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U N I V E R S I T Y O F C O P E N H A G E N F A C U L T Y O F S C I E N C E Johannes Wilhelm Goessling Marine Biological Section Department of Biology Biophotonics of diatoms Linking frustule structure to photobiology Biophotonics of diatoms Linking frustule structure to photobiology Biophotonics of diatoms Linking frustule structure to photobiology Johannes W. Goessling Ph.D. thesis Advised by Michael Kühl This PhD thesis has been submitted to the PhD school of Sciences, University of Copenhagen. Herewith I declare that this thesis and the work presented in it are my own and have been generated by me as the result of my own original research. Johannes W. Goessling Copenhagen, 2017 Author: Johannes Wilhelm Goessling, born in Hagen 1984, Germany Title: Biophotonics of diatoms Subtitle: Linking frustule structure to photobiology Academic advisor: Michael Kühl, PhD Full Professor Marine Biological Section University of Copenhagen, Denmark Opponents: Bruno Jesus, PhD Associate Professor Remote Sensing and Benthic Ecology team - MMS University of Nantes Mark Hildebrand, Dr. Full Professor Scripps Institution of Oceanography University of California, San Diego Faculty opponent: Nina Lundholm, PhD Associate Professor, Curator Natural History Museum of Denmark University of Copenhagen For my family Front cover: Silicate valves of different diatom species generate structural colors in dark field microscopy. Valves are fixed on a permanent microscope slide in resin (“Diatom Cubed ®”; RI>1.70). The micrograph was recorded at an angle of 25° incident white light. Collection, decoration and species identification were conducted by Stefano Barone (www.diatomshop.com). Species from top left to bottom right: Surilella testudo ; Surirella utahensis ; Cymbella mexicana ; Diploneis smithii ; Pinnularia viridis ; Navicula oblonga ; Epithemia argus ; Anomoconeis polygramma ; Endyctia oceanica ; Arachnoidiscus sp. ; Triceratium castellatum ; Triceratium favus . ” I think it remarkable that these regular parallelograms are all of the same size, the longest side not exceeds 1/3 of an hairs breadth, and that the length is just double the breadth, the squares being visibly made up of two parallelograms joyn'd longwise. They seem very thin and the texture of every one is nearly the same... I took these branches at first for Salts, but finding them always of the same size, and that there was no sensible increase of their bulk while they continued in the Water, that after they had lain a day or two dry on a Glass Plate they alter'd not their Figure, and upon the addition of new Water (warm or cold) they had still the same appearance and cohesion, and that their adherence (tho touching only in the angular points) was so firm and rigid, that all mov'd together, and kept the same position in respect of one another, however agitated by the Water; these considerations, I say, persuade me, that they may be rather Plants than Salts, but they being so very minute that no judgment can be made of 'em but by the Eye, I shall not determine anything positively.” The first certain record of a diatom communicated by an anonymous English country noblemen to the Philosophical Transactions of the Royal Society of London in 1703 1. He probably described the species Tabellaria floculosa 2 (micrograph on the right side). The light microscopic image was downloaded from http://www.lenaturaliste.net/forum/viewtopic.php?t=9934 (10.05.2017). Abstract Diatoms are unicellular microalgae present in all aquatic environments on earth. Due to their high photosynthetic productivity and abundance, diatoms are main components of aquatic food webs and among the main contributors of global photosynthetic carbon fixation. A unique feature of diatoms is the encasement of the cell in a silicate frustule compounded of two valves and corresponding girdle bands. Photonic structures in the frustule, i.e. pores and chambers on the micro- to nanoscale, interact with electromagnetic radiation in the visible spectrum of light. It has therefore been proposed that the optical properties of frustules could mediate efficient diatom photosynthesis; however, due to lack of optical data of frustules in water and live cells, such links remained purely speculative. The current thesis investigates the potential implications of frustule biophotonics and photobiology also in living diatom cells. We could show that the valve of the centric diatom species Coscinodiscus granii guides light in the horizontal plane, and redistributes photosynthetically productive radiation over the entire cell. Optical coupling of chloroplasts to the evanescent field of the valve induced photosynthesis in areas that were not directly illuminated with a laser beam focused onto the valve surface. The C. granii valve also strongly interacted with blue light which was scattered onto the chloroplasts inside the cell. However, this observation was restricted to an acute angle of light incidence in C. granii , while valves of some benthic diatom species showed similar phenomena at more obtuse-angled incidence. We hypothesized that the angle dependency of such phenomenon can be explained by differences in the light climate where these species live, i.e. sunlight might be incident at more acute angles in habitats close to the water surface, while the light climate is more diffusive inside sediments. Scattering of blue light by the frustules of pennate diatom species compensated for strong attenuation of such shorter wavelengths inside muddy sediment. Hence, variation of frustule photonic structures and optical properties between the species could have shaped niche differentiation of diatoms in habitats with different light climates. Data presented in this thesis also suggest that the different components of the frustule have various optical implications upon the living cell, i.e. we observed that photonic structures in girdle bands of the C. granii frustule have different optical properties than valves, such as iridescent coloration as a function of light incidence. We conclude that the different biophotonic properties of frustules contribute to the high photosynthetic flexibility of diatoms to various light conditions. We speculate that the photonic structures of frustules thereby enabled diatoms to inhabit environments with different light climates, and have hence influenced species diversification and evolution of diatoms. Resumé Kiselalger er unicellulære mikroalger der lever i alle vandmiljøer, er hovedkomponenter i vandmiljøer og nogle af de vigtigste bidragsydere til global fotosyntetisk kulstoffiksering. Photoniske krystalstrukturer kiselalgers i silikat frustule (vægstruktur) interagerer med elektromagnetisk stråling i den synlige den af lysets spektrum, men det er ikke klart hvornår og hvordan de optiske egenskaber hos frustulen påvirker den levende organisme. I denne afhandling er disse potentielle relationer undersøgt med bio-optiske og foto- fysiologiske metoder. Det viste sig i vores undersøgelser at strukturer i frustulen fungerer som en fotonisk waveguide, som kan overføre lysenergi til kloroplaster ved hjælp af optisk kobling. Dette sås for eksempel i at lys, som var fokuseret på et lille område af frustulen med en laser, blev jævnt fordelt i hele cellen gennem effektiv waveguiding, således at fotosyntesen også blev induceret ide kloroplaster, som ikke var direkte oplyst af det indfaldende laserlys. Ved lysdiffraktion på de store porer på indersiden af frustule blev det fotosyntetisk mest aktive blå lys jævnt fordelt over kloroplasterne. I centriske, levende kiselalger blev denne virkning kun observeret når hvidt lys faldt ind i en spids vinkel. Dette kan være af stor betydning ved vandoverfladen, hvor sollyset ofte kommer ind vinkelret og fokuseret. I bentiske, sediment-levende kiselalger er den samme virkning kun synlig ved fladere indfaldsvinkler. Den således inducerede diffraktion af blåt lys modvirker den stærke dæmpning af korte bølgelængder i sedimentet. Mangfoldigheden af nanostrukturer i frustuler og deres underliggende optiske egenskaber kan dermed forklares ved hjælp af niche differentiering; et centralt element i klassisk økologisk teori. Yderligere tyder vores datapå at frustulen har forskellige optiske komponenter med delvist komplementære optiske egenskaber, i.e. frustulens bånd producerer iridescence. Med disse forskellige optiske egenskaber, forårsaget af fotoniske krystalstrukturer, har frustulen en central betydning for kiselalgers fotosyntetiske produktivitet, og bidrager dermed til kiselalgers mangfoldighed og evolutionære succes. Acknowledgements I am deeply grateful for the friendly environment at the Marine Biological Section. It would not have been possible to write this thesis without the open-minded spirit and the manifold scientific possibilities at KU’s Faculty of Science. A heartfelt thank-you to my dear colleagues at KU! My sincere gratitude is owed to my academic advisor Michael Kühl, who has been an inspiration both scientifically and as a group leader. I am deeply obliged to his trust in me and my work, and to his scientific open-mindedness and high flexibility that allowed development of the thesis into a direction not initially planned. His input has significantly improved the current thesis. My utmost respect and admiration is owed to Marianne Ellegaard who has been extremely supportive during my entire work in Copenhagen. The inspiring discussions and free exchange of information has significantly shaped this thesis in its current form. I would like to express my sincere thanks to