Insights into the ecology and biogeochemistry of ocean microbes revealed through transcriptomics of bacterial-phytoplankton model systems
Durham, Bryndan Paige
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Marine phytoplankton and heterotrophic bacteria are the major producers and consumers of the oceans, respectively, and influence all of Earth’s key biogeochemical cycles. Given that about half of the carbon fixed by phytoplankton is degraded by bacteria, determining the specific substrates and mechanisms that underlie this exchange is critical to our understanding of the marine microbial food web. Tight metabolic coupling during such trophic interactions could result in element cycling that leaves virtually no measurable signals in bulk seawater, representing gaps in current marine elemental models. To explore the biogeochemical and ecological impacts of such associations across taxonomic groups, bacterial-dinoflagellate and bacterial-diatom model systems were developed that consisted of Roseobacter clade members Roseovarius nubinhibens ISM or Ruegeria pomeroyi DSS-3 with the dinoflagellate Alexandrium tamarense CCMP1771 or the diatom Thalassiosira pseudonana CCMP1335. In all of these systems, the bacterium relied on its phytoplankter partner for organic substrates, while the phytoplankter relied on the bacterium for a source of vitamin B12. Using RNA-Seq methodology to investigate differences in gene expression in co-cultures and mono-cultures, several taxon-specific currencies that result in metabolic linkages between the plankton groups were discovered. Some of these compounds fit established views of the primary mediators of phytoplankton-bacterial trophic interactions in the marine microbial food web, including osmolytes, amino acids, and sugars. Others represent potentially novel substrates not previously considered to play roles in trophic interactions between marine plankton. These unexpected metabolites, including sulfonates, urea derivatives, methylated amines, and opines, may be cycled over short time scales at sub-micron distances and represent cryptic links in carbon, nitrogen, and sulfur cycling in the ocean. In addition to the metabolic responses detected in the co-culture systems, evidence was also found for cell-cell signaling, demonstrating active recognition between the two trophic levels. The taxon-specific metabolites and interdependencies revealed in this model system approach shed light on new aspects of ocean biogeochemistry.