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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.
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Diel investments in metabolite production and consumption in a model microbial system
Abstract Organic carbon transfer between surface ocean photosynthetic and heterotrophic microbes is a central but poorly understood process in the global carbon cycle. In a model community in which diatom extracellular release of organic molecules sustained growth of a co-cultured bacterium, we determined quantitative changes in the diatom endometabolome and the bacterial uptake transcriptome over two diel cycles. Of the nuclear magnetic resonance (NMR) peaks in the diatom endometabolites, 38% had diel patterns with noon or mid-afternoon maxima; the remaining either increased (36%) or decreased (26%) through time. Of the genes in the bacterial uptake transcriptome, 94% had a diel pattern with a noon maximum; the remaining decreased over time (6%). Eight diatom endometabolites identified with high confidence were matched to the bacterial genes mediating their utilization. Modeling of these coupled inventories with only diffusion-based phytoplankton extracellular release could not reproduce all the patterns. Addition of active release mechanisms for physiological balance and bacterial recognition significantly improved model performance. Estimates of phytoplankton extracellular release range from only a few percent to nearly half of annual net primary production. Improved understanding of the factors that influence metabolite release and consumption by surface ocean microbes will better constrain this globally significant carbon flux.
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- PAR ID:
- 10366569
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 16
- Issue:
- 5
- ISSN:
- 1751-7362
- Format(s):
- Medium: X Size: p. 1306-1317
- Size(s):
- p. 1306-1317
- Sponsoring Org:
- National Science Foundation
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