Award: OCE-1434916

This project aimed to improve our understanding of marine cyanobacteria utilization of organic matter. A major goal was to characterize the role of light in organic molecules (carbon and nutrients) assimilation and the importance of mixotrophy (also called photoheterotrophy) within cyanobacteria metabolism. Marine cyanobacteria, the most abundant marine phytoplankton, have a major role in shaping nutrients cycling and are major contributors to primary production and carbon export in the open ocean. Marine cyanobacteria are considered to be photoautotrophic (use light for energy and CO2 as a source of carbon), but recent evidence suggests they may also benefit from assimilation of organic molecules, including single carbon containing molecules, and may therefore be mixotrophic (capable of using inorganic and organic carbon sources). However, their mixotrophic metabolism is still poorly understood. Before this project, most studies investigating the light-dependent organic carbon uptake potential of marine cyanobacteria had been performed with cultures, while only one field study had demonstrated glucose uptake by Prochlorococcus in the Atlantic Ocean. Hence, in situ data was lacking to assess the potential mixotrophic nutrition of these globally relevant marine cyanobacteria, how it compares to their autotrophic nutrition mode (CO2 fixation), and its environmental controls (nutrients, light levels, etc.). Using a combination of innovative approaches, which leveraged cruises of opportunity we confirmed that natural marine cyanobacteria of the genus Prochlorococcus and Synechococcus can incorporate organic molecules with variable C:N:P composition, including glucose, a single C-containing molecule. In fact, mixotrophy by these unicellular cyanobacteria was widespread over a wide range of biogeochemically distinct regions of the Western Tropical South Pacific Ocean and the North Pacific subtropical gyre. We similarly found that organic molecules could also be directly taken up by the nitrogen-fixing filamentous cyanobacteria Trichodesmium or primarily consumed by heterotrophic bacteria colonizing its surface, that ultimately transfer reduced organic compounds to their host. Therefore, our results showed that mixotrophy is widespread among unicellular and filamentous groups of marine cyanobacteria, nitrogen fixers and non-nitrogen fixers, and across ocean basins. However, based on group specific measurements of carbon assimilation from CO2 or glucose, we demonstrated that Prochlorococcus and Synechococcus, remain primarily photoautotrophic. Our findings indicate that mixotrophy by marine cyanobacteria is more likely to be an adaptation to low inorganic nutrient availability rather than a facultative pathway for carbon acquisition. Additional critical gaps in our understanding of cyanobacteria mixotrophic metabolism concern regulating factors. In particular, how organic C assimilation by marine unicellular cyanobacteria depends upon light availability and photosynthetic electron transport in natural settings. We showed that assimilation rates of organic molecules are reduced in the dark or when photosynthesis is impaired, meaning that this mixotrophic metabolism is likely dependent on light energy fueling photosynthesis. In follow-up experiments we demonstrated that the uptake of glucose by natural cyanobacteria responds to light intensity similarly to photosynthesis and follows a diel pattern. Finally, we found that over a third of the total leucine uptake was by the Prochlorococcus group. This is important because bacterial production, a fundamental parameter for biological oceanography, is commonly measured based on the incorporation of leucine in bacterial proteins. Therefore, we recommend that the contribution of picocyanobacteria to bacterial production estimates should be considered when measuring bacterial production in marine environments, even in dark incubations. Overall these results suggest that dissolved organic matter utilization provides nutritional plasticity to marine cyanobacteria in oligotrophic environments. Results from the project have been published in peer-reviewed journals (eight manuscripts as of November 2018, plus several in preparation), and disseminated through presentations at scientific meetings and databases. This research stimulated new international collaborations. A video was created for the large public to learn about an international research cruise that was key to this project (OUTPACE: Oligotrophy to UlTra-oligotrophy PACific Experiment). Our findings have also been shared with high school teachers for diffusion to their classroom, and to many public outreach events at sciences fairs, science festivals and open houses in museums and at Columbia University. This project supported an early career female scientist, a graduate student, two Bachelor theses from female students and several undergraduate and high school students. Last Modified: 10/30/2018 Submitted by: Solange Duhamel