pH regulatory systems of marine larvae: new models for gastro-intestinal health and biomineralization in a changing environment
Final Report Abstract
In this project I employed the sea urchin larva, a highly tractable model system that can work from the whole animal level to specific manipulations of the genetic material, to investigate pH regulatory systems relevant for gastro-intestinal-health and biomineralization of the larval skeleton. In the frame of this fife year program my group made exiting new discoveries in the different parts of this project. The first objective addressed the epithelial transport mechanisms that regulate the ionic and pH homeostasis of the midgut. We were able to identify some of the major ion transporters that are responsible to maintain these specific conditions in the larval midgut. Exposure to acidified conditions as predicted for the near future in the frame of the ongoing global change phenomenon ocean acidification (OA) led to a partial reduction in midgut pH that was however compensated by increased ion transport activity to defend midgut homeostasis. This for the first time identified a physiological process that explains a shift in the animal´s energy budget towards compensatory processes leaving less energy for growth and development- a commonly observed phenomenon when organisms are raised under OA conditions. Interestingly, this compensatory reaction was particularly strong when larvae were exposed to a marine pathogen in combination with decreased seawater pH. This finding of the second objective addressing the role of midgut pH as a first line of defense against environmental pathogens confirmed our initial hypothesis that alkaline conditions help to regulate a healthy gut microbiome. Furthermore, we could show that a pharmacological reduction in midgut pH substantially increases the susceptibility of the organisms to a marine pathogen. The third objective, addressed the cellular mechanisms that marine organisms use to generate mineralized shells and skeletons. This part has led to new fundamental discoveries in the cellular physiology of calcifying systems. We identified a proton channel that allows protons that are produced by the mineralization process to exit the cell. However, such a mechanism requires very stable pH conditions and may represent the Achilles heel of marine calcifiers to OA. Furthermore, this project identified a carbon concentration mechanisms in calcifying cells of the sea urchin larva that utilize metabolic CO2 to generate its calcitic skeletons. This project allowed me to develop and consolidate my scientific profile over the course of five years. Based on these findings, in particular the cellular mechanisms of mineralization I was able to generate new scientific venues for future research directions.
Publications
-
Boron isotope systematics of cultured brachiopods: Response to acidification, vital effects and implications for palaeo-pH reconstruction. Geochimica et Cosmochimica Acta, 248, 370-386.
Jurikova, Hana; Liebetrau, Volker; Gutjahr, Marcus; Rollion-Bard, Claire; Hu, Marian Y.; Krause, Stefan; Henkel, Daniela; Hiebenthal, Claas; Schmidt, Mark; Laudien, Jürgen & Eisenhauer, Anton
-
Electrophysiological evidence for light-activated cation transport in calcifying corals. Proceedings of the Royal Society B: Biological Sciences, 286(1896), 20182444.
Taubner, Isabelle; Hu, Marian Y.; Eisenhauer, Anton & Bleich, Markus
-
Full in vivo characterization of carbonate chemistry at the site of calcification in corals. Science Advances, 5(1).
Sevilgen, Duygu S.; Venn, Alexander A.; Hu, Marian Y.; Tambutté, Eric; de Beer, Dirk; Planas-Bielsa, Víctor & Tambutté, Sylvie
-
Measurement of feeding rates, respiration, and pH regulatory processes in the light of ocean acidification research. Methods in Cell Biology, 391-409. Elsevier.
Stumpp, Meike; Dupont, Sam & Hu, Marian Y.
-
Tipping points of gastric pH regulation and energetics in the sea urchin larva exposed to CO2 -induced seawater acidification. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 234, 87-97.
Lee, Hae-Gyeong; Stumpp, Meike; Yan, Jia-Jiun; Tseng, Yung-Che; Heinzel, Sebastian & Hu, Marian Yong-An
-
Active ion transport mechanisms and their role for past, present and future life in marine systems. Journal of the Marine Biological Association of the United Kingdom, 100(3), 331-332.
Hu, Marian Y.
-
Alkaline guts contribute to immunity during exposure to acidified seawater in the sea urchin larva. Journal of Experimental Biology.
Stumpp, Meike; Petersen, Inga; Thoben, Femke; Yan, Jia-Jiun; Leippe, Matthias & Hu, Marian Y.
-
Cellular bicarbonate accumulation and vesicular proton transport promote calcification in the sea urchin larva. Proceedings of the Royal Society B: Biological Sciences, 287, 20201506.
Hu, Marian Y.; Petersen, Inga; Chang, William Weijen; Blurton, Christine & Stumpp, Meike
-
Energy and nitrogenous waste from glutamate/glutamine catabolism facilitates acute osmotic adjustment in non-neuroectodermal branchial cells. Scientific Reports, 10(1).
Huang, Pei-Chen; Liu, Tzu-Yen; Hu, Marian Y.; Casties, Isabel & Tseng, Yung-Che
-
Intracellular pH regulation in mantle epithelial cells of the Pacific oyster, Crassostrea gigas. Journal of Comparative Physiology B, 190(6), 691-700.
Ramesh, Kirti; Hu, Marian Y.; Melzner, Frank; Bleich, Markus & Himmerkus, Nina
-
Skeletal integrity of a marine keystone predator (Asterias rubens) threatened by ocean acidification. Journal of Experimental Marine Biology and Ecology, 526, 151335.
Di Giglio, Sarah; Lein, Etienne; Hu, Marian Y.; Stumpp, Meike; Melzner, Frank; Malet, Loïc; Pernet, Philippe & Dubois, Philippe
-
An otopetrin family proton channel promotes cellular acid efflux critical for biomineralization in a marine calcifier. Proceedings of the National Academy of Sciences, 118(30).
Chang, William W.; Matt, Ann-Sophie; Schewe, Marcus; Musinszki, Marianne; Grüssel, Sandra; Brandenburg, Jonas; Garfield, David; Bleich, Markus; Baukrowitz, Thomas & Hu, Marian Y.
-
Na+/H+ exchangers differentially contribute to midgut fluid sodium and proton concentration in the sea urchin larva. Journal of Experimental Biology, 224(7).
Petersen, Inga; Chang, William W. J. & Hu, Marian Y.
-
Extracellular carbonic anhydrase activity promotes a carbon concentration mechanism in metazoan calcifying cells. Proceedings of the National Academy of Sciences, 119(40).
Matt, Ann-Sophie; Chang, William W. & Hu, Marian Y.
-
Cellular mechanisms underlying extraordinary sulfide tolerance in a crustacean holobiont from hydrothermal vents. Proceedings of the Royal Society B: Biological Sciences, 290(1990).
Chou, Pei-Hsuan; Hu, Marian Y.; Guh, Ying-Jey; Wu, Guan-Chung; Yang, Shan-Hua; Tandon, Kshitij; Shao, Yi-Ta; Lin, Li-Yih; Chen, Chi; Tseng, Kuang-Yu; Wang, Min-Chen; Zhang, Cheng-Mao; Han, Bor-Cheng; Lin, Ching-Chun; Tang, Sen-Lin; Jeng, Ming-Shiou; Chang, Ching-Fong & Tseng, Yung-Che
-
Characterization of digestive proteases in the gut of a basal deuterostome. Journal of Experimental Biology, 226(15).
Hildebrand, Jasper; Chang, William W.; Hu, Marian Y. & Stumpp, Meike
-
Soluble adenylyl cyclase coordinates intracellular pH homeostasis and biomineralization in calcifying cells of a marine animal. American Journal of Physiology-Cell Physiology, 324(3), C777-C786.
Chang, William Weijen; Thies, Angus B.; Tresguerres, Martin & Hu, Marian Y.
-
Surviving in an Acidifying Ocean: Acid-Base Physiology and Energetics of the Sea Urchin Larva. Physiology, 38(5), 242-252.
Hu, Marian Y. & Stumpp, Meike
