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WILKES-DISSERTATION-2018.Pdf (4.378Mb) Chemostat and Modeling Investigations of Algal Photosynthetic Carbon Isotope Fractionation The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Wilkes, Elise. 2018. Chemostat and Modeling Investigations of Algal Photosynthetic Carbon Isotope Fractionation. Doctoral dissertation, Harvard University, Graduate School of Arts & Sciences. Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:41127152 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Chemostat and Modeling Investigations of Algal Photosynthetic Carbon Isotope Fractionation A dissertation presented by Elise Wilkes to The Department of Earth and Planetary Sciences In partial fulfillment of the requirements for the degree of Doctor of Philosophy in the subject of Earth and Planetary Sciences Harvard University Cambridge, Massachusetts April, 2018 2018 – Elise Wilkes All rights reserved. Dissertation Adviser: Ann Pearson Elise Wilkes Chemostat and Modeling Investigations of Algal Photosynthetic Carbon Isotope Fractionation Abstract Marine eukaryotic phytoplankton produce organic matter that is depleted in 13C relative to ambient dissolved carbon dioxide. This photosynthetic carbon isotope fractionation (εP) is recorded in marine sediments and used to resolve changes in the global carbon cycle, including variations in atmospheric pCO2. These applications rely upon a coherent understanding of the environmental and physiological controls on P. While classical models for εP are based on the balance between diffusion of CO2 and its fixation into biomass by the enzyme RubisCO, the details of phytoplankton carbon dynamics in reality are more complex. Phytoplankton employ a diversity of RubisCO types, and they also use carbon concentrating mechanisms (CCMs) that enhance intracellular CO2 concentrations. It is essential to understand the significance of these physiological features as controls on εp, as they may play important roles in explaining sedimentary archives. Here I performed CO2 and growth rate (μ) manipulation experiments with modern phytoplankton in chemostat cultures to address outstanding questions regarding the mechanistic underpinning of P. First, I characterized the stable carbon isotope ratios of coccolith-associated polysaccharides (CAPs) and other cellular constituents (bulk biomass, coccolith calcite, and alkenones) of Emiliania huxleyi. CAPs are involved in regulating calcification and have been recovered from sediments dating back ~180 Ma. It has been proposed that the carbon isotopic contents of CAPs may be used in combination with other proxies to reconstruct ancient atmospheric pCO2 levels. I find that the CAPs are isotopically enriched relative to bulk biomass and vary with μ and CO2. These results are explained by a simple model that predicts cellular carbon allocation to major organic carbon compound classes in E. huxleyi. My findings suggest that CAPs are less sensitive than alkenones as proxies for pCO2, but that combining CAP data together with data for alkenones and calcite may help reconstruct pCO2 with fewer assumptions than current approaches. I also performed chemostat culture experiments with the dinoflagellate Alexandrium tamarense, which uses an unusual form of the carbon-fixing enzyme RubisCO (Form II). It commonly is assumed that iii the kinetic isotope effect associated with RubisCO establishes the theoretical maximum value of εP, which is known as εf. I found that P values for A. tamarense varied with the ratio /[CO2(aq)] and approached an εf value of 27‰. This value is larger than theoretical predictions for Form II RubisCO and is not significantly different from the f values observed for more recently-evolved taxa that employ Form ID RubisCO, including E. huxleyi. This consistency across taxa may help to explain the broad uniformity of carbon isotope fractionation between organic and inorganic pools observed throughout the Phanerozoic, and it may pave the way for new algal pCO2 proxies based on dinoflagellate biomarkers or fossil dinoflagellate cysts. My work on A. tamarense also implies that an f value of 25-27‰ may be a universal property of red-lineage eukaryotic phytoplankton. This finding has major implications for reinterpreting the classical models for P, because it indicates that its maximum value (f) is unlikely to reflect the intrinsic isotope fractionation of RubisCO. By extension, this implies that RubisCO activity is not the kinetically slow step of carbon fixation in these phytoplankton, at least when cultivated in nutrient-limited chemostats. Based on this finding and other support from the literature, I propose a generalized model of carbon isotope fraction in eukaryotic phytoplankton that is able to reconcile the apparent uniformity of f (as inferred from in vivo studies) vs. the isotopic heterogeneity of RubisCO (as inferred from in vitro studies). The model introduces a nutrient- and light-dependent step upstream of RubisCO that is proposed to be a kinetic barrier to carbon acquisition and a significant source of isotope fractionation. Together, the results of this thesis imply that the kinetics, intrinsic discrimination, and taxonomy of RubisCO may be largely irrelevant to the expression of p under growth conditions of low nutrients and high photosynthetic activity, e.g., in the ocean gyres or away from coastal upwelling zones. Existing environmental data are consistent with this idea and suggest that alkenone and/or other organic pCO2 proxies should be reevaluated from the perspective of local nutrient dynamics and cellular growth conditions. iv Table of Contents Abstract iii Acknowledgements vi List of Tables and Figures viii Chapter 1 − Introduction 1 Chapter 2 − Carbon isotope ratios of coccolith-associated polysaccharides of Emiliania huxleyi 17 as a function of growth rate and CO2 concentration Chapter 3 − CO2-dependent carbon isotope fractionation in the dinoflagellate Alexandrium 47 tamarense Chapter 4 − A general model for carbon isotope fractionation in eukaryotic phytoplankton 80 Chapter 5 − Ongoing work and future directions 120 Appendix A – Supporting information for Chapter 2 133 Appendix B – Supporting information for Chapter 3 140 Appendix C – Supporting information for Chapter 4 144 Appendix D – Supporting information for Chapter 5 169 v Acknowledgements I am grateful to Ann Pearson for her endless optimism, and for her confidence in me and my ideas. I will always appreciate the time she has spent with me discussing science, the patience she has shown me throughout my time at Harvard, and her thorough, careful revisions of this dissertation. I would also like to thank Dave Johnston for his support and mentorship. I am grateful to Andy Knoll, Jerry Mitrovica, and Miaki Ishii for serving on my committee, past and present, and to my co-authors Rosalind Rickaby, Harry McClelland, and Renee Lee. Thank you to all the current and former members of the Pearson lab. Susie Carter deserves significant recognition for her contributions to this research. She has helped me with method development and to overcome many chemostat-related setbacks. I am grateful to Jenan Kharbush, Nagissa Mahmoudi, and Felix Elling for their friendship, advice, and for always being willing to answer my questions about biology lab techniques. Thank you to Ana C. Gonzalez Valdes, Jiaheng Shen, and Carolyn Zeiner for being generous with their time and friendship. I have shared my desk space and many conversations over the years with Lindsay Hays, Greg Henkes and Jordon Hemingway. I know I have benefitted tremendously from their perspectives. I am thankful to Sarah Hurley, Roderick Bovee, and Hilary Close for helping me to learn from their unique experiences. It has been a pleasure working with my student intern, Katie Mabbott, who helped with lab analyses supporting this work. I would also like to thank Einat Segev and Roberto Kolter for the opportunity to join the scientific party of the R/V Endeavor for field work. I would like to acknowledge my former mentors who inspired me to pursue graduate school and scientific research: Laura Wasylenki, Jill Mikucki, Ivan Apahamian, Ariel Anbar, Mukul Sharma, Justin Foy, and Bridget Alex. I appreciate the hard work of the Harvard EPS department administration and support staff. I feel fortunate to have shared my time in this department with so many wonderful people, including Harriet Lau, Alex Turner, Chris Parendo, Sunny Parker, Simon Lock, Tamara Pico, Anna Waldeck, Emma Bertran, Jocelyn Fuentes, Marena Lin, and Athena Eyster. I am also grateful for my time in HGWISE and the friendships I developed through that organization. vi I have an incredible support network outside of Harvard. Thank you to my dear friends in Boston: Mac Krumpak, Dalia Larios, Emily and Andy Stuntz, Emma Smithayer, Michelle and Alex Davis, and Jason Goodman. To Becky Rapf, Libby Parker, and Rachel Rosenberg—your support from afar means a lot. Thank you to my sister, Christine Wilkes. I am always so impressed by your wisdom, maturity, and adventurousness. To my grandmother, Joan Wilkes—you are an inspiration, and I appreciate all the experiences I have had because of you. To my parents-in-law, Robert and Marianne Kondziolka – I feel your support and love in all our interactions. And to my parents, Roger and Heather Wilkes
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