm). Bei Temperaturen von 5 °C und 10 °C zeigte sich ein vergleichbarer Verlauf. Während bei einem mittleren PCO2 Transkript-Sequenzen der Säure-Base-Regulation, des Energiestoffwechsels und der allgemeinen Stressantwort hochreguliert waren, zeigte sich bei einem hohen PCO2 eine relative Reduktion in der Expression. Es zeichnete sich ein starker Zusammenhang zwischen den funktionellen Gruppen ab. Die Expressionsprofile deuteten bei einem mittleren PCO2 auf eine gesteigerte Kapazität zur Säure- Base-Kompensation mittels einer hoch-regulierten V-ATPase hin. Bestätigt werden konnte dies durch den Säure-Base-Status der extrazellulären Flüssigkeit. Der dadurch implizierte erhöhte Energiebedarf war in der gesteigerten Expression des Elektronentransportsystems reflektiert. Möglicherweise führte dieser zu oxidativem Stress, welcher sich durch eine gesteigerte Expression von Transkript-Sequenzen zur Bekämpfung des oxidativen Stresses abzeichnete. Die Expressionsdaten offenbarten gleichzeitig ein erhöhtes Vorkommen von Zellstruktur verwandten Transkript-Sequenzen und wiesen so auf das Zytoskelett als Hauptangriffsziel des oxidativen Stresses hin. Bei einem hohen PCO2 waren diese Mechanismen möglicherweise auf Grund der beschränkten Säure-Base-Kompensation und einer Repression des Stoffwechsels abgeschwächt. Die Ergebnisse deuten daher auf einen PCO2-abhängigen Schwellenwert hin, ab welchem eine Kompensation durch Akklimatisation sich durch pH-bedingte Hemmung zunehmend verschlechtert. Da regulatorische Anpassungen nicht auf die transkriptionelle Ebene beschränkt sind, wurde konsequenter Weise im Anschluss eine Translations- (Proteinexpressions-) Analyse durchgeführt. Um etwaige innerartlicher Variationen in der regulatorischen Anpassung zu identifizieren, die sich aus V Zusammenfassung Anpassungen an unterschiedliche Umweltbedingungen in den Lebensräumen ergeben können, wurde die Analyse an zwei Populationen entlang einem latitudinalen Gradienten durchgeführt (Spitzbergen: N 78°58.635'; E 11°29.454' – Schweden: N 58°15.336’; E 11°26.891’). Die Proteinmuster reflektierten dabei in großen Teilen die transkriptomische Antwort. Die Abundanzen der direkt und indirekt mit oxidativem Stress in Verbindung stehenden Proteine deuteten ebenfalls auf einen durch Hyperkapnie initiierten oxidativen Stress hin. Außerdem zeigte sich bei einem mittleren und hohen PCO2 eine steigende Abundanz in Zellstrukturproteinen. Die Ergebnisse bestätigen somit das Zytoskelett als mögliches Hauptziel des oxidativen Stresses. Ein, auf die schwedische Population beschränktes, erhöhtes Vorkommen von Kutikula-Proteinen bei einem mittleren PCO2 deutete auf eine populationsspezifische Variation in der Antwort hin. Bei der für diese Population gewählten erhöhten Versuchstemperatur von 16 °C zeigte sich, im Gegensatz zur Kontrolltemperatur, bei einem hohen PCO2 eine gleichbleibende Kapazität zur pH- Kompensation. Da ein unkompensierter extrazellulärer pH eine Repression des Stoffwechsels zur Folge haben kann, könnte die Fähigkeit zur pH-Regulation den Eintritt in eine solche Repression verschieben. Dies könnte jedoch zu einer weiteren Steigerung des Energiebedarfs führen. In der vorliegenden Arbeit zeichnet sich für die relativ inaktive Crustaceenart Hyas araneus eine limitierte Fähigkeit zur Kompensation der durch Ozeanversauerung mit oder ohne Erwärmung ausgelösten Effekte ab. Die geringe kompensatorische Kapazität, und die möglicherweise
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