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IntroductionVolatile organic compounds (VOCs) are small, low-vapor-pressure molecules emitted from the surface ocean into the atmosphere. In the atmosphere, VOCs can change OH reactivity and condense onto particles to become cloud condensation nuclei. VOCs are produced by phytoplankton, but the conditions leading to VOC accumulation in the surface ocean are poorly understood. MethodsIn this study, VOC accumulation was measured in real time over a 12 h day−12 h night cycle in the model diatomPhaeodactylum tricornutumduring exponential growth. ResultsSixty-threem/zsignals were produced in higher concentrations than in cell-free controls. All VOCs, except methanol, were continuously produced over 24 h. All VOCs accumulated to higher concentrations during the day compared to the night, and 11 VOCs exhibited distinct accumulation patterns during the morning hours. Twenty-seven VOCs were associated with known metabolic pathways inP. tricornutum, with most VOCs involved in amino acid and fatty acid metabolism. DiscussionPatterns of VOC production were strongly associated with diel shifts in cell physiology and the cell cycle. Diel VOC production patterns give a fundamental understanding of the first steps in VOC accumulation in the surface ocean. 

Abstract Labile dissolved organic carbon in the surface oceans accounts for ~¼ of carbon produced through photosynthesis and turns over on average every three days, fueling one of the largest engines of microbial heterotrophic production on the planet. Volatile organic compounds are poorly constrained components of dissolved organic carbon. Here, we detected 72 m/z signals, corresponding to unique volatile organic compounds, including petroleum hydrocarbons, totaling approximately 18.5 nM in the culture medium of a model diatom. In five cocultures with bacteria adapted to grow with this diatom, 1 to 59 m/z signals were depleted. Two of the most active volatile organic compound consumers, Marinobacter and Roseibium, contained more genes encoding volatile organic compound oxidation proteins, and attached to the diatom, suggesting volatile organic compound specialism. With nanoscale secondary ion mass spectrometry and stable isotope labeling, we confirmed that Marinobacter incorporated carbon from benzene, one of the depleted m/z signals detected in the co-culture. Diatom gross carbon production increased by up to 29% in the presence of volatile organic compound consumers, indicating that volatile organic compound consumption by heterotrophic bacteria in the phycosphere – a region of rapid organic carbon oxidation that surrounds phytoplankton cells – could impact global rates of gross primary production. 

The ocean is a vast reservoir of bioavailable dissolved organic compounds (DOCs). Phytoplankton and bacterioplankton are the primary producers and consumers of these organic compounds, respectively, driving DOCs turnover on timescales of minutes to days. Volatile organic compounds (VOCs) make up about a third of DOCs, and their diffusivity and reactivity cause them to be important contributors to plankton carbon cycling and atmospheric chemistry. This research sought to describe plankton interactions mediated by VOCs. A model diatom, Phaeodactylum tricornutum, and five bacterial species known to be associated with the P. tricornutum phycosphere were studied in monocultures and co-cultures. Investigations evaluated the VOCs produced and consumed, temporal dynamics of VOC production and their roles in diatom metabolism, and physiological strategies of bacterial VOC consumers. P. tricornutum produced 78 VOCs during exponential growth. About 60% of these VOCs were hydrocarbons. In co-cultures with P. tricornutum, bacteria consumed different ranges of VOCs. The VOC specialists, Marinobacter and Roseibium, consumed the most, had hydrocarbon oxidation genes, and showed motility and physical attachment to the diatom. Rhodobacter and Stappia consumed fewer VOCs and were non-motile, while Yoonia consumed only acetaldehyde. Diatom gross carbon fixation was 29% higher in the presence of VOC specialists, suggesting rapid VOC consumption in the phycosphere impacts global gross carbon production. Temporal VOC production in P. tricornutum was monitored over a diel cycle. All VOCs were produced in higher concentrations during the day compared to night. Regression spline functions revealed six unique temporal production patterns associated with diel shifts in metabolism and the cell cycle. Physiological strategies for VOC uptake were studied in the VOC specialist Marinobacter. Marinobacter consumed some benzenoids at concentrations ranging from pM to μM and most increased cell densities compared to no VOC added controls and were not chemoattractants. Other VOCs that did not stimulate higher cell densities were strong chemoattractants. Thus, some VOCs are chemoattractants that guide motile cells toward co-emitted growth substrates. VOC discrimination may optimize spatial and temporal positioning in the phycosphere and enhance VOC uptake, sustaining the extremely low VOC concentrations in the surface ocean. This research revealed phytoplankton and ii bacterioplankton physiological processes that underlie the biological cycling of surface ocean VOCs and their potential for air-sea flux. This dissertation on microbiology in the phycosphere provided a foundation for exploring elements of science art that promote audience engagement through an exhibition that used scientific findings from the dissertation. Original art and audience surveys were used iteratively to increase science accessibility to general audiences.