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Morphological Studies of the Dinoflagellate Karenia Papilionacea in Culture

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Morphological Studies of the Dinoflagellate Karenia Papilionacea in Culture MORPHOLOGICAL STUDIES OF THE DINOFLAGELLATE KARENIA PAPILIONACEA IN CULTURE Michelle R. Stuart A Thesis Submitted to the University of North Carolina Wilmington in Partial Fulfillment of the Requirements for the Degree of Master of Science Department of Biology and Marine Biology University of North Carolina Wilmington 2011 Approved by Advisory Committee Alison R. Taylor Richard M. Dillaman Carmelo R. Tomas Chair Accepted by __________________________ Dean, Graduate School This thesis has been prepared in the style and format consistent with the journal Journal of Phycology ii TABLE OF CONTENTS ABSTRACT ................................................................................................................................... iv ACKNOWLEDGMENTS .............................................................................................................. v DEDICATION ............................................................................................................................... vi LIST OF TABLES ........................................................................................................................ vii LIST OF FIGURES ..................................................................................................................... viii INTRODUCTION .......................................................................................................................... 1 MATERIALS AND METHODS .................................................................................................... 5 RESULTS ....................................................................................................................................... 9 DISCUSSION ............................................................................................................................... 14 LITERATURE CITED ................................................................................................................. 22 TABLES ....................................................................................................................................... 26 FIGURES ...................................................................................................................................... 28 APPENDIX .................................................................................................................................. 36 iii ABSTRACT Various morphologies of the unarmored dinoflagellate Karenia papilionacea were observed in culture and some forms could easily be mistaken for other toxic species. Using DIC, epifluorescent microscopy and DAPI staining for nuclear DNA, three morphologies were defined in detail, those being a wider than tall butterfly-shape, a wide as tall brevis-shape, and a round spherical shape. The first hypothesis examined was that K. papilionacea develops a K. brevis- like form that can be confused with known toxic species found in the Gulf of Mexico. Morphological analysis revealed that while the especially wide, clearly butterfly- like cells do occur, the majority of the population was actually very similar in appearance to K. brevis. The second hypothesis was that brevis-shaped cells, as well as other morphologies such as spherical cyst-like cells, represent sexually induced reproductive stages in the K. papilionacea life cycle and therefore would display different DNA contents. There was no statistical difference between the DNA content of brevis-shaped and butterfly-shaped cells supporting the notion that both morphologies represent a natural variation of size with the same ploidy. The third hypothesis was that the butterfly-shaped form was the dominant haploid stage. The majority of K. papilionacea cells observed in culture were not the extremely broad butterfly form that was proposed as the classic representative of this species. These findings emphasize the need for a combination of morphological and molecular evidence when identifying cells in environmental samples. Also, evidence supporting the existence of a pellicle cyst could lead to insight into the bloom dynamics of K. papilionacea. iv ACKNOWLEDGEMENTS I am deeply grateful to Carmelo Tomas, Alison Taylor, and Richard Dillaman for inspiration, as well as intellectual and moral support. I sincerely thank Brooke Stuerke, Bob York, Erika Schwarz, Harris Muhlstein, Tara Haney and Kendra Coles for being such great lab mates and partners in brainstorming. I am grateful to Tyler Cyronak for his generous assistance with flow cytometry. I dearly appreciate all of my friends and family who supported me through this endeavor and helped me to laugh when it was needed. I would also like to thank the Graduate School and MARBIONC for funding this project. v DEDICATION For Dale Trimble and Jackie Prinz. vi LIST OF TABLES Table Page 1. A summary of descriptive statistical values for the three morphological classifications of Karenia papilionacea. ........................................................................... 26 2. The DNA content in cultured dinoflagellates from non-Symbiodinium genera ............... 27 vii LIST OF FIGURES Figure Page 1. Growth curve of Karenia papilionacea Kp0707-1 including cell morphologies of A) log phase; B) stationary phase; C) decline phase. ....................................................... 28 2. Frequency distribution of width to height ratios of Karenia papilionacea ...................... 29 3. Differential interference contrast images of Karenia papilionacea morphologies in culture; A) log phase butterfly-shaped cell; B) stationary phase butterfly-shaped cell; C) log phase brevis-shaped cell; D) stationary phase brevis-shaped cell; E) stationary phase spherical cell. Scale bar = 20 µm ........................................................... 30 4. Variation within the morphology classifications of Karenia papilionacea: A) butterfly-shaped cells; B) brevis-shaped cells; C) cells losing morphology to become spherical. Nuclei are stained blue with DAPI and viewed with epifluorescent microscopy. Scale bar = 20 µm ................................................................ 31 5. Epifluorescent images of DAPI stained nuclei of Karenia papilionacea progressing through mitosis: A) pre-mitotic nucleus; B) chromosomes beginning to move toward poles; C) nucleus is beginning to take on a hourglass shape; D) hourglass shape has formed with distinct outlines of the two future nuclei; E) two nuclei are evident joined by a small amount of chromatin; F) two nuclei have moved to poles of daughter cells. Scale bar = 20 µm. ...................................................... 32 6. Differential interference contrast images of Karenia papilionacea undergoing cytokinesis: A) the two daughter nuclei are located in separate lobes of the hypotheca; B) the cleft between lobes of the hypotheca deepens; C) additional lobes form; D) cytokinetic cell appears as two mature cells, attached at a midpoint; E) the final point of attachment at the apical tip. Nuclei are stained blue with DAPI. Scale bar = 20 µm ......................................................................................... 33 7. Frequency distribution of DNA content in picograms per cell (pg · cell-1) for all cells analyzed. ................................................................................................................... 34 8. Frequency distribution of DNA content (pg · cell-1) of Karenia papilionacea in A) butterfly-shaped cells; B) brevis-shaped cells, and C) spherical cells .............................. 35 viii INTRODUCTION Dinoflagellates are a large component of primary producers and are estimated to make up about 40% of the total species of marine phytoplankton (Simon et al. 2009). They are key components in food webs, nutrient cycling and the conversion of carbon dioxide to oxygen in ocean systems. A typical dinoflagellate life cycle consists of a motile, haploid (Pfeister and Anderson, 1987), asexually reproductive cell that undergoes mitosis regularly (Dale 1986). Sometimes these asexual cells form pellicle cysts (formerly referred to as temporary cysts, see Bravo et al. 2010) to survive an environmental change. An environmental or internal cue elicits vegetative cells to initiate sexual reproduction by forming haploid homothallic or heterothallic gametes that fuse to form motile, diploid planozygotes, distinguishable by the presence of two longitudinal flagella. The planozygote will undergo reductive division (meiosis) to form planktonic vegetative cells or it will lose motility by absorbing the flagella and undergoing cellular reorganization to form a resting cyst called a hypnozygote. Resting cysts are defined as cells having double walls and a mandatory dormancy period (Bravo et al. 2010). The hypnozygote has the potential to excyst releasing a diploid planomeiocyte that has two longitudinal flagella. Meiosis of the planomeiocyte produces haploid vegetative cells and the cycle continues. Ecologically these cysts have a function as vegetative propagules and can release motile cells under favorable conditions to reestablish motile populations in the water column. Cysts are thus used as indicators of previous blooms, as a potential for forming motile populations and as a means of disseminating a population to new areas. With both motile and resting (cyst) stages, dinoflagellates express a variety of morphologies, making detailed morphological and molecular studies essential in the accurate identification of the bloom formers. Relatively few (~ 2%) dinoflagellates are known to
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