Microbes and the marine phosphorus cycle

Author Posting. © Oceanography Society, 2007. This article is posted here by permission of Oceanography Society for personal use, not for redistribution. The definitive version was published in Oceanography 20, 2 (2007): 110-116.Phosphorus (P) is fundamental to life, and years of study in marine systems have built a broad understanding of the marine P cycle. Various aspects of marine P biogeochemistry have been reviewed previously (Benitez-Nelson, 2000; Paytan and McLaughlin, 2007). Here, we focus on recent advances in our understanding of marine P and the interactions between microbes and the P cycle. These advances come from a variety of disciplines, but generally highlight three main themes: (1) ocean microbes are adapted for surviving in a variable P environment, (2) the dissolved organic phosphorus (DOP) pool likely plays a critical role in driving growth, metabolism, and community composition of ocean microorganisms, and (3) P is very rapidly cycled, which highlights its importance in marine systems

Sinking phytoplankton associated with carbon flux in the Atlantic Ocean

© The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Limnology and Oceanography 61 (2016): 1172–1187, doi:10.1002/lno.10253.The composition of sinking particles and the mechanisms leading to their transport ultimately control how much carbon is naturally sequestered in the deep ocean by the “biological pump.” While detrital particles often contain much of the sinking carbon, sinking of intact phytoplankton cells can also contribute to carbon export, which represents a direct flux of carbon from the atmosphere to the deep ocean by circumventing the surface ocean food web. Phytoplankton that contributed to carbon flux were identified in sinking material collected by short-term sediment trap deployments conducted along a transect off the eastern shore of South America. Particulate organic carbon flux at 125 m depth did not change significantly along the transect. Instead, changes occurred in the composition and association of phytoplankton with detrital particles. The fluxes of diatoms, coccolithophores, dinoflagellates, and nano-sized cells at 125 m were unrelated to the overlying surface population abundances, indicating that functional-group specific transport mechanisms were variable across locations. The dominant export mechanism of phytoplankton at each station was putatively identified by principal component analysis and fell into one of three categories; (1) transport and sinking of individual, viable diatom cells, (2) transport by aggregates and fecal pellets, or (3) enhanced export of coccolithophores through direct settling and/or aggregationFunding for the DeepDOM cruise was provided by the National Science Foundation (NSF) grant OCE-1154320 to E. B. Kujawinski and K. Longnecker, WHOI. Partial research support was provided by NSF through grants OCE-0925284, and OCE-1316036 to S.T. Dyhrman. C.A. Durkin was supported by a Woods Hole Oceanographic Institution Devonshire Postdoctoral Scholarship

Growth and specific P-uptake rates of bacterial and phytoplanktonic communities in the Southeast Pacific (BIOSOPE cruise)

© 2007 Author(s) et al. This is an open-access article distributed under the terms of a Creative Commons License. The definitive version was published in Biogeosciences 4 (2007): 941-956, doi:10.5194/bg-4-941-2007Predicting heterotrophic bacteria and phytoplankton specific growth rates (μ) is of great scientific interest. Many methods have been developed in order to assess bacterial or phytoplankton μ. One widely used method is to estimate μ from data obtained on biomass or cell abundance and rates of biomass or cell production. According to Kirchman (2002), the most appropriate approach for estimating μ is simply to divide the production rate by the biomass or cell abundance estimate. Most methods using this approach to estimate μ are based on carbon (C) incorporation rates and C biomass measurements. Nevertheless it is also possible to estimate μ using phosphate (P) data. We showed that particulate phosphate (PartP) can be used to estimate biomass and that the P uptake rate to PartP ratio can be employed to assess μ. Contrary to other methods using C, this estimator does not need conversion factors and provides an evaluation of μ for both autotrophic and heterotrophic organisms. We report values of P-based μ in three size fractions (0.2–0.6; 0.6–2 and >2 μm) along a Southeast Pacific transect, over a wide range of P-replete trophic status. P-based μ values were higher in the 0.6–2 μm fraction than in the >2 μm fraction, suggesting that picoplankton-sized cells grew faster than the larger cells, whatever the trophic regime encountered. Picoplankton-sized cells grew significantly faster in the deep chlorophyll maximum layer than in the upper part of the photic zone in the oligotrophic gyre area, suggesting that picoplankton might outcompete >2 μm cells in this particular high-nutrient, low-light environment. P-based μ attributed to free-living bacteria (0.2-0.6 μm) and picoplankton (0.6–2 μm) size-fractions were relatively low (0.11±0.07 d−1 and 0.14±0.04 d−1, respectively) in the Southeast Pacific gyre, suggesting that the microbial community turns over very slowly.This research was funded by the Centre National de la Recherche Scientifique (CNRS), the Institut des Sciences de l’Univers (INSU), the Centre National d’Etudes Spatiales (CNES), the European Space Agency (ESA), The National Aeronautics and Space Administration (NASA) and the Natural Sciences and Engineering Research Council of Canada (NSERC). This work is funded in part by the French Research and Education council

Resource allocation by the marine cyanobacterium Synechococcus WH8102 in response to different nutrient supply ratios

Differences in relative availability of nitrate vs. phosphate may contribute to regional variations in plankton elemental stoichiometry. As a representative of the globally abundant marine Synechococcus, strain WH8102 was grown in 16 chemostats up to 52  d at a fixed growth rate with nitrogen–phosphorus ratios (N : Psupply) of 1–50. Initially, the phosphate and nitrate concentrations in the vessel decreased when the respective nutrient was limiting. Cell growth generally stabilized, although several chemostats had apparent oscillations in biomass. We observed extensive plasticity in the elemental content and ratios. N : Pcell matched the supply values between N : Psupply 5 and 20. The C : Pcell followed a similar trend. In contrast, the mean C : Ncell was 6.8 and did not vary as a function of supply ratios. We also observed that induction of alkaline phosphatase, the fraction of P allocated to nucleic acids, and the lipid sulfoquinovosyldiacylglycerol : phosphatidyglycerol ratio inversely correlated with P availability. Our results suggest that this extensive plasticity in the elemental content and ratios depends both on the external nutrient availability as well as past growth history. Thus, our study provides a quantitative understanding of the regulation of the elemental stoichiometry of an abundant ocean phytoplankton lineage

Temperature-induced viral resistance in Emiliania huxleyi (Prymnesiophyceae)

© The Author(s), 2014. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS One 9 (2014): e112134, doi:10.1371/journal.pone.0112134.Annual Emiliania huxleyi blooms (along with other coccolithophorid species) play important roles in the global carbon and sulfur cycles. E. huxleyi blooms are routinely terminated by large, host-specific dsDNA viruses, (Emiliania huxleyi Viruses; EhVs), making these host-virus interactions a driving force behind their potential impact on global biogeochemical cycles. Given projected increases in sea surface temperature due to climate change, it is imperative to understand the effects of temperature on E. huxleyi’s susceptibility to viral infection and its production of climatically active dimethylated sulfur species (DSS). Here we demonstrate that a 3°C increase in temperature induces EhV-resistant phenotypes in three E. huxleyi strains and that successful virus infection impacts DSS pool sizes. We also examined cellular polar lipids, given their documented roles in regulating host-virus interactions in this system, and propose that alterations to membrane-bound surface receptors are responsible for the observed temperature-induced resistance. Our findings have potential implications for global biogeochemical cycles in a warming climate and for deciphering the particular mechanism(s) by which some E. huxleyi strains exhibit viral resistance.This study was supported by funding from the National Science Foundation (OCE-1061883 to KDB, BVM, and OCE-1061876 to GRD) and in part by grants from The Gordon and Betty Moore Foundation (to BVM and KDB)

Dynamics of extracellular superoxide production by Trichodesmium colonies from the Sargasso Sea

Author Posting. © Association for the Sciences of Limnology and Oceanography, 2016. This article is posted here by permission of Association for the Sciences of Limnology and Oceanography for personal use, not for redistribution. The definitive version was published in Limnology and Oceanography 61 (2016): 1188–1200, doi:10.1002/lno.10266.Reactive oxygen species (ROS) are key players in the health and biogeochemistry of the ocean and its inhabitants. The vital contribution of microorganisms to marine ROS levels, particularly superoxide, has only recently come to light, and thus the specific biological sources and pathways involved in ROS production are largely unknown. To better understand the biogenic controls on ROS levels in tropical oligotrophic systems, we determined rates of superoxide production under various conditions by natural populations of the nitrogen-fixing diazotroph Trichodesmium obtained from various surface waters in the Sargasso Sea. Trichodesmium colonies collected from eight different stations all produced extracellular superoxide at high rates in both the dark and light. Colony density and light had a variable impact on extracellular superoxide production depending on the morphology of the Trichodesmium colonies. Raft morphotypes showed a rapid increase in superoxide production in response to even low levels of light, which was not observed for puff colonies. In contrast, superoxide production rates per colony decreased with increasing colony density for puff morphotypes but not for rafts. These findings point to Trichodesmium as a likely key source of ROS to the surface oligotrophic ocean. The physiological and/or ecological factors underpinning morphology-dependent controls on superoxide production need to be unveiled to better understand and predict superoxide production by Trichodesmium and ROS dynamics within marine systems.Major support for this work was provided by NSF OCE- 1246174 to CMH, NSF OCE-1332912 to STD and NSF OCE-13329898 to BASVM

Combined pigment and metatranscriptomic analysis reveals highly synchronized diel patterns of phenotypic light response across domains in the open oligotrophic ocean

Sunlight is the most important environmental control on diel fluctuations in phytoplankton activity, and understanding diel microbial processes is essential to the study of oceanic biogeochemical cycles. Yet, little is known about the in situ temporal dynamics of phytoplankton metabolic activities and their coordination across different populations. We investigated diel orchestration of phytoplankton activity in photosynthesis, photoacclimation, and photoprotection by analyzing pigment and quinone distributions in combination with metatranscriptomes in surface waters of the North Pacific Subtropical Gyre (NPSG). We found diel cycles in pigment abundances resulting from the balance of their synthesis and consumption. These dynamics suggest that night represents a metabolic recovery phase, refilling cellular pigment stores, while photosystems are remodeled towards photoprotection during daytime. Transcript levels of genes involved in photosynthesis and pigment metabolism had synchronized diel expression patterns among all taxa, reflecting the driving force light imparts upon photosynthetic organisms in the ocean, while other environmental factors drive niche differentiation. For instance, observed decoupling of diel oscillations in transcripts and related pigments indicates that pigment abundances are modulated by environmental factors extending beyond gene expression/regulation reinforcing the need to combine metatranscriptomics with proteomics and metabolomics to fully understand the timing of these critical processes in situ

An autonomous, in situ light-dark bottle device for determining community respiration and net community production

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 Limnology and Oceanography-Methods 16 (2018): 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.This research was supported by the U.S. National Science Foundation (awards OCE-1155438 to B.A.S.V.M., J.R.V., and R.G.K., and OCE- 1059884 to B.A.S.V.M.), the Woods Hole Oceanographic Institution through a Cecil and Ida Green Foundation Innovative Technology Award and an Interdisciplinary Science Award, and a U.S. Environmental Protection Agency (EPA) STAR Graduate Fellowship to J.R.C. under Fellowship Assistance Agreement no. FP-91744301-0

The multiple fates of sinking particles in the North Atlantic Ocean

Author Posting. © American Geophysical Union, 2015. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Global Biogeochemical Cycles 29 (2015): 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.U.S. Environmental Protection Agency (EPA) STAR Grant Number: FP-91744301-0; National Science Foundation Grant Numbers OCE-1061883, EF-0424599, OCE-1155438, OCE-1059884, OCE-1031143; Gordon and Betty Moore Foundation Grant Numbers: 3301, 3789; Gordon and Betty Moore Foundation; Woods Hole Oceanographic Institution2016-03-2

Metabolite composition of sinking particles differs from surface suspended particles across a latitudinal transect in the South Atlantic

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in [citation], doi:[doi]. Johnson, W. M., Longnecker, K., Soule, M. C. K., Arnold, W. A., Bhatia, M. P., Hallam, S. J., Van Mooy, B. A. S., & Kujawinski, E. B. Metabolite composition of sinking particles differs from surface suspended particles across a latitudinal transect in the South Atlantic. Limnology and Oceanography, (2019), doi:10.1002/lno.11255.Marine sinking particles transport carbon from the surface and bury it in deep‐sea sediments, where it can be sequestered on geologic time scales. The combination of the surface ocean food web that produces these particles and the particle‐associated microbial community that degrades them creates a complex set of variables that control organic matter cycling. We use targeted metabolomics to characterize a suite of small biomolecules, or metabolites, in sinking particles and compare their metabolite composition to that of the suspended particles in the euphotic zone from which they are likely derived. These samples were collected in the South Atlantic subtropical gyre, as well as in the equatorial Atlantic region and the Amazon River plume. The composition of targeted metabolites in the sinking particles was relatively similar throughout the transect, despite the distinct oceanic regions in which they were generated. Metabolites possibly derived from the degradation of nucleic acids and lipids, such as xanthine and glycine betaine, were an increased mole fraction of the targeted metabolites in the sinking particles relative to surface suspended particles, while algal‐derived metabolites like the osmolyte dimethylsulfoniopropionate were a smaller fraction of the observed metabolites on the sinking particles. These compositional changes are shaped both by the removal of metabolites associated with detritus delivered from the surface ocean and by production of metabolites by the sinking particle‐associated microbial communities. Furthermore, they provide a basis for examining the types and quantities of metabolites that may be delivered to the deep sea by sinking particles.The authors would like to thank the captain and crew of the R/V Knorr and R/V Atlantic Explorer, as well as Justin Ossolinski, Catherine Carmichael, and Sean Sylva for helping to make this data set possible. Special thanks to Colleen Durkin for sharing her data and providing feedback on the manuscript. Funding for this work came from the National Science Foundation (NSF Grant OCE‐1154320 to EBK and KL) and a WHOI Ocean Ventures Fund award to WMJ. The instruments in the WHOI FT‐MS Facility were purchased with support from the Gordon & Betty Moore Foundation and NSF. Support for WMJ was provided by a National Defense Science and Engineering Fellowship. Sequencing was performed under the auspices of the US Department of Energy (DOE) JGI Community Science Program (CSP) project (CSP 1685) supported by the Office of Science of US DOE Contract DE‐AC02‐ 05CH11231. Additional work related to sample collection and processing was supported by the G. Unger Vetlesen and Ambrose Monell Foundations, the Natural Sciences and Engineering Research Council of Canada (NSERC), the Canadian Institute for Advanced Study (CIFAR), and the Canada Foundation for Innovation through grants awarded to SJH. MPB was supported by a CIFAR Global Scholarship and NSERC postdoctoral fellowship