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Osmoregulation | with Focus on Fluid and Solute Dynamics in Tardigrada

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Osmoregulation | With Focus on Fluid and Solute Dynamics in Tardigrada PhD Dissertation KENNETH A. HALBERG © Kenneth A. Halberg FACULTY OF SCIENCE UNIVERSITY OF COPENHAGEN Osmoregulation│With Focus on Fluid and Solute Dynamics in Tardigrada PhD Dissertation Kenneth A. Halberg UNIVERSITAS Dissertation submitted Monday the 14th of May 2012. HAFNIENSIS Supervisor: Associate Professor Nadja Møbjerg, PhD. 2012 Dissertation presented at University of Copenhagen to be publicly examined (provided acceptance in its current form) in Auditorium 1, August Krogh Building, Universitetsparken 13, Thursday, June 28, 2012 at 14:00 for the degree of Doctor of Philosophy. The examination will be conducted in English. Abstract Halberg, K. A. 2012. Osmoregulation │With Focus on Fluid and Solute Dynamics in Tardigrada. Osmoregulation is the regulated control of water and solute composition in body fluid compartments. On one hand, the internal composition must be kept within optimal conditions for metabolic processes in the face of external perturbation. On the other hand, the nature of the living state demands a continuous traffic of compounds in and out of the organism. These demands appear to be in fundamental contradiction however cells and animals achieve so-called “steady-state” by means of an array of transport proteins, which provide a stringent control on the exchange of water and solutes across body surfaces. The distinct mechanisms of solute transport have been studied in most animal groups, but there are still large gaps in our understanding of how animals cope with osmotic stress. In the present thesis, osmoregulatory phenomena were studied in vertebrate and invertebrate organism alike, with the main focus being on fluid and solute dynamics in Tardigrada. For example, the inorganic ion composition of several species was investigated, which revealed that tardigrades contain roughly similar relative contributions of inorganic ions to total osmotic concentration, when compared to closely related animal groups. Moreover, it was inferred that cryptobiotic tardigrades (species able to enter a state of latent life) contain a large fraction of organic osmolytes. The mechanisms of organic anion transport in a marine species of tardigrade was investigated pharmacologically, and compared to that of insects. These data showed that organic anion transport is localized to the midgut epithelium and that the transport is both active and transporter mediated with a pharmacological profile similar to that of insects. Tardigrades survive in a variety of osmotic environments (semi-terrestrial, limnic and marine habitats), why the ability to volume and osmoregulate was examined. These studies demonstrated an ability to regulate total body volume during both hypo- and hyperosmotic conditions, and that the ability to hyper-regulate could be a general theme among members of eutardigrades. Thus, the work presented herein, have contributed to establishing tardigrades as an important experimental group in which central physiological questions may be answered, including aspects of osmotic and ionic regulation. Keywords: osmoregulation, volume regulation, organic anion transport, hyper-regulate, inorganic ions, organic osmolytes, tardigrade, insect, Kenneth A. Halberg, The August Krogh Centre, Department of Biology, Universitetsparken 13, DK-2100 Copenhagen Ø, Denmark © Kenneth A. Halberg 2012 “Beautiful is what we see, More beautiful is what we perceive, Most beautiful is what we do not understand” - Niels Stensen List of Papers This thesis is based on the following papers and manuscripts, which are referred to in the text by their Roman numerals. I. Halberg, K. A., Larsen, K. W., Jørgensen, A., Ramløv, H. & Møbjerg, N. Cryptobiotic tardigrades contain large fraction of unidentified organic solutes: A comparative study on inorganic ion composition in Tardigrada. II. Halberg, K. A., & Møbjerg, N. (2012). First evidence of epithelial transport in tardigrades: A comparative investigation of organic anion transport. Journal of Experimental Biology, 215: 497-507. III. Møbjerg, N. M., Halberg, K. A., Jørgensen, A. Persson., D., Bjørn M, Ramløv H & Kristensen R. M. (2011). Survival in extreme environments – on current knowledge of adaptations in tardigrades. Acta Physiologica, 202: 409-420. IV. Haugen, B.M., Halberg, K.A., Jespersen, Å., Prehn, L.R. & Møbjerg, N. (2010). Functional characterization of the vertebrate primary ureter: Structure and ion transport mechanisms of the pronephric duct of axolotl larvae (Amphibia). BMC developmental Biology, 10: 56. V. Halberg, K. A., Persson, D., Ramløv, H., Westh, P., Kristensen, R. M. & Møbjerg, N. (2009). Cyclomorphosis in Tardigrada: Adaption to environmental constraints. Journal of Experimental Biology, 212: 2803-2811. Additionally, the following papers and manuscripts were prepared during the course of my PhD studies, but are not included in the thesis: VI. Halberg K. A., Jørgensen, A. and Møbjerg, N. (in prep.). Surviving without water: Tun formation in tardigrades is an active process mediated by the musculature VII. Halberg K. A., Persson, D., Jørgensen, A. Kristensen, R. M. and Møbjerg, N. (submitted). Population dynamics of a marine tardigrade: Temperature limits geographic distribution of Halobiotus crispae. Marine Biological Research VIII. Persson, D., Halberg K. A., Jørgensen A., Møbjerg N. & Kristensen R. M. (in review). Neuroanatomy of Halobiotus crispae (Eutardigrada: Hypsibiidae): Tardigrade brain structure suggests inclusion into Panarthropoda. Journal of Morphology. IX. Persson, D., Halberg K. A., Jørgensen A., Ricci C., Møbjerg N. & Kristensen R. M. (2010). Extreme stress tolerance in tardigrades: Surviving space conditions in low earth orbit. Journal of Zoological Systematics and Evolutionary Research, 49: 90-97. X. Halberg, K. A., Persson D., Møbjerg N., Wanninger A. & Kristensen R. M. (2009). Myoanatomy of the Marine Tardigrade Halobiotus crispae (Eutardigrada: Hypsibiidae). Journal of Morphology, 270: 996-1013. Lastly, following paper provides important background knowledge for the work presented herein: XI. Møbjerg, N., A. Jørgensen, J. Eibye-Jacobsen, K. A. Halberg, D. Persson & R. M. Kristensen (2007). New Records on cyclomorphosis in the marine eutardigrade Halobiotus crispae (Eutardigrada: Hypsibiidae). Journal of Limnology, 66 (suppl. 1): 132-140. Reprint and publication is made with permission from the respective copyright holders. Paper II, V © The Company of Biologists. Paper IV, is copyright of the authors. Paper III © Wiley-Blackwell Statement of authorship Paper I: KAH was deeply involved in study design. KAH participated in extracting animals and ion chromatography. KAH performed nanoliter osmometry. KAH performed the data analysis, prepared the figures, participated in discussions and interpretation of the data, and drafted the manuscript. Paper II: KAH performed the major part of the experimental work and data analysis. He participated in planning of experiments, data interpretation, prepared the figures and drafted the manuscript. Paper III: KAH performed cell counts and provided images of tardigrades. He helped draft parts of the manuscript. Paper IV: KAH participated in immunostaining experiments, performed CLSM and prepared the 3D images. KAH participated in discussions and interpretation of the data. Paper V: KAH participated in planning of experiments, sampling, staging, scanning electron microscopy, DSC experiments, experiments on cold hardiness and osmotic stress tolerance, volume measurements, hemolymph sample collections, and nanoliter osmometry. He furthermore participated in discussions and interpretation of data, prepared the figures and drafted the manuscript. Front cover: Scanning elecron micrographs of the tardigrades Rictersius coronifer (top left), Halobiotus crispae (middle right), and Echiniscus testudo (middle bottom). Contents Preface.......................................................................................................................... 9 Introduction ................................................................................................................ 11 Maintaining a stable internal environment .......................................................... 11 Osmoregulators and osmoconformers ................................................................. 12 Osmoregulatory organs........................................................................................ 12 Filtration-Reabsorption systems................................................................ 13 Secretion-Reabsorption systems................................................................ 14 Phylum Tardigrada..................................................................................................... 17 General morphology ............................................................................................ 18 Classification ....................................................................................................... 19 Ecology................................................................................................................ 21 Fluid and solute dynamics – an overview .................................................................. 23 Inorganic ion composition ................................................................................... 23 Organic anion transport ....................................................................................... 25 Volume and osmoregulation...............................................................................
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