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The Role of Nitrogen Availability on the Dominance of Planktothrix Agardhii in Sandusky Bay, Lake Erie

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The Role of Nitrogen Availability on the Dominance of Planktothrix Agardhii in Sandusky Bay, Lake Erie THE ROLE OF NITROGEN AVAILABILITY ON THE DOMINANCE OF PLANKTOTHRIX AGARDHII IN SANDUSKY BAY, LAKE ERIE Daniel H. Peck A Thesis Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE August 2020 Committee: George Bullerjahn, Advisor Timothy Davis Robert McKay © 2020 Daniel H. Peck All Rights Reserved iii ABSTRACT George S. Bullerjahn, Advisor Sandusky Bay and Lake Erie are plagued with harmful algal blooms every summer. Sandusky Bay is a drowned river mouth that is very shallow and turbid and is dominated by Planktothrix agardhii, while Lake Erie is dominated by Microcystis aeruginosa. Both species of cyanobacterium are non-diazotrophic and produce microcystin, a hepatotoxin. A competition experiment was conducted culturing both species alone and in coculture at nitrogen (nitrate) replete, nitrate restricted, and nitrogen-free environments. Planktothrix grew better alone at nitrogen restricted medium than in co-culture with Microcystis. In coculture, Microcystis was dominant over Planktothrix however, that dominance decreased as nitrogen was reduced in each treatment. In the nitrogen replete environment, the coculture produced significantly more toxin than the monocultures and in the no nitrogen environment the Planktothrix monoculture produced more toxin than the Microcystis monoculture or the coculture. The community composition in Sandusky Bay was monitored over the winter and spring months (January-April) to see how it changed as time progressed. Nutrient amendment experiments were also conducted adding nitrate, phosphate, and a combination of nitrate and phosphate to stimulate growth and identify any possible nutrient limitations. The initial community yielded low cell densities until the temperature increased and cell abundances followed shortly thereafter. Planktothrix dominated over the winter followed by a transitional period of cryptomonad and diatom dominations before transitioning back to Planktothrix. Both nitrate and phosphate were limiting Planktothrix growth in the spring, while nitrate alone was limiting the overall community. iv To my parents, David Peck and Sandra Maltzman for their constant support throughout everything. All the people I have met at BGSU and in the greater Bowling Green Community. I have truly enjoyed my time in Ohio and am regretful to see it end. v ACKNOWLEDGMENTS I would like to thank: George S. Bullerjahn, Timothy Davis, and R. Michael McKay for giving me the opportunity to continue my education at the graduate level, for the many opportunities both in the lab and in the field for me to learn and grow, and for their advice, understanding and patience. William Cody for assisting with the cellular enumeration for the sediment incubation portion of my thesis. My undergraduate research advisor Dr. Raymond L. Kepner at Marist College for allowing me to conduct research with him and cultivating my love of research that has helped me throughout the entire journey. The crews on the CCGS Limnos and CGC Neah Bay. The entire BGSU Lab: Kaitlyn McKindles, Michelle Neudeck, Christina Moore, Kari Lane Shupe, Jay DeMarco, Emily Beers, Callie Nauman, Seth Buchholz, Laura Reitz, Matthew Kennedy Dr. Paul Matson, and honorary lab member/Dr. McKay’s postdoc Dr. Thijs Frenken. vi TABLE OF CONTENTS Page CHAPTER 1: INTRODUCTION .......................................................................................... 1 1.1: Shallow Nearshore Cyanobacterial Harmful Algal Bloom Environments ......... 1 1.2: Composition of Western Lake Erie cHABs ........................................................ 2 1.3: Physicochemical Factors That Affect cHABs ................................................... 3 1.4: How Planktothrix Acclimates to Low Nitrogen Environments .......................... 4 1.5: Sandusky Bay cHABs-Dominated by Planktothrix agardhii ............................. 5 CHAPTER 2: MATERIALS AND METHODS ................................................................... 7 2.1: Competition Experiments ................................................................................... 7 2.1.1: Culture Experimental Design............................................................... 7 2.1.2: Monitoring the Growth of the Cultures ............................................... 9 2.1.2.1: Measurement of Growth Rates and Microcystis: Planktothrix Ratio ................................................................. 9 2.1.3: Determining Microcystin Concentrations ............................................ 9 2.2: Sediment Incubation Experiments ...................................................................... 10 2.2.1: Sample Site and Collection .................................................................. 10 2.2.2: Nutrient Amendment Experimental Setup and Initial Nutrient Analysis................................................................................................ 11 2.2.3: Sampling for Enumeration/Chlorophyll Analysis ............................... 12 2.2.4: Cell Enumeration ................................................................................. 13 2.2.5: Chlorophyll Extraction and Determining Chlorophyll Biomass ......... 13 CHAPTER 3: RESULTS ....................................................................................................... 15 vii 3.1: Competition Experiments ................................................................................... 15 3.1.1: Microcystis and Planktothrix Growth Rate ......................................... 15 3.1.2: The Influence of Nitrogen on the Ratio of Microcystis to Planktothrix 20 3.1.3: The Influence of Competition and Nitrogen Levels on Toxin Accumulation ....................................................................................... 22 3.2: Sediment Incubation Experiments ...................................................................... 23 3.2.1: Community Composition/Dominance ................................................. 23 3.2.2: Impacts of Nutrient Limitation ............................................................ 27 CHAPTER 4: DISCUSSION ................................................................................................. 30 4.1: Competition Experiments ................................................................................... 30 4.2: Sediment Incubation Experiments ...................................................................... 32 CHAPTER 5: FUTURE WORK ........................................................................................... 34 LITERATURE CITED .......................................................................................................... 35 viii LIST OF FIGURES Figure Page 1 Schematic of trial setup for the reduced and nitrogen absent environments ............. 8 2 Map of Sandusky Bay ................................................................................................ 11 3 Microcystis average growth rates when grown in monoculture and co-culture with Planktothrix over three different nitrogen treatments based on cell enumeration ..... 15 4 Planktothrix average growth rates when grown in monoculture and co-culture with Microcystis over three different nitrogen treatments based on cell enumeration ...... 16 5 Microcystis and Planktothrix growth when grown in monoculture over three different nitrogen treatments based on cell enumeration ........................................... 18 6 Microcystis and Planktothrix growth when grown in monoculture over three different nitrogen treatments based on in vivo chlorophyll fluorescence .................. 18 7 Microcystis to Planktothrix biovolume (µm3/mL) ratios in co-culture over three different treatments .................................................................................................... 20 8 Average rate of Microcystis to Planktothrix change per day over the course of two trials per treatment ..................................................................................................... 21 9 Temperature of Sandusky Bay on each sampling day ............................................... 23 10 Dissolved nutrient concentrations in Sandusky Bay from early March thru late April ........................................................................................................................... 24 11 Total nutrient concentrations in Sandusky Bay from early March thru late April .... 24 12 Community composition in Sandusky Bay from late January thru late April ........... 25 13 Proportional breakdown of phytoplankton in the Sandusky Bay water samples....... 26 14 Proportional breakdown of cyanobacteria in the Sandusky Bay water samples ....... 27 ix 15 Cellular density of Planktothrix under four nutrient treatments at initial and final (t=4) stages ................................................................................................................. 28 16 Amount of average chlorophyll biomass presented initially and at the end of each nutrient amendment trial .................................................................................... 29 x LIST OF TABLES Table Page 1 Temperature of incubation for each trial of the sediment incubation experiment ..... 12 2 Probability value of significance of Microcystis monoculture vs co-culture from each treatment ............................................................................................................ 15 3 Probability value of significance of monoculture vs co-culture from each treatment
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