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Functional Diversification of Multiple Lungfish Globins

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Functional Diversification of Multiple Lungfish Globins Functional Diversification of Multiple Lungfish Globins Dissertation with the aim of achieving a doctoral degree (Dr. rer. nat.) at the Faculty of Mathematics, Informatics and Natural Science Department of Biology University of Hamburg submitted by Julia Katrin Lüdemann born in Hamburg Hamburg, June 2019 Day of oral defense: 27. September 2019 The following reviewers recommended the admission of the dissertation: Prof. Dr. Susanne Dobler Prof. Dr. Angela Fago Everything that human beings or living animals do is done by protein molecules. And therefore the kind of proteins that one has and therefore the ability one has is determined by the genes that one has. Har Gobind Khorana (1922 – 2011) Molecular Biologist Functional Diversity of Globins Table of Contents Table of Contents Zusammenfassung ................................................................................................................. 8 Abstract ................................................................................................................................ 10 I. Introduction .................................................................................................................. 12 1.1 Hemoglobin ................................................................................................................. 15 1.2 Myoglobin ................................................................................................................... 15 1.3 Neuroglobin ................................................................................................................. 17 1.4 Cytoglobin ................................................................................................................... 19 1.5 Globin E ....................................................................................................................... 20 1.6 Globin Y ....................................................................................................................... 20 1.7 Globin X ....................................................................................................................... 21 1.8 Androglobin ................................................................................................................. 21 1.9 Evolution of globins ..................................................................................................... 22 1.10 Lungfish ..................................................................................................................... 25 1.10.1 Aestivation .............................................................................................................. 27 1.11 Multiple globins in lungfish ........................................................................................ 28 1.12 Aim of the thesis ........................................................................................................ 30 II. Chapter 1: ...................................................................................................................... 31 Unusual diversity of myoglobin genes in the lungfish ............................................................ 31 2.1 Abstract....................................................................................................................... 32 2.2 Introduction ................................................................................................................. 33 2.3 Results ......................................................................................................................... 35 2.3.1 An unexpected diversity of myoglobins in P. annectens .......................................... 35 2.3.2 Early emergence and fast evolution of lungfish myoglobins .................................... 35 2.3.3 Differential, tissue-specific expression of lungfish myoglobins ................................ 36 2.3.4 Lungfish myoglobins protect cultured cells from hypoxia and reduce ROS production ......................................................................................................................... 38 2.4 Discussion .................................................................................................................... 39 2.4.1 Ancient and specific amplification of myoglobin genes ........................................... 39 2.4.2 High myoglobin concentrations may protect the lungfish brain from hypoxia during aestivation ......................................................................................................................... 40 2.4.3 Different myoglobins with distinct roles in skeletal muscle and heart ..................... 41 4 Functional Diversity of Globins Table of Contents 2.4.4 Conclusion: Myoglobin diversity in lungfish as an example for the functional diversification of globin genes ........................................................................................... 43 2.5 Materials and Methods ................................................................................................ 43 2.5.1 Transcriptome and database analyses ..................................................................... 43 2.5.2 Phylogenetic analyses............................................................................................... 44 2.5.3 Tissue preparation, RNA extraction cDNA cloning ................................................... 45 2.5.4 Quantitative real-time reverse transcription PCR .................................................... 45 2.5.5 Analyses of myoglobin proteins ............................................................................... 46 2.5.6 Cell culture experiments .......................................................................................... 47 2.6 Acknowledgments ....................................................................................................... 47 III. Chapter 2: ...................................................................................................................... 49 Genetic and functional diversity of the multiple lungfish myoglobins .................................... 49 3.1 Abstract....................................................................................................................... 50 3.2 Introduction ................................................................................................................. 51 3.3 Material and Methods ................................................................................................. 53 3.3.1 Identification and analyses of lungfish Mb cDNA sequences ................................... 53 3.3.2 Recombinant expression and purification of P. annectens Mbs .............................. 55 3.3.3 O2 equilibrium measurements ................................................................................. 55 3.3.4 Gel-filtration experiments ........................................................................................ 56 3.3.5 Nitrite reductase activity .......................................................................................... 56 3.3.6 Dynamic light scattering (DLS) .................................................................................. 57 3.3.7 Circular dichroism (CD) spectroscopy ....................................................................... 57 3.3.8 Small-angle X-ray scattering (SAXS) .......................................................................... 57 3.4 Results ......................................................................................................................... 58 3.4.1 Identification of myoglobin cDNA in four lungfish species ....................................... 58 3.4.2 O2 equilibria of P. annectens myoglobins ................................................................. 59 3.4.3 Enzymatic activities of P. annectens myoglobins ..................................................... 60 3.4.4 Structural analyses of P. annectens myoglobins ....................................................... 61 3.5 Discussion .................................................................................................................... 63 3.5.1 Emergence of multiple myoglobins as a possible adaptation of lungfish ................. 63 3.5.2 Conserved structure of P. annectens myoglobins .................................................... 65 3.5.3 Functional differentiation of P. annectens myoglobins ............................................ 66 3.5.4 Functional differentiation of lungfish myoglobin in evolution ................................. 66 5 Functional Diversity of Globins Table of Contents 3.6 Acknowledgements ...................................................................................................... 67 IV. Chapter 3: ...................................................................................................................... 68 Globin E is a myoglobin-related, respiratory protein highly expressed in lungfish oocytes ..... 68 4.1 Abstract....................................................................................................................... 69 4.2 Introduction ................................................................................................................. 69 4.3 Results ......................................................................................................................... 71 4.3.1 Identification of GbE genes in lungfish species ........................................................ 71 4.3.2 Conservation and lungfish-specific amplification
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