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1.
Proc Natl Acad Sci U S A ; 119(2)2022 01 11.
Article in English | MEDLINE | ID: mdl-34983874

ABSTRACT

Prochlorococcus is both the smallest and numerically most abundant photosynthesizing organism on the planet. While thriving in the warm oligotrophic gyres, Prochlorococcus concentrations drop rapidly in higher-latitude regions. Transect data from the North Pacific show the collapse occurring at a wide range of temperatures and latitudes (temperature is often hypothesized to cause this shift), suggesting an ecological mechanism may be at play. An often used size-based theory of phytoplankton community structure that has been incorporated into computational models correctly predicts the dominance of Prochlorococcus in the gyres, and the relative dominance of larger cells at high latitudes. However, both theory and computational models fail to explain the poleward collapse. When heterotrophic bacteria and predators that prey nonspecifically on both Prochlorococcus and bacteria are included in the theoretical framework, the collapse of Prochlorococcus occurs with increasing nutrient supplies. The poleward collapse of Prochlorococcus populations then naturally emerges when this mechanism of "shared predation" is implemented in a complex global ecosystem model. Additionally, the theory correctly predicts trends in both the abundance and mean size of the heterotrophic bacteria. These results suggest that ecological controls need to be considered to understand the biogeography of Prochlorococcus and predict its changes under future ocean conditions. Indirect interactions within a microbial network can be essential in setting community structure.


Subject(s)
Bacteria/metabolism , Heterotrophic Processes/physiology , Prochlorococcus/metabolism , Animals , Autotrophic Processes/physiology , Ecosystem , Models, Biological , Photosynthesis , Phytoplankton , Seawater/microbiology , Temperature , Zooplankton
2.
Proc Natl Acad Sci U S A ; 118(6)2021 02 09.
Article in English | MEDLINE | ID: mdl-33547239

ABSTRACT

The 24-h cycle of light and darkness governs daily rhythms of complex behaviors across all domains of life. Intracellular photoreceptors sense specific wavelengths of light that can reset the internal circadian clock and/or elicit distinct phenotypic responses. In the surface ocean, microbial communities additionally modulate nonrhythmic changes in light quality and quantity as they are mixed to different depths. Here, we show that eukaryotic plankton in the North Pacific Subtropical Gyre transcribe genes encoding light-sensitive proteins that may serve as light-activated transcription factors, elicit light-driven electrical/chemical cascades, or initiate secondary messenger-signaling cascades. Overall, the protistan community relies on blue light-sensitive photoreceptors of the cryptochrome/photolyase family, and proteins containing the Light-Oxygen-Voltage (LOV) domain. The greatest diversification occurred within Haptophyta and photosynthetic stramenopiles where the LOV domain was combined with different DNA-binding domains and secondary signal-transduction motifs. Flagellated protists utilize green-light sensory rhodopsins and blue-light helmchromes, potentially underlying phototactic/photophobic and other behaviors toward specific wavelengths of light. Photoreceptors such as phytochromes appear to play minor roles in the North Pacific Subtropical Gyre. Transcript abundance of environmental light-sensitive protein-encoding genes that display diel patterns are found to primarily peak at dawn. The exceptions are the LOV-domain transcription factors with peaks in transcript abundances at different times and putative phototaxis photoreceptors transcribed throughout the day. Together, these data illustrate the diversity of light-sensitive proteins that may allow disparate groups of protists to respond to light and potentially synchronize patterns of growth, division, and mortality within the dynamic ocean environment.


Subject(s)
Circadian Rhythm/genetics , Eukaryotic Cells/radiation effects , Light , Oceans and Seas , Plankton/growth & development , Plankton/radiation effects , Regulatory Sequences, Nucleic Acid/genetics , Transcription, Genetic/radiation effects , Chlamydomonas/genetics , Chlamydomonas/radiation effects , Circadian Rhythm/radiation effects , Eukaryotic Cells/metabolism , Photoreceptor Cells/metabolism , Phylogeny , Protein Domains , RNA, Messenger/genetics , RNA, Messenger/metabolism
3.
PLoS Comput Biol ; 18(1): e1009733, 2022 01.
Article in English | MEDLINE | ID: mdl-35030163

ABSTRACT

The rates of cell growth, division, and carbon loss of microbial populations are key parameters for understanding how organisms interact with their environment and how they contribute to the carbon cycle. However, the invasive nature of current analytical methods has hindered efforts to reliably quantify these parameters. In recent years, size-structured matrix population models (MPMs) have gained popularity for estimating division rates of microbial populations by mechanistically describing changes in microbial cell size distributions over time. Motivated by the mechanistic structure of these models, we employ a Bayesian approach to extend size-structured MPMs to capture additional biological processes describing the dynamics of a marine phytoplankton population over the day-night cycle. Our Bayesian framework is able to take prior scientific knowledge into account and generate biologically interpretable results. Using data from an exponentially growing laboratory culture of the cyanobacterium Prochlorococcus, we isolate respiratory and exudative carbon losses as critical parameters for the modeling of their population dynamics. The results suggest that this modeling framework can provide deeper insights into microbial population dynamics provided by size distribution time-series data.


Subject(s)
Bayes Theorem , Computational Biology/methods , Models, Biological , Phytoplankton/physiology , Population Dynamics , Time Factors
4.
Appl Opt ; 59(22): 6702-6716, 2020 Aug 01.
Article in English | MEDLINE | ID: mdl-32749375

ABSTRACT

Cross-platform observing systems are requisite to capturing the temporal and spatial dynamics of particles in the ocean. We present simultaneous observations of bulk optical properties, including the particulate beam attenuation (cp) and backscattering (bbp) coefficients, and particle size distributions collected in the North Pacific Subtropical Gyre. Clear and coherent diel cycles are observed in all bulk and size-fractionated optical proxies for particle biomass. We show evidence linking diurnal increases in cp and bbp to daytime particle growth and division of cells, with particles <7µm driving the daily cycle of particle production and loss within the mixed layer. Flow cytometry data reveal the nitrogen-fixing cyanobacterium Crocosphaera (∼4-7µm) to be an important driver of cp at the time of sampling, whereas Prochlorococcus dynamics (∼0.5µm) were essential to reproducing temporal variability in bbp. This study is a step towards improved characterization of the particle size range represented by in situ bulk optical properties and a better understanding of the mechanisms that drive variability in particle production in the oligotrophic open ocean.


Subject(s)
Cell Division , Optical Phenomena , Phytoplankton/cytology , Phytoplankton/growth & development , Tropical Climate , Biomass , Carbon/analysis , Chlorophyll A/analysis , Fluorometry , Pacific Ocean , Time Factors
5.
Proc Natl Acad Sci U S A ; 114(2): 364-369, 2017 01 10.
Article in English | MEDLINE | ID: mdl-28028206

ABSTRACT

Organisms within all domains of life require the cofactor cobalamin (vitamin B12), which is produced only by a subset of bacteria and archaea. On the basis of genomic analyses, cobalamin biosynthesis in marine systems has been inferred in three main groups: select heterotrophic Proteobacteria, chemoautotrophic Thaumarchaeota, and photoautotrophic Cyanobacteria. Culture work demonstrates that many Cyanobacteria do not synthesize cobalamin but rather produce pseudocobalamin, challenging the connection between the occurrence of cobalamin biosynthesis genes and production of the compound in marine ecosystems. Here we show that cobalamin and pseudocobalamin coexist in the surface ocean, have distinct microbial sources, and support different enzymatic demands. Even in the presence of cobalamin, Cyanobacteria synthesize pseudocobalamin-likely reflecting their retention of an oxygen-independent pathway to produce pseudocobalamin, which is used as a cofactor in their specialized methionine synthase (MetH). This contrasts a model diatom, Thalassiosira pseudonana, which transported pseudocobalamin into the cell but was unable to use pseudocobalamin in its homolog of MetH. Our genomic and culture analyses showed that marine Thaumarchaeota and select heterotrophic bacteria produce cobalamin. This indicates that cobalamin in the surface ocean is a result of de novo synthesis by heterotrophic bacteria or via modification of closely related compounds like cyanobacterially produced pseudocobalamin. Deeper in the water column, our study implicates Thaumarchaeota as major producers of cobalamin based on genomic potential, cobalamin cell quotas, and abundance. Together, these findings establish the distinctive roles played by abundant prokaryotes in cobalamin-based microbial interdependencies that sustain community structure and function in the ocean.


Subject(s)
Vitamin B 12/metabolism , 5-Methyltetrahydrofolate-Homocysteine S-Methyltransferase/metabolism , Archaea/metabolism , Cyanobacteria/metabolism , Diatoms/metabolism , Ecosystem , Heterotrophic Processes/physiology , Oceans and Seas
6.
Proc Natl Acad Sci U S A ; 112(26): 8008-12, 2015 Jun 30.
Article in English | MEDLINE | ID: mdl-26080407

ABSTRACT

Theoretical studies predict that competition for limited resources reduces biodiversity to the point of ecological instability, whereas strong predator/prey interactions enhance the number of coexisting species and limit fluctuations in abundances. In open ocean ecosystems, competition for low availability of essential nutrients results in relatively few abundant microbial species. The remarkable stability in overall cell abundance of the dominant photosynthetic cyanobacterium Prochlorococcus is assumed to reflect a simple food web structure strongly controlled by grazers and/or viruses. This hypothesized link between stability and ecological interactions, however, has been difficult to test with open ocean microbes because sampling methods commonly have poor temporal and spatial resolution. Here we use continuous techniques on two different winter-time cruises to show that Prochlorococcus cell production and mortality rates are tightly synchronized to the day/night cycle across the subtropical Pacific Ocean. In warmer waters, we observed harmonic oscillations in cell production and mortality rates, with a peak in mortality rate consistently occurring ∼6 h after the peak in cell production. Essentially no cell mortality was observed during daylight. Our results are best explained as a synchronized two-component trophic interaction with the per-capita rates of Prochlorococcus consumption driven either directly by the day/night cycle or indirectly by Prochlorococcus cell production. Light-driven synchrony of food web dynamics in which most of the newly produced Prochlorococcus cells are consumed each night likely enforces ecosystem stability across vast expanses of the open ocean.


Subject(s)
Light , Prochlorococcus/growth & development , Water Microbiology , Ecosystem , Food Chain , Pacific Ocean , Temperature
7.
Bioinformatics ; 32(3): 417-23, 2016 Feb 01.
Article in English | MEDLINE | ID: mdl-26476780

ABSTRACT

MOTIVATION: Recent technological innovations in flow cytometry now allow oceanographers to collect high-frequency flow cytometry data from particles in aquatic environments on a scale far surpassing conventional flow cytometers. The SeaFlow cytometer continuously profiles microbial phytoplankton populations across thousands of kilometers of the surface ocean. The data streams produced by instruments such as SeaFlow challenge the traditional sample-by-sample approach in cytometric analysis and highlight the need for scalable clustering algorithms to extract population information from these large-scale, high-frequency flow cytometers. RESULTS: We explore how available algorithms commonly used for medical applications perform at classification of such a large-scale, environmental flow cytometry data. We apply large-scale Gaussian mixture models to massive datasets using Hadoop. This approach outperforms current state-of-the-art cytometry classification algorithms in accuracy and can be coupled with manual or automatic partitioning of data into homogeneous sections for further classification gains. We propose the Gaussian mixture model with partitioning approach for classification of large-scale, high-frequency flow cytometry data. AVAILABILITY AND IMPLEMENTATION: Source code available for download at https://github.com/jhyrkas/seaflow_cluster, implemented in Java for use with Hadoop. CONTACT: hyrkas@cs.washington.edu SUPPLEMENTARY INFORMATION: Supplementary data are available at Bioinformatics online.


Subject(s)
Algorithms , Computational Biology/methods , Flow Cytometry/methods , Models, Theoretical , Software , Cluster Analysis , Environment , Humans , Normal Distribution
8.
Nature ; 457(7228): 467-70, 2009 Jan 22.
Article in English | MEDLINE | ID: mdl-19037243

ABSTRACT

Primary productivity in 30-40% of the world's oceans is limited by availability of the micronutrient iron. Regions with chronically low iron concentrations are sporadically pulsed with new iron inputs by way of dust or lateral advection from continental margins. Addition of iron to surface waters in these areas induces massive phytoplankton blooms dominated primarily by pennate diatoms. Here we provide evidence that the bloom-forming pennate diatoms Pseudo-nitzschia and Fragilariopsis use the iron-concentrating protein, ferritin, to safely store iron. Ferritin has not been reported previously in any member of the Stramenopiles, a diverse eukaryotic lineage that includes unicellular algae, macroalgae and plant parasites. Phylogenetic analyses suggest that ferritin may have arisen in this small subset of diatoms through a lateral gene transfer. The crystal structure and functional assays of recombinant ferritin derived from Pseudo-nitzschia multiseries reveal a maxi-ferritin that exhibits ferroxidase activity and binds iron. The protein is predicted to be targeted to the chloroplast to control the distribution and storage of iron for proper functioning of the photosynthetic machinery. Abundance of Pseudo-nitzschia ferritin transcripts is regulated by iron nutritional status, and is closely tied to the loss and recovery of photosynthetic competence. Enhanced iron storage with ferritin allows the oceanic diatom Pseudo-nitzschia granii to undergo several more cell divisions in the absence of iron than the comparably sized, oceanic centric diatom Thalassiosira oceanica. Ferritin in pennate diatoms probably contributes to their success in chronically low-iron regions that receive intermittent iron inputs, and provides an explanation for the importance of these organisms in regulating oceanic CO(2) over geological timescales.


Subject(s)
Diatoms/metabolism , Eutrophication , Ferritins/chemistry , Ferritins/metabolism , Iron/metabolism , Binding Sites , Ceruloplasmin/metabolism , Crystallography, X-Ray , Diatoms/chemistry , Diatoms/genetics , Diatoms/growth & development , Ferritins/genetics , Gene Transfer, Horizontal , Iron Deficiencies , Marine Biology , Models, Molecular , Molecular Sequence Data , Phylogeny , RNA, Messenger/analysis , RNA, Messenger/genetics , Seawater
9.
Nat Commun ; 15(1): 2105, 2024 Mar 07.
Article in English | MEDLINE | ID: mdl-38453897

ABSTRACT

Photosynthesis fuels primary production at the base of marine food webs. Yet, in many surface ocean ecosystems, diel-driven primary production is tightly coupled to daily loss. This tight coupling raises the question: which top-down drivers predominate in maintaining persistently stable picocyanobacterial populations over longer time scales? Motivated by high-frequency surface water measurements taken in the North Pacific Subtropical Gyre (NPSG), we developed multitrophic models to investigate bottom-up and top-down mechanisms underlying the balanced control of Prochlorococcus populations. We find that incorporating photosynthetic growth with viral- and predator-induced mortality is sufficient to recapitulate daily oscillations of Prochlorococcus abundances with baseline community abundances. In doing so, we infer that grazers in this environment function as the predominant top-down factor despite high standing viral particle densities. The model-data fits also reveal the ecological relevance of light-dependent viral traits and non-canonical factors to cellular loss. Finally, we leverage sensitivity analyses to demonstrate how variation in life history traits across distinct oceanic contexts, including variation in viral adsorption and grazer clearance rates, can transform the quantitative and even qualitative importance of top-down controls in shaping Prochlorococcus population dynamics.


Subject(s)
Ecosystem , Prochlorococcus , Oceans and Seas , Food Chain , Population Dynamics , Seawater/microbiology , Pacific Ocean
10.
Proc Natl Acad Sci U S A ; 107(38): 16571-6, 2010 Sep 21.
Article in English | MEDLINE | ID: mdl-20823224

ABSTRACT

In terrestrial ecosystems, transitional areas between different plant communities (ecotones) are formed by steep environmental gradients and are commonly characterized by high species diversity and primary productivity, which in turn influences the foodweb structure of these regions. Whether comparable zones of elevated diversity and productivity characterize ecotones in the oceans remains poorly understood. Here we describe a previously hidden hotspot of phytoplankton diversity and productivity in a narrow but seasonally persistent transition zone at the intersection of iron-poor, nitrate-rich offshore waters and iron-rich, nitrate-poor coastal waters of the Northeast Pacific Ocean. Novel continuous measurements of phytoplankton cell abundance and composition identified a complex succession of blooms of five distinct size classes of phytoplankton populations within a 100-km-wide transition zone. The blooms appear to be fueled by natural iron enrichment of offshore communities as they are transported toward the coast. The observed succession of phytoplankton populations is likely driven by spatial gradients in iron availability or time since iron enrichment. Regardless of the underlying mechanism, the resulting communities have a strong impact on the regional biogeochemistry as evidenced by the low partial pressure of CO(2) and the nearly complete depletion of nutrients. Enhanced phytoplankton productivity and diversity associated with steep environmental gradients are expected wherever water masses with complementary nutrient compositions mix to create a region more favorable for phytoplankton growth. The ability to detect and track these important but poorly characterized marine ecotones is critical for understanding their impact on productivity and ecosystem structure in the oceans.


Subject(s)
Ecosystem , Phytoplankton/growth & development , Seawater/microbiology , Biomass , British Columbia , Carbon Dioxide/metabolism , Chlorophyll/metabolism , Chlorophyll A , Food Chain , Pacific Ocean , Phytoplankton/metabolism
11.
Ann Appl Stat ; 17(1): 357-377, 2023 Mar.
Article in English | MEDLINE | ID: mdl-37485300

ABSTRACT

The ocean is filled with microscopic microalgae, called phytoplankton, which together are responsible for as much photosynthesis as all plants on land combined. Our ability to predict their response to the warming ocean relies on understanding how the dynamics of phytoplankton populations is influenced by changes in environmental conditions. One powerful technique to study the dynamics of phytoplankton is flow cytometry which measures the optical properties of thousands of individual cells per second. Today, oceanographers are able to collect flow cytometry data in real time onboard a moving ship, providing them with fine-scale resolution of the distribution of phytoplankton across thousands of kilometers. One of the current challenges is to understand how these small- and large-scale variations relate to environmental conditions, such as nutrient availability, temperature, light and ocean currents. In this paper we propose a novel sparse mixture of multivariate regressions model to estimate the time-varying phytoplankton subpopulations while simultaneously identifying the specific environmental covariates that are predictive of the observed changes to these subpopulations. We demonstrate the usefulness and interpretability of the approach using both synthetic data and real observations collected on an oceanographic cruise conducted in the northeast Pacific in the spring of 2017.

12.
Bioinformatics ; 27(5): 732-3, 2011 Mar 01.
Article in English | MEDLINE | ID: mdl-21208987

ABSTRACT

MOTIVATION: Flow cytometry is a widely used technique among biologists to study the abundances of populations of microscopic algae living in aquatic environments. A new generation of high-frequency flow cytometers collects up to several hundred samples per day and can run continuously for several weeks. Automated computational methods are needed to analyze the different phytoplankton populations present in each sample. Software packages in the programming environment R provide powerful tools for conducting such analyses. RESULTS: We introduce flowPhyto, an R package that performs aggregate statistics on virtually unlimited collections of raw flow cytometry files and provides a memory efficient, parallelized solution for analyzing high-throughput flow cytometric data. AVAILABILITY: Freely accessible at http://www.bioconductor.org.


Subject(s)
Electronic Data Processing/methods , Flow Cytometry/methods , Microalgae/growth & development , Software , Computer Graphics , Statistics as Topic
13.
Nat Microbiol ; 7(4): 570-580, 2022 04.
Article in English | MEDLINE | ID: mdl-35365792

ABSTRACT

The photosynthetic picocyanobacteria Prochlorococcus and Synechococcus are models for dissecting how ecological niches are defined by environmental conditions, but how interactions with bacteriophages affect picocyanobacterial biogeography in open ocean biomes has rarely been assessed. We applied single-virus and single-cell infection approaches to quantify cyanophage abundance and infected picocyanobacteria in 87 surface water samples from five transects that traversed approximately 2,200 km in the North Pacific Ocean on three cruises, with a duration of 2-4 weeks, between 2015 and 2017. We detected a 550-km-wide hotspot of cyanophages and virus-infected picocyanobacteria in the transition zone between the North Pacific Subtropical and Subpolar gyres that was present in each transect. Notably, the hotspot occurred at a consistent temperature and displayed distinct cyanophage-lineage composition on all transects. On two of these transects, the levels of infection in the hotspot were estimated to be sufficient to substantially limit the geographical range of Prochlorococcus. Coincident with the detection of high levels of virally infected picocyanobacteria, we measured an increase of 10-100-fold in the Synechococcus populations in samples that are usually dominated by Prochlorococcus. We developed a multiple regression model of cyanophages, temperature and chlorophyll concentrations that inferred that the hotspot extended across the North Pacific Ocean, creating a biological boundary between gyres, with the potential to release organic matter comparable to that of the sevenfold-larger North Pacific Subtropical Gyre. Our results highlight the probable impact of viruses on large-scale phytoplankton biogeography and biogeochemistry in distinct regions of the oceans.


Subject(s)
Prochlorococcus , Synechococcus , Viruses , Pacific Ocean , Seawater/microbiology
14.
ISME J ; 15(1): 41-54, 2021 01.
Article in English | MEDLINE | ID: mdl-32918065

ABSTRACT

Long-term stability of picocyanobacteria in the open oceans is maintained by a balance between synchronous division and death on daily timescales. Viruses are considered a major source of microbial mortality, however, current methods to measure infection have significant methodological limitations. Here we describe a method that pairs flow-cytometric sorting with a PCR-based polony technique to simultaneously screen thousands of taxonomically resolved individual cells for intracellular virus DNA, enabling sensitive, high-throughput, and direct quantification of infection by different virus lineages. Under controlled conditions with picocyanobacteria-cyanophage models, the method detected infection throughout the lytic cycle and discriminated between varying infection levels. In North Pacific subtropical surface waters, the method revealed that only a small percentage of Prochlorococcus (0.35-1.6%) were infected, predominantly by T4-like cyanophages, and that infection oscillated 2-fold in phase with the diel cycle. This corresponds to 0.35-4.8% of Prochlorococcus mortality daily. Cyanophages were 2-4-fold more abundant than Prochlorococcus, indicating that most encounters did not result in infection and suggesting infection is mitigated via host resistance, reduced phage infectivity and inefficient adsorption. This method will enable quantification of infection for key microbial taxa across oceanic regimes and will help determine the extent that viruses shape microbial communities and ecosystem level processes.


Subject(s)
Bacteriophages , Prochlorococcus , Bacteriophages/genetics , DNA Viruses , Ecosystem , Oceans and Seas , Prochlorococcus/genetics , Seawater
15.
mSystems ; 6(3)2021 May 04.
Article in English | MEDLINE | ID: mdl-33947800

ABSTRACT

Phytoplankton transform inorganic carbon into thousands of biomolecules that represent an important pool of fixed carbon, nitrogen, and sulfur in the surface ocean. Metabolite production differs between phytoplankton, and the flux of these molecules through the microbial food web depends on compound-specific bioavailability to members of a wider microbial community. Yet relatively little is known about the diversity or concentration of metabolites within marine plankton. Here, we compare 313 polar metabolites in 21 cultured phytoplankton species and in natural planktonic communities across environmental gradients to show that bulk community metabolomes reflect the chemical composition of the phytoplankton community. We also show that groups of compounds have similar patterns across space and taxonomy, suggesting that the concentrations of these compounds in the environment are controlled by similar sources and sinks. We quantify several compounds in the surface ocean that represent substantial understudied pools of labile carbon. For example, the N-containing metabolite homarine was up to 3% of particulate carbon and is produced in high concentrations by cultured Synechococcus, and S-containing gonyol accumulated up to 2.5 nM in surface particles and likely originates from dinoflagellates or haptophytes. Our results show that phytoplankton composition directly shapes the carbon composition of the surface ocean. Our findings suggest that in order to access these pools of bioavailable carbon, the wider microbial community must be adapted to phytoplankton community composition.IMPORTANCE Microscopic phytoplankton transform 100 million tons of inorganic carbon into thousands of different organic compounds each day. The structure of each chemical is critical to its biological and ecosystem function, yet the diversity of biomolecules produced by marine microbial communities remained mainly unexplored, especially small polar molecules which are often considered the currency of the microbial loop. Here, we explore the abundance and diversity of small biomolecules in planktonic communities across ecological gradients in the North Pacific and within 21 cultured phytoplankton species. Our work demonstrates that phytoplankton diversity is an important determinant of the chemical composition of the highly bioavailable pool of organic carbon in the ocean, and we highlight understudied yet abundant compounds in both the environment and cultured organisms. These findings add to understanding of how the chemical makeup of phytoplankton shapes marine microbial communities where the ability to sense and use biomolecules depends on the chemical structure.

16.
mSystems ; 6(3)2021 May 04.
Article in English | MEDLINE | ID: mdl-33947808

ABSTRACT

Light fuels photosynthesis and organic matter production by primary producers in the sunlit ocean. The quantity and quality of the organic matter produced influence community function, yet in situ measurements of metabolites, the products of cellular metabolism, over the diel cycle are lacking. We evaluated community-level biochemical consequences of oscillations of light in the North Pacific Subtropical Gyre by quantifying 79 metabolites in particulate organic matter from 15 m every 4 h over 8 days. Total particulate metabolite concentration peaked at dusk and represented up to 2% of total particulate organic carbon (POC). The concentrations of 55/79 (70%) individual metabolites exhibited significant 24-h periodicity, with daily fold changes from 1.6 to 12.8, often greater than those of POC and flow cytometry-resolvable biomass, which ranged from 1.2 to 2.8. Paired metatranscriptome analysis revealed the taxa involved in production and consumption of a subset of metabolites. Primary metabolites involved in anabolism and redox maintenance had significant 24-h periodicity and diverse organisms exhibited diel periodicity in transcript abundance associated with these metabolites. Compounds with osmotic properties displayed the largest oscillations in concentration, implying rapid turnover and supporting prior evidence of functions beyond cell turgor maintenance. The large daily oscillation of trehalose paired with metatranscriptome and culture data showed that trehalose is produced by the nitrogen-fixing cyanobacterium Crocosphaera, likely to store energy for nighttime metabolism. Together, paired measurements of particulate metabolites and transcripts resolve strategies that microbes use to manage daily energy and redox oscillations and highlight dynamic metabolites with cryptic roles in marine microbial ecosystems.IMPORTANCE Fueled by light, phytoplankton produce the organic matter that supports ocean ecosystems and carbon sequestration. Ocean change impacts microbial metabolism with repercussions for biogeochemical cycling. As the small molecule products of cellular metabolism, metabolites often change rapidly in response to environmental conditions and form the basis of energy and nutrient management and storage within cells. By pairing measurements of metabolites and gene expression in the stratified surface ocean, we reveal strategies of microbial energy management over the day-night cycle and hypothesize that oscillating metabolites are important substrates for dark respiration by phytoplankton. These high-resolution diel measurements of in situ metabolite concentrations form the basis for future work into the specific roles these compounds play in marine microbial communities.

17.
PLoS Biol ; 4(3): e60, 2006 Mar.
Article in English | MEDLINE | ID: mdl-16475869

ABSTRACT

Diatoms are an important group of eukaryotic phytoplankton, responsible for about 20% of global primary productivity. Study of the functional role of chemical signaling within phytoplankton assemblages is still in its infancy although recent reports in diatoms suggest the existence of chemical-based defense strategies. Here, we demonstrate how the accurate perception of diatom-derived reactive aldehydes can determine cell fate in diatoms. In particular, the aldehyde (2E,4E/Z)-decadienal (DD) can trigger intracellular calcium transients and the generation of nitric oxide (NO) by a calcium-dependent NO synthase-like activity, which results in cell death. However, pretreatment of cells with sublethal doses of aldehyde can induce resistance to subsequent lethal doses, which is reflected in an altered calcium signature and kinetics of NO production. We also present evidence for a DD-derived NO-based intercellular signaling system for the perception of stressed bystander cells. Based on these findings, we propose the existence of a sophisticated stress surveillance system in diatoms, which has important implications for understanding the cellular mechanisms responsible for acclimation versus death during phytoplankton bloom successions.


Subject(s)
Calcium/pharmacology , Diatoms/drug effects , Diatoms/metabolism , Nitric Oxide/metabolism , Aldehydes/pharmacology , Cell Death/drug effects , Diatoms/cytology , Drug Resistance , Oceans and Seas
18.
Sci Data ; 6(1): 277, 2019 11 22.
Article in English | MEDLINE | ID: mdl-31757971

ABSTRACT

SeaFlow is an underway flow cytometer that provides continuous shipboard observations of the abundance and optical properties of small phytoplankton (<5 µm in equivalent spherical diameter, ESD). Here we present data sets consisting of SeaFlow-based cell abundance, forward light scatter, and pigment fluorescence of individual cells, as well as derived estimates of ESD and cellular carbon content of picophytoplankton, which includes the cyanobacteria Prochlorococcus, Synechococcus and small-sized Crocosphaera (<5 µm ESD), and picophytoplankton and nanophytoplankton (2-5 µm ESD). Data were collected in surface waters (≈5 m depth) from 27 oceanographic cruises carried out in the Northeast Pacific Ocean between 2010 and 2018. Thirteen cruises provide high spatial resolution (≈1 km) measurements across 32,500 km of the Northeast Pacific Ocean and 14 near-monthly cruises beginning in 2015 provide seasonal distributions at the long-term sampling site (Station ALOHA) of the Hawaii Ocean Time-Series. These data sets expand our knowledge of the current spatial and temporal distributions of picophytoplankton in the surface ocean.


Subject(s)
Biomass , Phytoplankton/growth & development , Carbon/analysis , Fluorescence , Pacific Ocean , Pigments, Biological , Seawater
19.
Science ; 365(6457): 1040-1044, 2019 09 06.
Article in English | MEDLINE | ID: mdl-31488692

ABSTRACT

From June to August 2018, the eruption of Kilauea volcano on the island of Hawai'i injected millions of cubic meters of molten lava into the nutrient-poor waters of the North Pacific Subtropical Gyre. The lava-impacted seawater was characterized by high concentrations of metals and nutrients that stimulated phytoplankton growth, resulting in an extensive plume of chlorophyll a that was detectable by satellite. Chemical and molecular evidence revealed that this biological response hinged on unexpectedly high concentrations of nitrate, despite the negligible quantities of nitrogen in basaltic lava. We hypothesize that the high nitrate was caused by buoyant plumes of nutrient-rich deep waters created by the substantial input of lava into the ocean. This large-scale ocean fertilization was therefore a unique perturbation event that revealed how marine ecosystems respond to exogenous inputs of nutrients.


Subject(s)
Phytoplankton/growth & development , Seawater/chemistry , Volcanic Eruptions , Chlorophyll A/analysis , Chlorophyll A/metabolism , Eutrophication , Hawaii , Metals/analysis , Nitrates/analysis , Nitrogen/analysis , Pacific Ocean , Phytoplankton/metabolism , Seawater/analysis
20.
Aquat Toxicol ; 86(2): 249-55, 2008 Jan 31.
Article in English | MEDLINE | ID: mdl-18093670

ABSTRACT

Bioactive polyunsaturated aldehydes (PUAs) are produced by several marine phytoplankton (mainly diatoms) and have been shown to have a detrimental effect on a wide variety of organisms, including phytoplankton and invertebrates. However, their potential impact on marine bacteria has been largely neglected. We assess here the effect of three PUAs produced by marine diatoms: 2E,4E-decadienal, 2E,4E-octadienal and 2E,4E-heptadienal, on the growth of 33 marine bacterial strains, including 16 strains isolated during a bloom of the PUA-producing diatom Skeletonema marinoi in the Northern Adriatic Sea. A concentration-dependent growth reduction was observed for 19 bacterial strains at concentrations ranging from 3 to 145 micromolL(-1). Surprisingly, Eudora adriatica strain MOLA358 (Flavobacteriaceae) and Alteromonas hispanica strain MOLA151 (Alteromonadaceae) showed growth stimulation upon exposure to PUAs at concentrations between 13 and 18 micromolL(-1). The remaining 12 strains were unaffected by even very high PUA concentrations. Strains isolated during the diatom bloom showed remarkable resistance to PUA exposures, with only two out of 16 strains showing growth inhibition at PUA concentrations below 106, 130, and 145 micromolL(-1) for 2E,4E-decadienal, 2E,4E-octadienal and 2E,4E-heptadienal, respectively. No correlation between taxonomical position and sensitivity to PUA was observed. Considering that many bacteria thrive in close vicinity of diatom cells, it is likely that these compounds may shape the structure of associated bacterial communities by representing a selection force. This is even more relevant during the final stages of blooms, when senescence and nutrient limitation increase the potential production and release of aldehydes.


Subject(s)
Bacteria/drug effects , Marine Toxins/toxicity , Aldehydes/toxicity , Alkadienes/toxicity , Bacteria/growth & development , Diatoms/physiology , Time Factors , Water Microbiology
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