Title: Physiological ecology of Trichodesmium and its microbiome in the oligotrophic ocean
Description: The colonial, N2 fixing cyanobacterium Trichodesmium is a keystone species in oligotrophic ocean ecosystems. Trichodesmium is responsible for approximately 50% of the total biologically fixed N2 in the ocean, and this “new” nitrogen fuels primary productivity and the amount of carbon sequestered by the ocean. Trichodesmium does not exist in isolation. Colonies occur ubiquitously with an assemblage of epibiotic microorganisms that are distinct from planktonic microbes and modulated across environments, yet the implications of this relationship have not been explored. In this thesis, the ecology, physiology, and potential geochemical impact of interactions within the Trichodesmium host-microbiome system were examined across three different oligotrophic ocean environments. First, to establish the metabolic diversity contributed by the microbiome to Trichodesmium consortia, a whole community metagenomic sequencing approach was used across a transect the western North Atlantic. This study demonstrated that the microbiome contributes a large amount of unique functional potential and is modulated across a geochemical gradient.

In the following study, metatranscriptomics was used to show that such metabolic potential in Trichodesmium and the microbiome was expressed and modulated across the environment. Colonies were sampled in the western tropical South Pacific and gene expression dynamics indicated co-limitation by iron and phosphorus, and revealed a mechanism for phosphate reduction by Trichodesmium and subsequent utilization by the microbiome. These activities were verified with phosphate reduction rate measurements and indicated cryptic phosphorus cycling within colonies. Next, the suite of potential physiological interactions between host and microbiome was assessed with metatranscriptome sequencing on high frequency samples of Trichodesmium colonies from the North Pacific subtropical gyre. Synchronized day-night gene expression periodicity between consortia members indicated tightly linked metabolisms. The functional annotations of these synchronous genes indicated intra-consortia cycling of nitrogen, phosphorus and iron, as well as a microbiome dependence on Trichodesmium-derived cobalamin—interactions that could alter the transfer of these resources to the surrounding water column.

In the final study, the effect of the microbiome on Trichodesmium N2 fixation was assessed. Using colonies obtained from the North Atlantic, activity in the microbiome was selectively modified using quorum sensing acyl homoserine lactone cell-cell signaling, a mechanism that Trichodesmium itself does not possess. These experiments indicated that the microbiome has the potential to increase or decrease Trichodesmium N2 fixation to a degree that rivals the effects of alterations in nutrient concentration, but at a more rapid rate. In all, the research presented in this thesis demonstrates the integral importance of the microbiome to Trichodesmium physiology and ecology, highlighting the importance of an unexplored facet of marine microbial systems that likely influences the biogeochemistry of the planet.