Dissolved Organic Phosphorus Production during Simulated Phytoplankton Blooms in a Coastal Upwelling System

Dissolved organic phosphorus (DOP) is increasingly recognized as an important phosphorus source to marine primary producers. Despite its importance, the production rate and fate of DOP is poorly understood. In this study, patterns of DOP production were evaluated by tracking the evolution of DOP during simulated phytoplankton blooms initiated with nutrient amended surface waters, relative to controls, from the Oregon (USA) coastal upwelling system. Nitrogen (N) and phosphorus (P) additions were used to decouple DOP production and hydrolysis by inducing or repressing, respectively, community alkaline phosphatase activity. In order to examine the progression of nutrient uptake and DOP production under upwelling versus relaxation conditions, two experiments were initiated with waters collected during upwelling events, and two with waters collected during relaxation events. Maximum [under (+P) conditions] and minimum [under (+N) conditions] DOP production rates were calculated and applied to in situ DOP levels to evaluate which end-member rate most closely approximates the in situ DOP production rate at the four study sites in this coastal system. Increases in DOP concentration occurred by day-5 in control treatments in all experiments. N treatments displayed increased chlorophyll a, increased alkaline phosphatase activity, and yielded lower net DOP production rates relative to controls, suggesting that DOP levels were depressed as a consequence of increased hydrolysis of bioavailable DOP substrates. Phosphorus additions resulted in a significant net production of DOP at all stations, but no increase in chlorophyll a relative to control treatments. The contrasting patterns in DOP production between treatments suggests that changes in the ambient dissolved inorganic nitrogen:dissolved inorganic phosphorus (DIN:DIP) ratio could exert profound control over DOP production rates in this system. Patterns of DOP production across the different experiments also suggest that bathymetry-driven differences in water residence times can influence DOP cycling. Taken together, these factors may impact the potential export of DOP to offshore ecosystems

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

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

Evidence for the linked biogeochemical cycling of zinc, cobalt, and phosphorus in the western North Atlantic Ocean

Author Posting. © American Geophysical Union, 2008. 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 22 (2008): GB4012, doi:10.1029/2007GB003119.Many trace metals such as iron, copper, and manganese have lower concentrations in the surface waters of the North Pacific Ocean than in North Atlantic surface waters. However, cobalt and zinc concentrations in North Atlantic surface waters are often as low as those reported in the North Pacific. We studied the relationship between the distribution of cobalt, zinc, and phosphorus in surface waters of the western North Atlantic Ocean. Both metals show strong depletion in the southern Sargasso Sea, a region characterized by exceedingly low dissolved inorganic phosphorus (generally <4 nmol L−1) and measurable alkaline phosphatase activity. Alkaline phosphatase is a metalloenzyme (typically containing zinc) that cleaves phosphate monoesters and is a diagnostic indicator of phosphorus stress in phytoplankton. In contrast to the North Pacific Ocean, cobalt and zinc appear to be drawn down to their lowest values only when inorganic phosphorus is below 10 nmol L−1 in the North Atlantic Ocean. Lower levels of phosphorus in the Atlantic may contribute to these differences, possibly through an increased biological demand for zinc and cobalt associated with dissolved organic phosphorus acquisition. This hypothesis is consistent with results of a culture study where alkaline phosphatase activity decreased in the model coccolithophore Emiliania huxleyi upon zinc and cobalt limitation.This research was supported by NSF grant OCE- 0136835 to J.W.M. and S.D. R.W.J. was supported by an EPA STAR Fellowship

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

Proteome changes driven by phosphorus deficiency and recovery in the brown tide-forming alga Aureococcus anophagefferens

© The Author(s), 2011. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS One 6 (2011): e28949, doi:10.1371/journal.pone.0028949.Shotgun mass spectrometry was used to detect proteins in the harmful alga, Aureococcus anophagefferens, and monitor their relative abundance across nutrient replete (control), phosphate-deficient (−P) and −P refed with phosphate (P-refed) conditions. Spectral counting techniques identified differentially abundant proteins and demonstrated that under phosphate deficiency, A. anophagefferens increases proteins involved in both inorganic and organic phosphorus (P) scavenging, including a phosphate transporter, 5′-nucleotidase, and alkaline phosphatase. Additionally, an increase in abundance of a sulfolipid biosynthesis protein was detected in −P and P-refed conditions. Analysis of the polar membrane lipids showed that cellular concentrations of the sulfolipid sulphoquinovosyldiacylglycerol (SQDG) were nearly two-fold greater in the −P condition versus the control condition, while cellular phospholipids were approximately 8-fold less. Transcript and protein abundances were more tightly coupled for gene products involved in P metabolism compared to those involved in a range of other metabolic functions. Comparison of protein abundances between the −P and P-refed conditions identified differences in the timing of protein degradation and turnover. This suggests that culture studies examining nutrient starvation responses will be valuable in interpreting protein abundance patterns for cellular nutritional status and history in metaproteomic datasets.Research for this work was supported by a National Oceanic and Atmospheric Administration ECOHAB grant (#NA09NOS4780206) and National Science Foundation grant (#OCE-0723667) and a STAR Research Assistance Agreement No. R-83041501-0 awarded by the U.S. Environmental Protection Agency. Further support came from the Woods Hole Coastal Ocean Institute. LLW was supported by a Environmental Protection Agency STAR Fellowship (#FP916901). EMB was supported by a National Science Foundation (NSF) Graduate Research Fellowship (#2007037200) and an Environmental Protection Agency STAR Fellowship (#F6E20324)

Short-term variability in euphotic zone biogeochemistry and primary productivity at Station ALOHA : a case study of summer 2012

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): 1145–1164, doi:10.1002/2015GB005141.Time-series observations are critical to understand the structure, function, and dynamics of marine ecosystems. The Hawaii Ocean Time-series program has maintained near-monthly sampling at Station ALOHA (22°45′N, 158°00′W) in the oligotrophic North Pacific Subtropical Gyre (NPSG) since 1988 and has identified ecosystem variability over seasonal to interannual timescales. To further extend the temporal resolution of these near-monthly time-series observations, an extensive field campaign was conducted during July–September 2012 at Station ALOHA with near-daily sampling of upper water-column biogeochemistry, phytoplankton abundance, and activity. The resulting data set provided biogeochemical measurements at high temporal resolution and documents two important events at Station ALOHA: (1) a prolonged period of low productivity when net community production in the mixed layer shifted to a net heterotrophic state and (2) detection of a distinct sea-surface salinity minimum feature which was prominent in the upper water column (0–50 m) for a period of approximately 30 days. The shipboard observations during July–September 2012 were supplemented with in situ measurements provided by Seagliders, profiling floats, and remote satellite observations that together revealed the extent of the low productivity and the sea-surface salinity minimum feature in the NPSG.NOAA Climate Observation Division; National Science Foundation (NSF) Center for Microbial Oceanography: Research and Education (C-MORE) Grant Numbers: EF0424599, OCE-1153656, OCE-1260164; Gordon and Betty Moore Foundation Marine Microbiology Investigator2016-02-1

Empirical bayes analysis of sequencing-based transcriptional profiling without replicates

Background: Recent technological advancements have made high throughput sequencing an increasingly popular approach for transcriptome analysis. Advantages of sequencing-based transcriptional profiling over microarrays have been reported, including lower technical variability. However, advances in technology do not remove biological variation between replicates and this variation is often neglected in many analyses. Results: We propose an empirical Bayes method, titled Analysis of Sequence Counts (ASC), to detect differential expression based on sequencing technology. ASC borrows information across sequences to establish prior distribution of sample variation, so that biological variation can be accounted for even when replicates are not available. Compared to current approaches that simply tests for equality of proportions in two samples, ASC is less biased towards highly expressed sequences and can identify more genes with a greater log fold change at lower overall abundance. Conclusions: ASC unifies the biological and statistical significance of differential expression by estimating the posterior mean of log fold change and estimating false discovery rates based on the posterior mean. The implementation in R is available at http://www.stat.brown.edu/Zwu/research.aspx

Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics

Author Posting. © The Author(s), 2011. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 108 (2011): 4352-4357, doi:10.1073/pnas.1016106108.Harmful algal blooms (HABs) cause significant economic and ecological damage worldwide. Despite considerable efforts, a comprehensive understanding of the factors that promote these blooms has been lacking because the biochemical pathways that facilitate their dominance relative to other phytoplankton within specific environments have not been identified. Here, biogeochemical measurements demonstrated that the harmful 43 Aureococcus anophagefferens outcompeted co-occurring phytoplankton in estuaries with elevated levels of dissolved organic matter and turbidity and low levels of dissolved inorganic nitrogen. We subsequently sequenced the first HAB genome (A. anophagefferens) and compared its gene complement to those of six competing phytoplankton species identified via metaproteomics. Using an ecogenomic approach, we specifically focused on the gene sets that may facilitate dominance within the environmental conditions present during blooms. A. anophagefferens possesses a larger genome (56 mbp) and more genes involved in light harvesting, organic carbon and nitrogen utilization, and encoding selenium- and metal-requiring enzymes than competing phytoplankton. Genes for the synthesis of microbial deterrents likely permit the proliferation of this species with reduced mortality losses during blooms. Collectively, these findings suggest that anthropogenic activities resulting in elevated levels of turbidity, organic matter, and metals have opened a niche within coastal ecosystems that ideally suits the unique genetic capacity of A. anophagefferens and thus has facilitated the proliferation of this and potentially other HABs.Joint Genome Institute is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. Efforts were also supported by awards from New York Sea Grant to Stony Brook University, National Oceanic and Atmospheric Administration Center for Sponsored Coastal Ocean Research award #NA09NOS4780206 to Woods Hole Oceanographic Institution, NIH grant GM061603 to Harvard University, and NSF award IOS-0841918 to The University of Tennessee