Micro-scale measurements of marine microbial interactions with global scale consequences

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Interactions between marine phytoplankton and heterotrophic bacteria are emerging as key ecological processes that control marine biogeochemical cycles and ecosystem productivity. While these interactions have large-scale implications, they are generally played out across very small spatiotemporal scales and often involve intimate ecological relationships involving the exchange of a diverse suite of metabolites and infochemicals. Previous studies have focussed on the ecological relationships between heterotrophic bacteria and large phytoplankton cells, such as diatoms and dinoflagellates, however, the photosynthetic biomass across much of the global ocean is dominated by picocyanobacteria, mainly comprising two genera, Prochlorococcus and Synechococcus. It has recently been suggested that the nitrogen-rich exudates of Synechococcus may be consumed by heterotrophic bacteria, potentially establishing metabolic, and eventually physical interactions. Yet, due to extremely small size of both partners (0.8-2 µm), it is extremely challenging to observe and quantify their metabolic exchanges at the single-cell level using conventional methods. This means that some of the ecological and biogeochemical consequences of these interactions have potentially been overlooked until now. Recently, technological breakthroughs in high-resolution single-cell imaging techniques, such as Secondary Ion Mass Spectrometry (SIMS), have opened the door for studying microbial associations at relevant scales, allowing for more accurate quantification of their impact on nutrient cycling and oceanic productivity. This thesis focused on the associations between the picocyanobacteria Synechococcus and heterotrophic bacteria, I applied a combination of stable isotope labelling approaches and SIMS to study the metabolic exchanges and the behavioural mechanisms underpinning the onset of the interaction between these two partners, at the single-cell level. First, I compared bulk-scale mass spectrometry with two SIMS techniques (NanoSIMS and ToF-SIMS) to define their advantages and limitations in measuring nutrient uptake at both community and single-cell level. After determining that NanoSIMS was the most suitable tool to investigate Synechococcus-heterotrophic bacteria interactions, I applied this technique to determine if nutrient exchanges between Synechococcus and two of its culture-associated bacterial isolates were reciprocal. Finally, I determined the role that bacterial behaviour may have on the exploitation of Synechococcus-derived nutrients. This thesis demonstrates the single-cell variability and heterogeneity of the nutrient uptake and cycling between these small and ubiquitous marine microbes, this observed heterogeneity would have been completely missed by large-scale approaches. The associations between Synechococcus and different bacterial species lead to species-specific differences in nutrient exchanges. Cells can access significantly more Synechococcus derived nutrients by means of physical attachment and despite the small size of Synechococcus cells, this association is likely mediated by bacterial behaviour such as chemotaxis. The dynamics that determine these single-cell microbial interactions can have vast implications for global-scale processes.
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