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Doctor of Philosophy RICE UNIVERSITY Stress tolerance of the endosymbiotic cnidarian Hydra viridissima: Contributions of the host and the symbiont By Siao Ye A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE Doctor of Philosophy APPROVED, THESIS COMMITTEE Evan Siemann (Chair) Amy Dunham Evan Siemann Amy E. Dunham Scott P. Egan Meenakshi Bhattacharjee (Apr 13, 2020) Scott P. Egan (Apr 15, 2020) Meenaskshi Bhattacharjee Scott Egan Meenakshi Bhattacharjee Scott P. Egan Rudy Guerra (Apr 13, 2020) Rudy Guerra Rudy Guerra HOUSTON, TEXAS April 2020 iii ABSTRACT Stress tolerance of the endosymbiotic cnidarian Hydra viridissima: Contributions of the host and the symbiont by Siao Ye Endosymbiosis is a universal relationship in nature, in which the symbiont is tightly integrated into the host and alters the host’s ecological niche and evolutionary trajectory. However, endosymbiosis can be easily disrupted by stress, which raises concerns about holobiont (symbiont plus host) persistence with global climate change, because massive endosymbiosis breakdown could have severe ecological consequences. The hologenome theory proposes that the symbiont and the host jointly determine the holobiont phenotype, and so rapid holobiont phenotype alteration can be achieved through changes in symbiont composition via strain acquisition, adaptation or acclimation. Previous studies have confirmed that switching symbionts can change holobionts’ stress tolerance, yet the relative roles of the symbiont and the host in controlling the holobiont phenotype are unclear as is whether symbiont adaptation or acclimation alone could allow holobionts to persist in stressful environments. My thesis addressed factors affecting stress tolerance of the holobiont green hydra (Hydra viridissima) from both the symbiont (green algae) and the host (hydra) perspectives, and experimentally explored how manipulations of the symbiont or the host alone could alter holobiont stress tolerance. Furthermore, I used agent-based modeling to simulate the holobiont adaptation via symbiont adaptation. My experimental results showed unequal contributions of the host and the symbiont to holobiont stress tolerance, with the host playing a dominant role. Furthermore, I detected positive transgenerational effects in the host. Although host traits are usually overlooked in holobiont studies, my studies suggest they are equally or even more important in determining holobiont stress iii tolerance. On the other hand, symbiont adaptation or acclimation provides the holobiont an extra route to acquire stress tolerance if the host fails to acquire it directly, and such acquired stress tolerance can be inherited. In addition, my experiments proved the feasibility of altering holobiont phenotypes by symbiont manipulations in vivo. Simulations further demonstrated that holobionts with either vertical or horizontal symbiont transmission are able to evolve solely through adaption of the symbiont. These findings support the hologenome theory and have implications for forestry, agriculture and conservation by providing insights into the determination and management of holobiont stress tolerance. Acknowledgments Foremost I would like to thank my advisor Evan Siemann. Thanks for his time and knowledge, and especially the flexibility and independency under his supervision, which made this thesis possible. Being his only student all these years, I received his full support on my research. I would also like to thank my committee members, Dr. Amy Dunham, Dr. Meenakshi Bhattacharjee, Dr. Scott Egan and Dr. Rudy Guerra, who all supported my Ph.D study and provided important suggestions and feedback on my research in time. My special thanks give to Zhu Liu, my undergrad classmate and a close friend who is studying at University of South California, USA. He contributed significantly to my last chapter and helped me with the coding. For the supply of the hydra and algae in my lab, I would like to thank Dr. Daniel Martinez (Pomona College, Claremont, CA, USA), Dr. Hiroshi Shimizu (National Institute of Genetics, Mishima, Japan) and Dr. David Dunigan (University of Nebraska Lincoln, NE, USA). Also thanks Dr. Daniel Wagner and Dr. Jacob Robinson for their allowance of using their equipment. Next, I would like to thank Dr. Adrienne Correa, Dr. Tom Miller and Dr. Volker Rudolf, who all gave constructive suggestions during our discussions. I also want to thank people from my department who helped with my research: Brad Ochocki instructed me in R, Amanda shore and Therese Lamperty proofread my manuscript, Krishna Badhiwala and Eric Wice demonstrated how to monitor v animals, Linyi Zhang took care of my hydra when I was away, and Shannon Carter discussed about the agent-based modeling. A special thanks to Patrick Clay who took me and other students to watch “Guardian of the Galaxy” the first day we arrived, and organized activities all these years, which made my life not only fill with exams and lab work. I owe further thanks to my lab members, Stephen Truch and Maria Meza-Lopez, who supported my first year at Rice. I am also grateful for my undergrad research assistants, who all contributed their time and effort to the lab work. Finally, I cannot be more thankful to my family, my wife Yuan Song, my parents, Yubin Ye and Lezhen Zhao, and my sister Simiao Ye, as well as my dog Tutu. Your supports produce another “Dr.” in this world. Contents Acknowledgments .................................................................................................................. iv Contents ..................................................................................................................................... vi List of Figures ........................................................................................................................... ix List of Tables ............................................................................................................................ xi Introduction .............................................................................................................................. 1 1.1. Holobionts under stress ............................................................................................................ 1 1.2. Impacts of the symbiont on the holobiont stress tolerance ....................................... 3 1.2.1. Net impacts of symbionts ................................................................................................. 3 1.2.2. Existing symbiont composition alteration ................................................................ 4 1.2.3. Symbiont adaptation and acclimation ......................................................................... 5 1.3. Impacts of the host on the holobiont stress tolerance ................................................. 9 1.4. Heritability of symbiont-mediated traits ......................................................................... 20 1.5. Aim of the study .......................................................................................................................... 20 Thermal tolerance in green hydra: identifying the roles of algal endosymbionts and hosts in a freshwater holobiont under stress ..................... 23 2.1. Introduction .................................................................................................................................. 24 2.2. Methods .......................................................................................................................................... 27 2.2.1. Study Species and Culture Conditions ....................................................................... 27 2.2.2. Strains with Natural Symbionts ................................................................................... 28 2.2.3. Strains without Symbionts ............................................................................................. 29 2.2.4. Different Algal Strains Associated with a Single Hydra Strain ....................... 29 2.2.5. Control Hydra Strains Re-Associated with Their Original Symbionts ........ 30 2.2.6. Heat Shock Treatment ...................................................................................................... 30 2.2.7. Data Analysis ........................................................................................................................ 31 2.3. Results ............................................................................................................................................. 31 2.3.1.1. Establishment of Aposymbiotic Hydra, Novel Hydra, Control Hydra .. 31 2.3.2. Strain Specific Thermal Tolerance in Four Types of Hydra ............................. 32 2.3.3. Thermal Tolerance in Symbiotic and Aposymbiotic Hydra ............................. 35 2.3.4. Algae Thermal Tolerance ................................................................................................ 35 vii 2.4. Discussion ...................................................................................................................................... 36 2.4.1. Relative Contribution of the Host and the Endosymbiont to Hydra Thermal Tolerance ......................................................................................................................... 36 2.4.2. Adaptation Capability of Endosymbiotic Species from the Hologenome Perspective ........................................................................................................................................ 38 2.4.3.
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