Award: OCE-1646709

The cyanobacterium Prochlorococcus is the most abundant photosynthetic cell on Earth and contributes to global ocean carbon cycling and food webs. The outcome of this project is advancement of understanding of how the physiological dynamics and genetic diversity of Prochlorococcus underlie its global abundance and contributions to global carbon and energy cycles. Five publications were produced: Thompson et al. 2018; Thompson, Kouba, and Ahlgren 2021; van den Engh et al. 2017; Orellana et al. 2020; Thompson and Kouba 2019. Intellectual Merit. At the oceanographic time-series station ALOHA, we examined whether shifts in chlorophyll distributions corresponded to changes in Prochlorococcus genetic diversity (i.e. ecotype-level community structure) or photoacclimation of stable communities over short time intervals. We found that community structure was stable despite abrupt shifts in Prochlorococcus chlorophyll distributions, due to unexpected physiological plasticity of high-light adapted Prochlorococcus ecotypes. Through comparison with published seasonal-scale time-series, our data suggest that variability on daily scales triggers shifts in Prochlorococcus photoacclimation, while seasonal-scale dynamics trigger shifts in community structure. Together, these data highlight the importance of incorporating the process of photoacclimation into interpretations of Prochlorococcus population dynamics (Thompson et al. 2018; van den Engh et al. 2017). Extending from a single station, we examined Prochlorococcus diversity across latitudinal gradients in the North Pacific. We discovered that Prochlorococcus genetic diversity extends below the ecotype level, especially among low-light adapted Prochlorococcus. We also found a combination of ubiquitous and habitat specific subecotypes across the North Pacific Subtropical Front, suggesting that ecosystems across the front are connected but that microbial communities on either side are shaped by environmental selection (Thompson et al. 2021). Next, we examined differential contribution of these ecotypes, and subecotypes, to the carbon cycle and cell division patterns. While laboratory experiments and genomic analysis suggest that ecotypes, and subecotypes, contribute differently to biogeochemical cycles, no studies had previously tested the differential activity of coexisting ecotypes in natural assemblages of Prochlorococcus. Using stable-isotope probing experiments and cell cycle analysis, we found that even closely related co-existing subecotypes contributed differently to carbon cycling and cell division patterns (Thompson and Kouba, 2019). This work is the first to suggest that all coexisting picocyanobacteria are not equally active and that community structure, rather than abundance, predicts picocyanobacterial contributions to global processes. Overall, the work of this project discovered that the global abundance and stability of the marine cyanobacterium Prochlorococcus rests on its genetic diversity and physiological plasticity, which allow it to thrive across numerous oceanographic conditions. Broader Impacts. This project resulted in the training of over 10 undergraduate students, one M.S. student, and two laboratory technicians. In addition, in collaboration with 8 high school STEM teachers and the Institute for Systems Biology, we designed and distributed a 2-week educational module for high school classrooms. Specifically, the module engages students with the very small and the very large aspects of phytoplankton, leading to a deeper understanding of energy, oxygen, biological scales, and the ocean system, and meeting next generation science standards. Students practice processing real oceanographic data from time-series stations such as Station ALOHA and consider whether humans could survive in a world without land plants by learning about the photosynthetic microbes teeming within every drop of seawater. At the end of the module, students showcase via art how the cells in a drop of seawater support human life and the global Earth system. Throughout this phenomenon-based three-dimensional unit, a Project-Based-Learning component guides students as they explore microbial life in a drop of seawater. Students design and evaluate questions to investigate phytoplankton phenomena. Science, technology, engineering, art, and mathematics (STEAM) are blended, which gives students opportunities to express their learned knowledge through many means. The module was presented to over 100 teachers and will reach thousands of high school students. We published our framework for developing this module, and two other oceanographic educational modules in Orellana et al. (2020). Engh, G.J. van den, J.K. Doggett, A.W. Thompson, M.A. Doblin, C.N.G Gimpel, and D.M. Karl. 2017. Dynamics of Prochlorococcus and Synechococcus at Station ALOHA Revealed through Flow Cytometry and High-Resolution Vertical Sampling. Vol. 4. Orellana, Monica V., Claudia Ludwig, Anne W. Thompson, and Nitin S. Baliga. 2020. Integrating Oceanographic Research into High School Curricula: Achieving Broader Impacts Through Systems Education Experiences Modules. Oceanography 33 (3): 16-20. Thompson, Anne W, Ger van den Engh, Nathan A Ahlgren, Kathleen Kouba, Samantha Ward, Samuel T Wilson, and David M Karl. 2018. ?Dynamics of Prochlorococcus Diversity and Photoacclimation During Short-Term Shifts in Water Column Stratification at Station ALOHA. Frontiers in Marine Science 5: 488. Thompson, Anne W, and Kathleen Kouba. 2019. Differential Activity of Coexisting Prochlorococcus Ecotypes. Frontiers in Marine Science Vol. 6. Thompson, Anne W., Kathleen Kouba, and Nathan A. Ahlgren. 2021. Niche Partitioning of Low-Light Adapted Prochlorococcus Subecotypes across Oceanographic Gradients of the North Pacific Subtropical Front. Limnology and Oceanography. Last Modified: 04/26/2021 Submitted by: Anne W Thompson