Description: Author Posting. © The Author(s), 2018. This is the author's version of the work. It is posted here under a nonexclusive, irrevocable, paid-up, worldwide license granted to WHOI. It is made available for personal use, not for redistribution. The definitive version was published in Geochimica et Cosmochimica Acta 232 (2018): 244-264, doi:10.1016/j.gca.2018.04.030.

Description: 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 IPDAG 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.

Description: J.R.C. acknowledges support from a U.S. Environmental Protection Agency (EPA) STAR Graduate Fellowship (Fellowship Assistance agreement FP-91744301-0). This work was also supported by U.S. National Science Foundation awards OCE-1059884 and PLR-1543328 to B.A.S.V.M., NSF award PLR- 1341479 to A. M., the Gordon and Betty Moore Foundation through grant GBMF3301 to B.A.S.V.M., and a WHOI Ocean Ventures Fund award to J.R.C.

Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Kim, H. H., Bowman, J. S., Luo, Y.-W., Ducklow, H. W., Schofield, O. M., Steinberg, D. K., & Doney, S. C. Modeling polar marine ecosystem functions guided by bacterial physiological and taxonomic traits. Biogeosciences, 19(1), (2022): 117–136, https://doi.org/10.5194/bg-19-117-2022.

Description: Heterotrophic marine bacteria utilize organic carbon for growth and biomass synthesis. Thus, their physiological variability is key to the balance between the production and consumption of organic matter and ultimately particle export in the ocean. Here we investigate a potential link between bacterial traits and ecosystem functions in the rapidly warming West Antarctic Peninsula (WAP) region based on a bacteria-oriented ecosystem model. Using a data assimilation scheme, we utilize the observations of bacterial groups with different physiological traits to constrain the group-specific bacterial ecosystem functions in the model. We then examine the association of the modeled bacterial and other key ecosystem functions with eight recurrent modes representative of different bacterial taxonomic traits. Both taxonomic and physiological traits reflect the variability in bacterial carbon demand, net primary production, and particle sinking flux. Numerical experiments under perturbed climate conditions demonstrate a potential shift from low nucleic acid bacteria to high nucleic acid bacteria-dominated communities in the coastal WAP. Our study suggests that bacterial diversity via different taxonomic and physiological traits can guide the modeling of the polar marine ecosystem functions under climate change.

Description: This research has been supported by the NASA (grant no. NNX14AL86G) and the NSF (grant no. PLR-1440435).

Description: To investigate the balance between net photo- and heterotrophy throughout the Arctic autumn-winter-spring transition, we assessed the abundances of O2 and Ar in surface waters by means of membrane-inlet mass spectrometry . We derived biologically mediated O2 super-/undersaturation (ΔO2/Ar), reflecting the difference between gross primary production and the community’s combined autotrophic and heterotrophic respiration (i.e., ‘net community production’, NCP). We present first results on the magnitude of NCP over the autumn-winter-spring transition and extrapolate biological carbon drawdown and release. Further correlation with biological and chemical parameters assessed during MOSAiC is used to identify the controls on net community production and to better understand the ecological mechanisms that drive biogeochemical fluxes in the rapidly changing Arctic.

Description: © The Author(s), 2021 This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Bowman, J. S., Van Mooy, B. A. S., Lowenstein, D. P., Fredricks, H. F., Hansel, C. M., Gast, R., Collins, J. R., Couto, N., & Ducklow, H. W. Whole community metatranscriptomes and lipidomes reveal diverse responses among antarctic phytoplankton to changing ice conditions. Frontiers in Marine Science, 8,(2021): 593566, https://doi.org/10.3389/fmars.2021.593566.

Description: 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.

Description: JB was supported by NSF-OPP 1641019, NSF-OPP 1846837, and the Simons Foundation Early Career Marine Microbial Investigator program. BV, DL and JC were supported by NSF (OPP-1543328 and OCE-1756254). CH was supported by NSF OCE-1355720. The Palmer LTER project is support by NSF-OPP 1440435. A small-scale Community Sequencing Project (CSP) award from the DOE Joint Genome Institute supported part of the sequencing effort.

Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Sutherland, K. M., Coe, A., Gast, R. J., Plummer, S., Suffridge, C. P., Diaz, J. M., Bowman, J. S., Wankel, S. D., & Hansel, C. M. Extracellular superoxide production by key microbes in the global ocean. Limnology and Oceanography, (2019), doi:10.1002/lno.11247.

Description: Bacteria and eukaryotes produce the reactive oxygen species superoxide both within and outside the cell. Although superoxide is typically associated with the detrimental and sometimes fatal effects of oxidative stress, it has also been shown to be involved in a range of essential biochemical processes, including cell signaling, growth, differentiation, and defense. Light‐independent extracellular superoxide production has been shown to be widespread among many marine heterotrophs and phytoplankton, but the extent to which this trait is relevant to marine microbial physiology and ecology throughout the global ocean is unknown. Here, we investigate the dark extracellular superoxide production of five groups of organisms that are geographically widespread and represent some of the most abundant organisms in the global ocean. These include Prochlorococcus, Synechococcus, Pelagibacter, Phaeocystis, and Geminigera. Cell‐normalized net extracellular superoxide production rates ranged seven orders of magnitude, from undetectable to 14,830 amol cell−1 h−1, with the cyanobacterium Prochlorococcus being the lowest producer and the cryptophyte Geminigera being the most prolific producer. Extracellular superoxide production exhibited a strong inverse relationship with cell number, pointing to a potential role in cell signaling. We demonstrate that rapid, cell‐number–dependent changes in the net superoxide production rate by Synechococcus and Pelagibacter arose primarily from changes in gross production of extracellular superoxide, not decay. These results expand the relevance of dark extracellular superoxide production to key marine microbes of the global ocean, suggesting that superoxide production in marine waters is regulated by a diverse suite of marine organisms in both dark and sunlit waters.

Description: The authors would like to acknowledge their funding sources including NASA NESSF NNX15AR62H (K.M.S.), NASA Exobiology grant NNX15AM04G to S.D.W. and C.M.H., NSF‐OCE grant 1355720 to C.M.H., NSF‐OPP 1641019 (J.S.B), and Simons Foundation SCOPE Award ID 329108 (Sallie W. Chisholm). The authors would also like to thank the Harvey lab (Skidaway Institute of Oceanography) for use of their flow cytometer in this study. We thank Stephen Giovannoni and Sallie Chisholm for providing bacteria strains and laboratory facilities. Additional thanks to Marianne Acker, Rogier Braakman, and Aldo Arellano for assistance in lab and helpful conversations.

Description: Global biodiversity loss and mass extinction of species are two of the most critical environmental issues the world is currently facing, resulting in the disruption of various ecosystems central to environmental functions and human health. Microbiome-targeted interventions, such as probiotics and microbiome transplants, are emerging as potential options to reverse deterioration of biodiversity and increase the resilience of wildlife and ecosystems. However, the implementation of these interventions is urgently needed. We summarize the current concepts, bottlenecks and ethical aspects encompassing the careful and responsible management of ecosystem resources using the microbiome (termed microbiome stewardship) to rehabilitate organisms and ecosystem functions. We propose a real-world application framework to guide environmental and wildlife probiotic applications. This framework details steps that must be taken in the upscaling process while weighing risks against the high toll of inaction. In doing so, we draw parallels with other aspects of contemporary science moving swiftly in the face of urgent global challenges.