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.
more »
« less
This content will become publicly available on May 20, 2026
Volatile Organic Compounds Modulate the Biological and Chemical Environment of the Phycosphere
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.
more »
« less
- Award ID(s):
- 1948163
- PAR ID:
- 10633676
- Publisher / Repository:
- ScholarsArchive@OSU
- Date Published:
- Format(s):
- Medium: X
- Institution:
- Oregon State University
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
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.more » « less
-
Biogenic volatile organic compounds (VOCs) play key roles in coral reef ecosystems, where, together with dimethylated sulfur compounds, they are indicators of ecosystem health and are used as defense strategies and infochemicals. Assessment and prediction of the exchange rates of VOCs between the oceans and atmosphere, with implications for atmospheric reactivity and climate, are hampered by poor knowledge of the regulating processes and their temporal variability, including diel cycles. Here, we measured the variation over 36h of the concentrations of DMSPCs (dimethylsulfoniopropionate (DMSP)-related compounds, namely DMSP, dimethylsulfoxide, acrylate, dimethylsulfide, and methanethiol as dimethyl disulfide) and VOCs (COS, CS2, isoprene, the iodomethanes CH3I and CH2ClI, and the bromomethanes CHBr3and CH2Br2), in surface waters inside the shallow, northern coral-reef lagoon of Mo’orea (French Polynesia) and 4 km offshore, in the tropical open ocean. Comparisons with concurrent measurements of sea surface temperature, solar radiation, biogeochemical variables (nutrients, organic matter), and the abundances and taxonomic affiliations of microbial plankton were conducted with the aim to explain interconnections between DMSPCs, VOCs, and their environment across diel cycles. In open ocean waters, deeper surface mixing and low nutrient levels resulted in low phytoplankton biomass and bacterial activity. Consequently, the diel patterns of VOCs were more dependent on photochemical reactions, with daytime increases for several compounds including dissolved dimethylsulfoxide, COS, CS2, CH3I, and CH2ClI. A eukaryotic phytoplankton assemblage dominated by dinoflagellates and haptophytes provided higher cell-associated DMSP concentrations, yet the occurrence of DMSP degradation products (dimethylsulfide, dimethyl disulfide) was limited by photochemical loss. Conversely, in the shallow back reef lagoon the proximity of seafloor sediments, corals and abundant seaweeds resulted in higher nutrient levels, more freshly-produced organic matter, higher bacterial activity, and larger algal populations ofMamiellales, diatoms andCryptomonadales. Consequently, DMSP and dimethylsulfoxide concentrations were lower but those of most VOCs were higher. A combination of photobiological and photochemical processes yielded sunny-daytime increases and nighttime decreases of dimethylsulfide, dimethyl disulfide, COS, isoprene, iodomethanes and bromomethanes. Our results illustrate the important role of solar radiation in DMSPC and VOC cycling, and are relevant for the design of sampling strategies that seek representative and comparable measurements of these compounds.more » « less
-
Marine bacterioplankton face stiff competition for limited nutrient resources. SAR11, a ubiquitous clade of very small and highly abundant Alphaproteobacteria, are known to devote much of their energy to synthesizing ATP-binding cassette periplasmic proteins that bind substrates. We hypothesized that their small size and relatively large periplasmic space might enable them to outcompete other bacterioplankton for nutrients. Using uptake experiments with 14C-glycine betaine, we discovered that two strains of SAR11, Candidatus Pelagibacter sp. HTCC7211 and Cand. P. ubique HTCC1062, have extraordinarily high affinity for glycine betaine (GBT), with half-saturation (Ks) values around 1 nM and specific affinity values between 8 and 14 L mg cell−1 h−1. Competitive inhibition studies indicated that the GBT transporters in these strains are multifunctional, transporting multiple substrates in addition to GBT. Both strains could use most of the transported compounds for metabolism and ATP production. Our findings indicate that Pelagibacter cells are primarily responsible for the high affinity and multifunctional GBT uptake systems observed in seawater. Maximization of whole-cell affinities may enable these organisms to compete effectively for nutrients during periods when the gross transport capacity of the heterotrophic plankton community exceeds the supply, depressing ambient concentrations.more » « less
-
Abstract An extensive set of primary and secondary pollutants was measured at a ground site in a remote location in the Yellow River Delta, China during the Ozone Photochemistry and Export from China Experiment (OPECE) from March to April 2018. The measurements include volatile organic compounds (VOCs), peroxyacyl nitrates (PANs), ozone (O3), particulate species, nitrogen oxides (NOx), and SO2. Observed VOC mixing ratios were comparable to those measured in heavily polluted cities in the U.S. and China. The VOC source signatures suggest a strong influence from Oil and Natural Gas (O&NG) emissions with potentially large contributions from Liquified Petroleum Gas (LPG) sources as well. Consistently elevated concentrations of O3, PAN, and its rarely measured homologs peroxybenzoylic nitric anhydride (PBzN) and peroxyacrylic nitric anhydride (APAN) at the OPECE site indicate complex photochemistry in a heterogeneous VOC environment. Diagnostic 0‐D box model simulations are used to investigate the budgets of ROx(OH + HO2 + RO2), and the rate and efficiency of O3production. Model sensitivity calculations indicate that O3production at OPECE site is VOC limited in spring. This suggests that reduction in VOCs should be a priority for reducing O3, where production and fugitive emissions from O&NG provide an attractive target. While initial reductions in NOxmight increase O3production, reduction of NOxalong with VOCs will be a necessary step to achieve long‐term ozone reduction.more » « less
An official website of the United States government
