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Bowman, J. S., B. A. S. Van Mooy, D. P. Lowenstein, H. F. Fredricks, C. M. Hansel, R. Gast, J. R. Collins, N. Couto, and H. W. Ducklow. 2021. Whole community metatranscriptomes and lipidomes reveal diverse responses among Antarctic phytoplankton to changing ice conditions. Frontiers in Marine Science 8:593566; 10.3389/fmars.2021.593566

The transition from winter to spring represents a major shift in the basal energy source for the Antarctic marine ecosystem from lipids and other sources of stored energy to sunlight. Because sea ice imposes a strong control on the transmission of sunlight into the water column during the polar spring, we hypothesized that the timing of the sea ice retreat influences the timing of the transition from stored energy to photosynthesis. To test the influence of sea ice on water column microbial energy utilization we took advantage of unique sea ice conditions in Arthur Harbor, an embayment near Palmer Station on the western Antarctic Peninsula, during the 2015 spring–summer seasonal transition. Over a 5-week period we sampled water from below land-fast sea ice, in the marginal ice zone at nearby Palmer Station B, and conducted an ice removal experiment with incubations of water collected below the land-fast ice. Whole-community metatranscriptomes were paired with lipidomics to better understand how lipid production and utilization was influenced by light conditions. We identified several different phytoplankton taxa that responded similarly to light by the number of genes up-regulated, and in the transcriptional complexity of this response. We applied a principal components analysis to these data to reduce their dimensionality, revealing that each of these taxa exhibited a strikingly different pattern of gene up-regulation. By correlating the changes in lipid concentration to the first principal component of log fold-change for each taxa we could make predictions about which taxa were associated with different changes in the community lipidome. We found that genes coding for the catabolism of triacylglycerol storage lipids were expressed early on in phytoplankton associated with a Fragilariopsis kerguelensis reference transcriptome. Phytoplankton associated with a Corethron pennatum reference transcriptome occupied an adjacent niche, responding favorably to higher light conditions than F. kerguelensis. Other diatom and dinoflagellate taxa had distinct transcriptional profiles and correlations to lipids, suggesting diverse ecological strategies during the polar winter–spring transition.

» Article: Web, via publisher
» Supplementary material: Multiple files via publisher

Farnelid H., K. Turk-Kubo, H. Ploug, J. E. Ossolinski, J. R Collins, B. A. S. Van Mooy, and J. P. Zehr. 2018. Diverse diazotrophs are present on sinking particles in the North Pacific Subtropical Gyre. The ISME Journal 13:170-182; doi:10.1038/s41396-018-0259-x

Sinking particles transport carbon and nutrients from the surface ocean into the deep sea and are considered hot spots for bacterial diversity and activity. In the oligotrophic oceans, nitrogen (N2)-fixing organisms (diazotrophs) are an important source of new N but the extent to which these organisms are present and exported on sinking particles is not well known. Sinking particles were collected every 6 h over a 2-day period using net traps deployed at 150 m in the North Pacific Subtropical Gyre. The bacterial community and composition of diazotrophs associated with individual and bulk sinking particles was assessed using 16S rRNA and nifH gene amplicon sequencing. The bacterial community composition in bulk particles remained remarkably consistent throughout time and space while large variations of individually picked particles were observed. This difference suggests that unique biogeochemical conditions within individual particles may offer distinct ecological niches for specialized bacterial taxa. Compared to surrounding seawater, particle samples were enriched in different size classes of globally significant N2-fixing cyanobacteria including Trichodesmium, symbionts of diatoms, and the unicellular cyanobacteria Crocosphaera and UCYN-A. The particles also contained nifH gene sequences of diverse non-cyanobacterial diazotrophs suggesting that particles could be loci for N2 fixation by heterotrophic bacteria. The results demonstrate that diverse diazotrophs were present on particles and that new N may thereby be directly exported from surface waters on sinking particles.

» Article (as published): Web, via publisher
» Supplemental information: Multiple files via publisher

Becker, K. W., J. R. Collins, B. P. Durham, R. D. Groussman, A. E. White, H. F. Fredricks, J. E. Ossolinski, D. J. Repeta, P. Carini, E. V. Armbrust, and B. A. S. Van Mooy. 2018. Daily changes in phytoplankton lipidomes reveal mechanisms of energy storage in the open ocean. Nature Communications 9:5179; doi:10.1038/s41467-018-07346-z

Sunlight is the dominant control on phytoplankton biosynthetic activity, and darkness deprives them of their primary external energy source. Changes in the biochemical composition of phytoplankton communities over diel light cycles and attendant consequences for carbon and energy flux in environments remain poorly elucidated. Here we use lipidomic data from the North Pacific subtropical gyre to show that biosynthesis of energy-rich triacylglycerols (TAGs) by eukaryotic nanophytoplankton during the day and their subsequent consumption at night drives a large and previously uncharacterized daily carbon cycle. Diel oscillations in TAG concentration comprise 23 ± 11% of primary production by eukaryotic nanophytoplankton representing a global flux of about 2.4 Pg C yr−1. Metatranscriptomic analyses of genes required for TAG biosynthesis indicate that haptophytes and dinoflagellates are active members in TAG production. Estimates suggest that these organisms could contain as much as 40% more calories at sunset than at sunrise due to TAG production.

» Article (as published): PDF, via publisher
» Supplemental information: PDF
» Some code for my portions of the paper: R and Python scripts
» Supplemental data: Excel spreadsheet containing lipids identified using the LOBSTAHS software

J. R. Collins, H. F. Fredricks, J. S. Bowman, C. P. Ward, C. Moreno, K. Longnecker, A. Marchetti, C. M. Hansel, H. W. Ducklow, and B. A. S. Van Mooy. 2018. The molecular products and biogeochemical significance of lipid photooxidation in West Antarctic surface waters. Geochimica et Cosmochimica Acta 232:244–264; doi:10.1016/j.gca.2018.04.030

The seasonal depletion of stratospheric ozone over the Southern Hemisphere allows abnormally high doses of ultraviolet radiation (UVR) to reach surface waters of the West Antarctic Peninsula (WAP) in the austral spring, creating a natural laboratory for the study of lipid photooxidation in the shallow mixed layer of the marginal ice zone. The photooxidation of lipids under such conditions has been identified as a significant source of stress to microorganisms and short-chain fatty acids altered by photochemical processes have been found in both marine aerosols and sinking marine particle material. However, the biogeochemical impact of lipid photooxidation has not been quantitatively compared at ecosystem scale to the many other biological and abiotic processes that can transform particulate organic matter in the surface ocean. We combined results from field experiments with diverse environmental data, including high-resolution, accurate-mass HPLC-ESI-MS analysis of lipid extracts and in situ measurements of ultraviolet irradiance, to address several unresolved questions about lipid photooxidation in the marine environment. In our experiments, we used liposomes — nonliving, cell-like aggregations of lipids — to examine the photolability of various moieties of the intact polar diacylglycerol (IP-DAG) phosphatidylcholine (PC), a structural component of membranes in a broad range of microorganisms. We observed significant rates of photooxidation only when the molecule contained the polyunsaturated fatty acid (PUFA) docosahexaenoic acid (DHA). As the DHA-containing lipid was oxidized, we observed the steady ingrowth of a diversity of oxylipins and oxidized IP-DAG; our results suggest both the intact IP-DAG the degradation products were amenable to heterotrophic assimilation. To complement our experiments, we used an enhanced version of a new lipidomics discovery software package to identify the lipids in water column samples and in several diatom isolates. The galactolipid digalactosyldiacylglycerol (DGDG), the sulfolipid sulfoquinovosyldiacylglycerol (SQDG) and the phospholipids PC and phosphatidylglycerol (PG) accounted for the majority of IP-DAG in the water column particulate (≥ 0.2 µm) size fraction; between 3.4 and 5.3% of the IP-DAG contained fatty acids that were both highly polyunsaturated (i.e., each containing ≥ 5 double bonds). Using a broadband apparent quantum yield (AQY) that accounted for direct and Type I (i.e., radical-mediated) photooxidation of PUFA-containing IP-DAG, we estimated that 0.7 ± 0.2 µmol IP-DAG m-2 d-1 (0.5 ± 0.1 mg C m-2 d-1) were oxidized by photochemical processes in the mixed layer. This rate represented 4.4% (range, 3-21%) of the mean bacterial production rate measured in the same waters immediately following the retreat of the sea ice. Because our liposome experiments were not designed to account for oxidation by Type II photosensitized processes that often dominate in marine phytodetritus, our rate estimates may represent a sizeable underestimate of the true rate of lipid photooxidation in the water column. While production of such diverse oxidized lipids and oxylipins has been previously observed in terrestrial plants and mammals in response to biological stressors such as disease, we show here that a similar suite of molecules can be produced via an abiotic process in the environment and that the effect can be commensurate in magnitude with other ecosystem-scale biogeochemical processes.

» Article (as published): PDF, via publisher
» Article (author's preprint): PDF
» Supplemental information: PDF
» Code: R scripts used to produce all figures and model output
» Data: Diatom and water column lipid concentrations, UV radiation doses, and attenuation coefficients | PAL-LTER data, including nutrient concentrations and bacterial production rate measurements | NOAA Antarctic UV spectroradiometer data
» Detailed protocol: Liposome preparation, via protocols.io

J. R. Collins, P. D. Fucile, G. McDonald, J. E. Ossolinski, R. G. Keil, J. R. Valdes, S. C. Doney, and B. A. S. Van Mooy. 2018. An autonomous, in situ light-dark bottle device for determining community respiration and net community production. Limnology and Oceanography: Methods 16:323-338; doi:10.1002/lom3.10247

We describe a new, autonomous, incubation-based instrument that is deployed in situ to determine rates of gross community respiration and net community production in marine and aquatic ecosystems. During deployments at a coastal pier and in the open ocean, the PHORCYS (PHOtosynthesis and Respiration Comparison-Yielding System) captured dissolved oxygen fluxes over hourly timescales that were missed by traditional methods. The instrument uses fluorescence-quenching optodes fitted into separate light and dark chambers; these are opened and closed with piston-like actuators, allowing the instrument to make multiple, independent rate estimates in the course of each deployment. Consistent with other studies in which methods purporting to measure the same metabolic processes have yielded divergent results, respiration rate estimates from the PHORCYS were systematically higher than those calculated for the same waters using a traditional two-point Winkler titration technique. However, PHORCYS estimates of gross respiration agreed generally with separate incubations in bottles fitted with optode sensor spots. An Appendix describes a new method for estimating uncertainties in metabolic rates calculated from continuous dissolved oxygen data. Multiple successful, unattended deployments of the PHORCYS represent a small step toward fully autonomous observations of community metabolism. Yet the persistence of unexplained disagreements among aquatic metabolic rate estimates — such as those we observed between rates calculated with the PHORCYS and two existing, widely-accepted bottle-based methods — suggests that a new community intercalibration effort is warranted to address lingering sources of error in these critical measurements.

» Article (as published): PDF, via publisher
» Article (author's postprint): PDF
» Supplemental information: PDF
» Code: MATLAB and R scripts for processing of PHORCYS data (includes code, described in the Appendix, to estimate the uncertainty in a dissolved oxygen time-series from the effective degrees of freedom, Neff)
» Data: PHORCYS data (raw and processed) used in preparation of the manuscript

C. P. Laber, J. E. Hunter, F. Carvalho, J. R. Collins, E. J. Hunter, B. M. Schieler, E. Boss, K. More, M. Frada, K. Thamatrakoln, C. M. Brown, L. Haramaty, J. E. Ossolinski, H. F. Fredricks, J. I. Nissimov, R. Vandzura, U. Sheyn, Y. Lehahn, R. J. Chant, A. M. Martins, M. J. L. Coolen, A. Vardi, G. R. DiTullio, B. A. S. Van Mooy, and K. D. Bidle. 2018. Coccolithovirus facilitation of carbon export in the North Atlantic. Nature Microbiology 3:537–547; doi:10.1038/s41564-018-0128-4

Marine phytoplankton account for approximately half of global primary productivity, making their fate an important driver of the marine carbon cycle. Viruses are thought to recycle more than one-quarter of oceanic photosynthetically fixed organic carbon, which can stimulate nutrient regeneration, primary production and upper ocean respiration via lytic infection and the 'virus shunt'. Ultimately, this limits the trophic transfer of carbon and energy to both higher food webs and the deep ocean. Using imagery taken by the Moderate Resolution Imaging Spectroradiometer (MODIS) onboard the Aqua satellite, along with a suite of diagnostic lipid- and gene-based molecular biomarkers, in situ optical sensors and sediment traps, we show that Coccolithovirus infections of mesoscale (~100 km) Emiliania huxleyi blooms in the North Atlantic are coupled with particle aggregation, high zooplankton grazing and greater downward vertical fluxes of both particulate organic and particulate inorganic carbon from the upper mixed layer. Our analyses captured blooms in different phases of infection (early, late and post) and revealed the highest export flux in 'early-infected blooms' with sinking particles being disproportionately enriched with infected cells and subsequently remineralized at depth in the mesopelagic. Our findings reveal viral infection as a previously unrecognized ecosystem process enhancing biological pump efficiency.

» Article: PDF
» Supplementary information: PDF
» Code: MATLAB scripts for processing of sinking particle flux data and R scripts for determination of bottle-based respiration rates (my primary contribution) | C. P. Laber's MATLAB scripts for profiling floats, Cremin, spike signature analysis and particle origins, as well as for generating the satellite images
» Data: BCO-DMO KN207-1 cruise data | BCO-DMO KN207-3 cruise data | Additional data including flow cytometry counts

Fassbender, A. J., H. I. Palevsky, T. R. Martz, A. E. Ingalls, M. Gledhille, S. E. Fawcett. J. A. Brandes, L. I. Aluwihare, J. R. Collins and other participants of COME ABOARD and DISCO XXV. 2017. Perspectives on Chemical Oceanography in the 21st century: Participants of the COME ABOARD Meeting examine aspects of the field in the context of 40 years of DISCO. Marine Chemistry 196:181-190; doi:10.1016/j.marchem.2017.09.002

The questions that chemical oceanographers prioritize over the coming decades, and the methods we use to address these questions, will define our field's contribution to 21st century science. In recognition of this, the U.S. National Science Foundation and National Oceanic and Atmospheric Administration galvanized a community effort (the Chemical Oceanography MEeting: A BOttom-up Approach to Research Directions, or COME ABOARD) to synthesize bottom-up perspectives on selected areas of research in Chemical Oceanography. Representing only a small subset of the community, COME ABOARD participants did not attempt to identify targeted research directions for the field. Instead, we focused on how best to foster diverse research in Chemical Oceanography, placing emphasis on the following themes: strengthening our core chemical skillset; expanding our tools through collaboration with chemists, engineers, and computer scientists; considering new roles for large programs; enhancing interface research through interdisciplinary collaboration; and expanding ocean literacy by engaging with the public. For each theme, COME ABOARD participants reflected on the present state of Chemical Oceanography, where the community hopes to go and why, and actionable pathways to get there. A unifying concept among the discussions was that dissimilar funding structures and metrics of success may be required to accommodate the various levels of readiness and stages of knowledge development found throughout our community. In addition to the science, participants of the concurrent Dissertations Symposium in Chemical Oceanography (DISCO) XXV, a meeting of recent and forthcoming Ph.D. graduates in Chemical Oceanography, provided perspectives on how our field could show leadership in addressing long-standing diversity and early-career challenges that are pervasive throughout science. Here we summarize the COME ABOARD Meeting discussions, providing a synthesis of reflections and perspectives on the field.

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J. R. Collins, B. R. Edwards, H. F. Fredricks, and B. A. S. Van Mooy. 2016. LOBSTAHS: An adduct-based lipidomics strategy for discovery and identification of oxidative stress biomarkers. Analytical Chemistry 88:7154-7162; doi:10.1021/acs.analchem.6b01260

Discovery and identification of molecular biomarkers in large LC/MS datasets requires significant automation without loss of accuracy in the compound screening and annotation process. Here we describe a lipidomics workflow and open-source software package for high-throughput annotation and putative identification of lipid, oxidized lipid, and oxylipin biomarkers in high-mass-accuracy HPLC-MS data. Lipid and Oxylipin Biomarker Screening through Adduct Hierarchy Sequences, or LOBSTAHS, uses orthogonal screening criteria based on adduct ion formation patterns and other properties to identify thousands of compounds while providing the user with a confidence score for each assignment. Assignments are made from one of two customizable databases; the default databases contain 14,068 unique entries. To demonstrate the software's functionality, we screened more than 340,000 mass spectral features from an experiment in which hydrogen peroxide was used to induce oxidative stress in the marine diatom Phaeodactylum tricornutum. LOBSTAHS putatively identified 1,969 unique parent compounds in 21,869 features that survived the multi-stage screening process. While P. tricornutum maintained more than 92% of its core lipidome under oxidative stress, patterns in biomarker distribution and abundance indicated remodeling was both subtle and pervasive. Treatment with 150 μM H2O2 promoted statistically significant carbon-chain elongation across lipid classes, with the strongest elongation accompanying oxidation in moieties of monogalactosyldiacylglycerol, a lipid typically localized to the chloroplast. Oxidative stress also induced a pronounced reallocation of lipidome peak area to triacylglycerols. LOBSTAHS can be used with environmental or experimental data from a variety of systems and is freely available at https://github.com/vanmooylipidomics/LOBSTAHS.

» Article: PDF
» Supporting information, including detailed instructions for reproduction of results and figures: PDF
» Software: "LOBSTAHS" R package
» Code: R scripts used for data analysis and generation of figures
» Data: Thermo .raw data files | "PtH2O2lipids" R package; processed data in xcms and LOBSTAHS objects

J. R. Collins, B. R. Edwards, K. Thamatrakoln, J. E. Ossolinski, G. R. DiTullio, K. D. Bidle, S. C. Doney, and B. A. S. Van Mooy. 2015. The multiple fates of sinking particles in the North Atlantic Ocean. Global Biogeochemical Cycles 29:1471-1494; doi:10.1002/2014GB005037

The direct respiration of sinking organic matter by attached bacteria is often invoked as the dominant sink for settling particles in the mesopelagic ocean. However, other processes, such as enzymatic solubilization and mechanical disaggregation, also contribute to particle flux attenuation by transferring organic matter to the water column. Here we use observations from the North Atlantic Ocean, coupled to sensitivity analyses of a simple model, to assess the relative importance of particle-attached microbial respiration compared to the other processes that can degrade sinking particles. The observed carbon fluxes, bacterial production rates, and respiration by water column and particle-attached microbial communities each spanned more than an order of magnitude. Rates of substrate-specific respiration on sinking particle material ranged from 0.007 ± 0.003 to 0.173 ± 0.105 day-1. A comparison of these substrate-specific respiration rates with model results suggested sinking particle material was transferred to the water column by various biological and mechanical processes nearly 3.5 times as fast as it was directly respired. This finding, coupled with strong metabolic demand imposed by measurements of water column respiration (729.3 ± 266.0 mg C m-2 d-1, on average, over the 50 to 150 m depth interval), suggested a large fraction of the organic matter evolved from sinking particles ultimately met its fate through subsequent remineralization in the water column. At three sites, we also measured very low bacterial growth efficiencies and large discrepancies between depth-integrated mesopelagic respiration and carbon inputs.

» Article: PDF
» Supplementary information: PDF
» Code: MATLAB & R scripts for model and figures | MATLAB scripts for analysis of bacterial production data
» Cruise data: KN207-1 | KN207-3

J. R. Collins, P. A. Raymond, W. F. Bohlen, and M. M. Howard-Strobel. 2013. Estimates of new and total productivity in central Long Island Sound from in situ measurements of nitrate and dissolved oxygen. Estuaries and Coasts 36:74-97; doi:10.1007/s12237-012-9560-5

Biogeochemical cycles in estuaries are regulated by a diverse set of physical and biological variables that operate over a variety of time scales. Using in situ optical sensors, we conducted a high-frequency time-series study of several biogeochemical parameters at a mooring in central Long Island Sound from May to August 2010. During this period, we documented well-defined diel cycles in nitrate concentration that were correlated to dissolved oxygen, wind stress, tidal mixing, and irradiance. By filtering the data to separate the nitrate time series into various signal components, we estimated the amount of variation that could be ascribed to each process. Primary production and surface wind stress explained 59 and 19%, respectively, of the variation in nitrate concentrations. Less frequent physical forcings, including large-magnitude wind events and spring tides, served to decouple the relationship between oxygen, nitrate, and sunlight on about one quarter of study days. Daytime nitrate minima and dissolved oxygen maxima occurred nearly simultaneously on the majority (>80 %) of days during the study period; both were strongly correlated with the daily peak in irradiance. Nighttime nitrate maxima reflected a pattern in which surface-layer stocks were depleted each afternoon and recharged the following night. Changes in nitrate concentrations were used to generate daily estimates of new primary production (182 ± 37 mg C m-2 day-1) and the ƒ ratio (0.25), i.e., the ratio of production based on nitrate to total production. These estimates, the first of their kind in Long Island Sound, were compared to values of community respiration, primary productivity, and net ecosystem metabolism, which were derived from in situ measurements of oxygen concentration. Daily averages of the three metabolic parameters were 1,660 ± 431, 2,080 ± 419, and 429 ± 203 mg C m-2 day-1, respectively. While the system remained weakly autotrophic over the duration of the study period, we observed very large day-to-day differences in the ƒ ratio and in the various metabolic parameters.

» Article: PDF
» Data: Excel files containing all data and calculations