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Making Sense of Protists -Aspects of Phototaxis and Chemo Sensory Behavior

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Making Sense of Protists -Aspects of Phototaxis and Chemo Sensory Behavior FACULTY OF SCIENCE UNIVERSITY OF COPENHAGEN PhD thesis Morten Moldrup Making Sense of Protists -aspects of phototaxis and chemo sensory behavior Academic advisor: Assosciate Professor Per Juel Hansen Submitted: 06/07/10 "Anyone who has never made a mistake has never tried anything new." Albert Einstein Contents Supervisor and committee 3 Papers and manuscripts included 3 Preface 4 Summary 5 Sammenfatning (Danish summary) 7 Introduction 9 Part 1 10 Part 2 12 Part 3 15 Conclusion and perspectives 16 References 18 Paper I Paper II Paper III Paper IV Paper V 2 Committee Chairman: Marianne Ellegaard, Evolution and Ecology of Aquatic Organisms. University of Copenhagen, Denmark Eric Warrant, Cell and Organism Biology, Lund University, Sweden Urban Tillmann, Alfred Wegener Institute for Polar and Marine Research, Germany Papers and manuscripts included Paper I Moldrup M, Moestrup Ø and Hansen PJ. Loss of phototaxis and degeneration of an eyespot in long term algal cultures: evidence from ultrastructure and behavior in the dinoflagellate Kryptoperidinium foliaceum. (draft manuscript) Paper II Moldrup M, Garm A. “Spectral sensitivity of the dinoflagellate Kryptoperidinium foliaceum and their reaction to physical encounters”. (draft manuscript) Paper III Poulsen LK, Moldrup M, Berge T, Hansen PJ. “Grazing of Copepod fecal pellets by dinoflagellates –a new trophic role as detritivores”. (draft manuscript) Paper IV Berge T, Poulsen LK, Moldrup M, Hansen PJ. “Bloom-forming marine microalga kills and eats copepods and other metazoans”. (draft manuscript) Paper V Hansen PJ, Moldrup M, Tarangkoon, W, Garcia, L, Daugbjerg, N, Moestrup, Ø. “Does the marine red tide ciliate Mesodinium rubrum have replaceable symbionts?” (draft manuscript) 3 Preface This thesis is written as part of the requirements for a Danish PhD degree from Department of Biology, Faculty of Science, University of Copenhagen, Denmark. I was based at the Marine Biological Laboratory (now MBS) in Helsingør funded by the Faculty of Science, University of Copenhagen. During my time as a PhD student I was associated with the PhD School of Science. During my years at MBL in my advisor Per Juel Hansen lab I have always appreciated that if you had a good idea you were always ushered to do it rather than talk about it. This has made my stay here playful and maturing. Of course I also have to acknowledge his credo “focus”, it certainly did me some good at times. It has been a pleasure and a privilege and I owe Per heartfelt thanks. I also like to thank my collaborator and at times advisor Anders Garm for his unending optimism. Many times I have been frustrated about various projects and then, for one reason or the other, had to see Anders, I always have come back to MBL with a new zest for the projects. Øjvind Moestrup deserves thanks for taking the time to teach me TEM. My co-workers on the manuscripts also deserves thank. They are: Lydia Garcia, Woraporn Tarangkoon, Terje Berge, Louise K Poulsen. Especially you Louise for being the best lab-partner ever! All the student in and out of Per’s lab also deserve thanks for a great atmosphere: Karen, Rasmus, Bettina, Lasse, Hannah and Nikolaj. Bent Vismann also needs to be acknowledged for making and drinking the worst coffee you will ever see. Minor details such as his ongoing (and never ending probably) PhD course on the inner workings and governance of university and sharp eye on experimental data may also need to be thanked. I have thoroughly enjoyed drinking my morning coffee with you and I will miss it! I had the privilege of working in Jens Høeg’s lab for a couple of months and for enduring algae in his lab he deserves huge thanks. I also owe Hans Henrik Jakobsen huge thanks for taking the time to help me and for taking me on a Cruise with R/V Dana. The Captain and crew of which also deserve thanks, especially the kitchen gang. I owe want to thank Professor Dan-Eric Nilsson who has been a partner in this project all along Unfortunately did out projects not work at all but I learned so much from you the few times we were working together. The Staff and Students at MBL also deserve thanks for making my stay here very nice indeed. My beloved M-L and the kid deserve loving thanks for the support and especially for enduring my mental absense throughout the completion of this dissertation. Helsingør June 2010 Morten Moldrup 4 Summary Phototaxis provides phytoplankton with the means to orient themselves in a light gradient. This is accomplished using an eyespot and associated organelles. For the dinoflagellate Kryptoperidinium foliaceum, which has been described as having one of the most elaborate eyespot complexes known, positive phototaxis has hitherto not been reported. In this study we show that a newly isolated strain of K. foliaceum is indeed capable of positive phototaxis with a mean vector (±95% CI) of 352°±2.2° where 0/360° indicate the direction of the light source. A study of three strains (UTEX1688, CCMP and MBL07) of Kryptoperidinium foliaceum, showed that the eyespot in two of these strains have degenerated following decades in culture. Thus, previous studies have failed to report positive phototaxis due to loss of directionality caused by the degenerated eyespot. The results are discussed in a broader context; and we conclude that studies on algal morphology and physiology may result in erroneous conclusions if based on algal cultures maintained under laboratory conditions for extended periods. Until recently it not believed to be phototactic and its spectral sensitivity therefore remains unstudied. We find the dynamic range of phototaxis to be ~2 log units. Additionally, we find indications that the spectral sensitivity behind the phototaxis is based on a single opsin with peak sensitivity around 500 nm. The spectral sensitivity agrees reasonably well with the absorption curve of a theoretical opsin. This is maintained although the expected peak in the near UV range is missing probably due to some sort of shading/filtering of harmful UV radiation. Interestingly, the phototaxis could be temporarily overruled by tactile stimuli. After physical contact with the light guide the cells escaped the area. They may do this as some sort of predator avoidance. Field studies have indicated that dinoflagellates are key degraders of copepod fecal pellets in the sea, however, direct evidence of pellet feeding by dinoflagellates have not been published prior to this study. Feeding and growth of dinoflagellates on copepod fecal pellets was studied for 3 species of mixotrophic dinoflagellates and 4 species of heterotrophic dinoflagellates using a combination of video recordings of feeding behavior and classic incubation experiments. Fecal pellets offered were produced by adult Acartia tonsa on Rhodomonas salina as a food source. One out of 3 mixotrophic species (Karlodinium armiger) and 4 out of the 6 the heterotrophic dinoflagellates (Gyrodinium dominans, G. spirale, Diplopsalis lenticula, Protoperidinium depressum) studied fed on fecal pellets. Using natural concentrations of dinoflagellates and copepod fecal pellets, ingestion rates of 0.21 and 0.11 pellets cell-1 d-1 and clearance rates of between 0.21 and 0.32 ml cell-1 d-1 were obtained for Gyrodinium spirale and Protoperidinium depressum, respectively. Pellet feeding resulted in growth rates of 0.69 and 0.08 d-1 with a growth yield of 0.58 and 0.50, for the Gyrodinium spirale and Protoperidinium depressum, respectively. The main determining factors for the grazing impact of the dinoflagellates on fecal pellets were the dinoflagellate to pellet size ratio in combination with the feeding mechanism employed by the dinoflagellate species, pellet age, and pellet concentration. This study reveals a new trophic role for dinoflagellates as detritivores, which provides a less energy consuming pathway for recycling of pellet material than the several trophic levels which are transversed through the microbial loop; and proves that dinoflagellates can function as an effective “protozoan filter” for fecal pellets in the water column. The photosynthetic dinoflagellate Karlodinium is known to form massive blooms worldwide and often these are associated with fish kills. Here we show that Karlodinum armiger can reverse the traditional trophic pathway from primary producers to copepods, by attacking, immobilizing and engulfing the much larger metazoan grazers. Copepod immobilisation is fast but dependent on cell density of K. armiger, suggesting the presence of a potent paralytic toxin. Karlodinium armiger 5 immobilises copepods by direct cell-contact, before ingesting parts of the copepod through a feeding tube. The common copepod Acartia tonsa was immobilised within a few hours and died 12 hours after exposure to ecologically relevant bloom cell densities in the laboratory. Karlodinium armiger increases its growth rate when exposed to copepods and most cells contain large visible food vacuoles following engulfment. Our results show a novel trophic pathway at the base of planktonic food web which reverses the typical flux of organic matter. Behavioural observations of K. armiger have also revealed a novel mechanism for faunal kills by this phototrophic microalga. The red tide ciliate Mesodinium rubrum (=Myrionecta rubra) is known to contain a symbiont of cryptophyte origin. Molecular data have shown that the symbiont is very closely related or similar to free-living species belonging to the “Teleaulax clade”. This suggests that the symbiont of M. rubrum is either a temporary symbiont or a quite recently established symbiont. Here we present data from a number of experiments in which we tried to replace the symbionts in M. rubrum by supplying a number of different cryptophyte species belonging to different cryptophyte clades. Growth and ingestion rates of M. rubrum fed these cryptophytes were measured. In addition, cells of M. rubrum were analyzed for type of chloroplast using transmission electron microscopy and DNA sequences of the nucleomorph LSU.
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