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Directed Motility of Benthic Diatoms

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Directed Motility of Benthic Diatoms DIRECTED MOTILITY OF BENTHIC DIATOMS DISSERTATION (KUMULATIV) zur Erlangung des akademischen Grades doctor rerum naturalium (Dr. rer. nat.) vorgelegt dem Rat der Chemisch-Geowissenschaftlichen Fakultät der Friedrich-Schiller-Universität Jena von Diplom-Chemikerin von M.Sc. (Marine Science) Karen Grace V. Bondoc geboren am 03.06.1988 in Amulung, Cagayan, Philippinen Dissertation, Friedrich-Schiller-Universität Jena [2017] Gutachter: 1. Prof. Dr. Georg Pohnert, Friedrich-Schiller-Universität Jena 2. Prof. Dr. Wilhelm Boland, Friedrich-Schiller-Universität Jena 3. Prof. Dr. Knut Drescher, Philipps-Universität Marburg Tag der Verteidigung: 14 Dec 2017 For the One who created the oceans. “But I don’t want to go among mad people," Alice remarked. "Oh, you can’t help that," said the Cat: "we’re all mad here. I’m mad. You’re mad." "How do you know I’m mad?" said Alice. "You must be," said the Cat, "or you wouldn’t have come here.” ― Lewis Carroll, Alice in Wonderland Table of Contents V TABLE OF CONTENTS TABLE OF CONTENTS ............................................................................................................................................. V SUMMARY ............................................................................................................................................................ VII ZUSAMMENFASSUNG ............................................................................................................................................ XI ABBREVIATIONS ................................................................................................................................................. XV LIST OF FIGURES ................................................................................................................................................ XVI 1 INTRODUCTION ............................................................................................................................................. 1 1.1 Characteristics and ecology of diatoms ............................................................................................... 1 1.1.1 Motility ............................................................................................................................................... 2 1.1.2 Reproduction ................................................................................................................................... 4 1.2 Diatom biofilms: success in patchiness ............................................................................................... 6 1.3 From small-scale to large-scale processes: Bigger impacts of behaviour .......................... 11 1.3.1 Behaviour ....................................................................................................................................... 11 1.3.2 Investigations in motility ......................................................................................................... 12 2 SCOPE OF THE STUDY ................................................................................................................................ 17 3 PUBLICATIONS ........................................................................................................................................... 19 3.1 Publication A ................................................................................................................................................ 19 3.2 Publication B ................................................................................................................................................ 37 3.3 Publication C ................................................................................................................................................ 51 4 DISCUSSION AND FUTURE PERSPECTIVES ............................................................................................... 99 4.1 Nutrient attraction across the life cycle ........................................................................................... 99 4.1.1 Nutrient starvation and recovery....................................................................................... 100 4.1.2 Behavioural response to nutrient starvation ................................................................ 102 4.1.3 Nutrient uptake enhanced by motility ............................................................................. 104 4.2 Pheromone-mediated chemoattraction of sexual cells ............................................................ 105 4.3 Sensing mechanisms: How do diatoms find chemical signals? ............................................. 108 4.4 Prioritization mechanisms: Food vs. sex on sexually-available diatoms .......................... 108 4.5 Implications of directed motility – evolutionary aspects and ecological cascades ...... 110 4.6 Future perspectives ................................................................................................................................ 112 5 REFERENCES ............................................................................................................................................. 115 6 DECLARATIONS ........................................................................................................................................ 125 VI Table of Contents Selbstständigkeitserklärung ......................................................................................................................... 125 Weitere Erklärungen ....................................................................................................................................... 125 Einverständniserklärung des Betreuers .................................................................................................. 126 AFTERWORD..................................................................................................................................................... 127 Summary VII SUMMARY Diatoms are a group of highly diverse microalgae dominating aquatic systems and contributing to a quarter of the global primary production. They have a unique morphology including a biomineralized silicate-based cell wall. This rigid cell wall leads to cell size reduction during mitosis followed by size restoration through sexual reproduction. In intertidal sediments, they significantly contribute to microphytobenthic biofilm communities, thereby playing an important role in ecosystem functioning. A biofilm is a complex and dynamic environment where growth and reproduction are under the control of signal molecules and nutrient resources. As diatoms are key players for biogeochemical cycling, collective behaviour and interactions can create a cascade of events with global-scale consequences. I used the model pennate diatom Seminavis robusta to determine how benthic diatoms forage for nutrients and locate their mating partners. Like most pennate diatoms, S. robusta moves by gliding back-and-forth across surfaces through excretion of extrapolymeric substances (EPS) from the raphe, a slit on its cell wall. The sexual phase of this microalga is pheromone-mediated, with both mating types (MT+ and MT-) secreting sex-inducing pheromones (SIP+ and SIP-, respectively) as priming signals for each other once they reach sexual size threshold (SST). MT- cells then produce the attraction pheromone diproline for chemoattraction of MT+. Hotspot sources of stimuli were mimicked using specific beads that adsorb dissolved nutrients or the pheromone diproline. Upon medium contact, beads release the stimuli, forming a diffusion gradient. A combination of video monitoring, trajectory analysis, and statistical modelling was utilized to determine how nutrient-starved or sexually-induced cells responded to the signal gradients formed. As cells in both vegetative and sexual phases of S. robusta were used for the attraction assays, this study is the first to provide comprehensive knowledge on a microorganism’s behavioural motility across its life cycle. I tested the responses of diatoms to the macronutrients dissolved silicate (dSi), phosphate (dP), and nitrate and ammonium (dN). Foraging cells were attracted to dSi and dP, but not to any form of dN. Cells accumulated around the nutrient-loaded bead within ~5 min for dSi and ~20 min for dP, respectively, while control beads did not elicit attraction. The observed dSi response was universal, as no inter- and the intra-specific difference in reaction of different strains of S. robusta, as well as of another pennate diatom, Navicula sp. was found. Additionally, the dSi response was substrate-specific, as gradients of germanium dioxide (dGe), which have comparable chemical characteristics as dSi, elicited a negative response. Since dSi elicited the fastest response among the tested nutrients, I verified the differential behaviour of large-sized vegetative cells (>50 µm) and cells of two sexual sizes VIII Summary below the sexual size threshold (SST): medium- (~40 µm) and critically small-sized (24-27 µm) cells. No variability in the response towards dSi was observed, albeit, large-sized cells required a longer starvation time. Foraging cells utilized a simultaneous tactic and kinetic approach in locating nutrient resources. Changes in the gliding behaviour enable the cells to locate the stimulus and maximize their encounter rate with it. Overall, the fine tuning of motility parameters while foraging increased nutrient uptake up to 170-fold, which may circumvent severe limitation scenarios in the benthic
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