Kido Soule Melissa C.

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Kido Soule

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Melissa C.

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Fate of dispersants associated with the Deepwater Horizon oil spill

( 2011-01-05) Kujawinski, Elizabeth B. ; Kido Soule, Melissa C. ; Valentine, David L. ; Boysen, Angela K. ; Longnecker, Krista ; Redmond, Molly C.

Response actions to the Deepwater Horizon oil spill included the injection of ~771,000 gallons (2,900,000 L) of chemical dispersant into the flow of oil near the seafloor. Prior to this incident, no deepwater applications of dispersant had been conducted and thus no data exists on the environmental fate of dispersants in deepwater. We used ultrahigh resolution mass spectrometry and liquid chromatography with tandem mass spectrometry (LC/MS/MS) to identify and quantify one key ingredient of the dispersant, the anionic surfactant DOSS (dioctyl sodium sulfosuccinate), in the Gulf of Mexico deepwater during active flow and again after flow had ceased. Here we show that DOSS was sequestered in deepwater hydrocarbon plumes at 1000-1200m water depth and did not intermingle with surface dispersant applications. Further, its concentration distribution was consistent with conservative transport and dilution at depth and it persisted up to 300 km from the well, 64 days after deepwater dispersant applications ceased. We conclude that DOSS was selectively associated with the oil and gas phases in the deepwater plume, yet underwent negligible, or slow, rates of biodegradation in the affected waters. These results provide important constraints on accurate modeling of the deepwater plume and critical geochemical contexts for future toxicological studies.
Dissolved organic matter produced by Thalassiosira pseudonana

( 2014-10) Longnecker, Krista ; Kido Soule, Melissa C. ; Kujawinski, Elizabeth B.

Phytoplankton are significant producers of dissolved organic matter (DOM) in marine ecosystems but the identity and dynamics of this DOM remain poorly constrained. Knowledge on the identity and dynamics of DOM are crucial for understanding the molecular-level reactions at the base of the global carbon cycle. Here we apply emerging analytical and computational tools from metabolomics to investigate the composition of DOM produced by the centric diatom Thalassiosira pseudonana. We assessed both intracellular metabolites within T. pseudonana (the endo-metabolome) and extracellular metabolites released by T. pseudonana (the exo-metabolome). The intracellular metabolites had a more variable composition than the extracellular metabolites. We putatively identified novel compounds not previously associated with T. pseudonana as well as compounds that have previously been identified within T. pseudonana’s metabolic capacity (e.g. dimethylsulfoniopropionate and degradation products of chitin). The resulting information will provide the basis for future experiments to assess the impact of T. pseudonana on the composition of dissolved organic matter in marine environments.
Benthic exometabolites and their ecological significance on threatened Caribbean coral reefs

(Springer, 2022-10-17) Weber, Laura ; Soule, Melissa Kido ; Longnecker, Krista ; Becker, Cynthia C. ; Huntley, Naomi ; Kujawinski, Elizabeth B. ; Apprill, Amy

Benthic organisms are the architectural framework supporting coral reef ecosystems, but their community composition has recently shifted on many reefs. Little is known about the metabolites released from these benthic organisms and how compositional shifts may influence other reef life, including prolific microorganisms. To investigate the metabolite composition of benthic exudates and their ecological significance for reef microbial communities, we harvested exudates from six species of Caribbean benthic organisms including stony corals, octocorals, and an invasive encrusting alga, and subjected these exudates to untargeted and targeted metabolomics approaches using liquid chromatography-mass spectrometry. Incubations with reef seawater microorganisms were conducted to monitor changes in microbial abundances and community composition using 16 S rRNA gene sequencing in relation to exudate source and three specific metabolites. Exudates were enriched in amino acids, nucleosides, vitamins, and indole-based metabolites, showing that benthic organisms contribute labile organic matter to reefs. Furthermore, exudate compositions were species-specific, and riboflavin and pantothenic acid emerged as significant coral-produced metabolites, while caffeine emerged as a significant invasive algal-produced metabolite. Microbial abundances and individual microbial taxa responded differently to exudates from stony corals and octocorals, demonstrating that exudate mixtures released from different coral species select for specific bacteria. In contrast, microbial communities did not respond to individual additions of riboflavin, pantothenic acid, or caffeine. This work indicates that recent shifts in benthic organisms alter exudate composition and likely impact microbial communities on coral reefs.
Extracellular reef metabolites across the protected Jardines de la Reina, Cuba Reef System

(Frontiers Media, 2020-12-14) Weber, Laura ; Armenteros, Maickel ; Kido Soule, Melissa C. ; Longnecker, Krista ; Kujawinski, Elizabeth B. ; Apprill, Amy

Coral reef ecosystems are incredibly diverse marine biomes that rely on nutrient cycling by microorganisms to sustain high productivity in generally oligotrophic regions of the ocean. Understanding the composition of extracellular reef metabolites in seawater, the small organic molecules that serve as the currency for microorganisms, may provide insight into benthic-pelagic coupling as well as the complexity of nutrient cycling in coral reef ecosystems. Jardines de la Reina (JR), Cuba is an ideal environment to examine extracellular metabolites across protected and high-quality reefs. Here, we used liquid chromatography mass spectrometry (LC-MS) to quantify specific known metabolites of interest (targeted metabolomics approach) and to survey trends in metabolite feature composition (untargeted metabolomics approach) from surface and reef depth (6 – 14 m) seawater overlying nine forereef sites in JR. We found that untargeted metabolite feature composition was surprisingly similar between reef depth and surface seawater, corresponding with other biogeochemical and physicochemical measurements and suggesting that environmental conditions were largely homogenous across forereefs within JR. Additionally, we quantified 32 of 53 detected metabolites using the targeted approach, including amino acids, nucleosides, vitamins, and other metabolic intermediates. Two of the quantified metabolites, riboflavin and xanthosine, displayed interesting trends by depth. Riboflavin concentrations were higher in reef depth compared to surface seawater, suggesting that riboflavin may be produced by reef organisms at depth and degraded in the surface through photochemical oxidation. Xanthosine concentrations were significantly higher in surface reef seawater. 5′-methylthioadenosine (MTA) concentrations increased significantly within the central region of the archipelago, displaying biogeographic patterns that warrant further investigation. Here we lay the groundwork for future investigations of variations in metabolite composition across reefs, sources and sinks of reef metabolites, and changes in metabolites over environmental, temporal, and reef health gradients.
Release of ecologically relevant metabolites by the cyanobacterium Synechococcus elongatus CCMP 1631

( 2015-04-30) Fiore, Cara L. ; Longnecker, Krista ; Kido Soule, Melissa C. ; Kujawinski, Elizabeth B.

Photoautotrophic plankton in the surface ocean release organic compounds that fuel secondary production by heterotrophic bacteria. Here we show that an abundant marine cyanobacterium, Synechococcus elongatus, contributes a variety of nitrogen-rich and sulfur-containing compounds to dissolved organic matter. A combination of targeted and untargeted metabolomics and genomic tools was used to characterize the intracellular and extracellular metabolites of S. elongatus. Aromatic compounds such as 4-hydroxybenzoic acid and phenylalanine, as well as nucleosides (e.g., thymidine, 5’-methylthioadenosine, xanthosine), the organosulfur compound 3-mercaptopropionate, and the plant auxin indole 3-acetic acid, were released by S. elongatus at multiple time points during its growth. Further, the amino acid kynurenine was found to accumulate in the media even though it was not present in the predicted metabolome of S. elongatus. This indicates that some metabolites, including those not predicted by an organism’s genome, are likely excreted into the environment as waste; however, these molecules may have broader ecological relevance if they are labile to nearby microbes. The compounds described herein provide excellent targets for quantitative analysis in field settings to assess the source and lability of dissolved organic matter in situ.
Extraction efficiency and quantification of dissolved metabolites in targeted marine metabolomics

(John Wiley & Sons, 2017-03-20) Johnson, Winifred M. ; Kido Soule, Melissa C. ; Kujawinski, Elizabeth B.

The field of metabolomics seeks to characterize the suite of small molecules that comprise the end-products of cellular regulation. Metabolomics has been used in biomedical applications as well as environmental studies that explore ecological and biogeochemical questions. We have developed a targeted metabolomics method using electrospray ionization–liquid chromatography tandem mass spectrometry to analyze metabolites dissolved in seawater. Preparation of samples from the marine environment presents challenges because dilute metabolites must be concentrated and desalted. We present the extraction efficiencies of 89 metabolites in our targeted method using solid phase extraction (SPE). In addition, we calculate the limits of detection and quantification for the metabolites in the method and compare the instrument response factors in five different matrices ranging from deionized water to spent medium from cultured marine microbes. High background organic matter content reduces the instrument response factor for only a small group of metabolites, yet enhances the extraction efficiency for other metabolites on the SPE cartridge used here, a modified styrene-divinylbenzene polymer called PPL. Aromatic or larger uncharged compounds, in particular, are reproducibly well retained on the PPL polymer. This method is suitable for the detection of dissolved metabolites in marine samples, with limits of detection ranging from < 1 pM to ∼ 2 nM dependent on the dual impacts of seawater matrix on extraction efficiency and on instrument response factors.
Environmental metabolomics : databases and tools for data analysis

(Elsevier, 2015-06-19) Longnecker, Krista ; Futrelle, Joe ; Coburn, Elizabeth ; Kido Soule, Melissa C. ; Kujawinski, Elizabeth B.

Metabolomics is the study of small molecules, or ‘metabolites’, that are the end products of biological processes. While -omics technologies such as genomics, transcriptomics, and proteomics measure the metabolic potential of organisms, metabolomics provides detailed information on the organic compounds produced during metabolism and found within cells and in the environment. Improvements in analytical techniques have expanded our understanding of metabolomics and developments in computational tools have made metabolomics data accessible to a broad segment of the scientific community. Yet, metabolomics methods have only been applied to a limited number of projects in the marine environment. Here, we review analysis techniques for mass spectrometry data and summarize the current state of metabolomics databases. We then describe a boutique database developed in our laboratory for efficient data analysis and selection of mass spectral targets for metabolite identification. The code to implement the database is freely available on GitHub (https://github.com/joefutrelle/domdb). Data organization and analysis are critical, but often under-appreciated, components of metabolomics research. Future advances in environmental metabolomics will take advantage of continued development of new tools that facilitate analysis of large metabolomics datasets.
Hepatic metabolite profiling of polychlorinated biphenyl (PCB)-resistant and sensitive populations of Atlantic killifish (Fundulus heteroclitus)

( 2018-10-15) Glazer, Lilah ; Kido Soule, Melissa C. ; Longnecker, Krista ; Kujawinski, Elizabeth B. ; Aluru, Neelakanteswar

Atlantic killifish inhabiting polluted sites along the east coast of the U.S. have evolved resistance to toxic effects of contaminants. One such contaminated site is the Acushnet River estuary, near New Bedford Harbor (NBH), Massachusetts, which is characterized by very high PCB concentrations in the sediments and in the tissues of resident killifish. Though killifish at this site appear to be thriving, the metabolic costs of survival in a highly contaminated environment are not well understood. In this study we compared the hepatic metabolite profiles of resistant (NBH) and sensitive populations (Scorton Creek (SC), Sandwich, MA) using a targeted metabolomics approach in which polar metabolites were extracted from adult fish livers and quantified. Our results revealed differences in the levels of several metabolites between fish from the two sites. The majority of these metabolites are associated with one-carbon metabolism, an important pathway that supports multiple physiological processes including DNA and protein methylation, nucleic acid biosynthesis and amino acid metabolism. We measured the gene expression of DNA methylation (DNA methyltransferase 1, dnmt1) and demethylation genes (Ten-Eleven Translocation (TET) genes) in the two populations, and observed lower levels of dnmt1 and higher levels of TET gene expression in the NBH livers, suggesting possible differences in DNA methylation profiles. Consistent with this, the two populations differed significantly in the levels of 5-methylcytosine and 5-hydroxymethylcytosine nucleotides. Overall, our results suggest that the unique hepatic metabolite signatures observed in NBH and SC reflect the adaptive mechanisms for survival in their respective habitats.
Organic sulfur: a spatially variable and understudied component of marine organic matter

(Wiley Open Access, 2020-02-05) Longnecker, Krista ; Oswald, Lisa ; Kido Soule, Melissa C. ; Cutter, Gregory A. ; Kujawinski, Elizabeth B.

Sulfur (S) is a major heteroatom in organic matter. This project evaluated spatial variability in the concentration and molecular‐level composition of organic sulfur along gradients of depth and latitude. We measured the concentration of total organic sulfur (TOS) directly from whole seawater. Our data reveal high variability in organic sulfur, relative to established variability in total organic carbon or nitrogen. The deep ocean contained significant amounts of organic sulfur, and the concentration of TOS in North Atlantic Deep Water (NADW) decreased with increasing age while total organic carbon remained stable. Analysis of dissolved organic matter extracts by ultrahigh resolution mass spectrometry revealed that 6% of elemental formulas contained sulfur. The sulfur‐containing compounds were structurally diverse, and showed higher numbers of sulfur‐containing elemental formulas as NADW moved southward. These measurements of organic sulfur in seawater provide the foundation needed to define the factors controlling organic sulfur in the global ocean.
A phosphate starvation response gene (psr1-like) is present and expressed in Micromonas pusilla and other marine algae

(Inter Research, 2021-02-25) Fiore, Cara L. ; Alexander, Harriet ; Kido Soule, Melissa C. ; Kujawinski, Elizabeth B.

Phosphorus (P) limits primary production in regions of the surface ocean, and many plankton species exhibit specific physiological responses to P deficiency. The metabolic response of Micromonas pusilla, an ecologically relevant marine photoautotroph, to P deficiency was investigated using metabolomics and comparative genomics. The concentrations of some intracellular metabolites were elevated in the P-deficient cells (e.g. xanthine, inosine), and genes involved in the associated metabolic pathways shared a predicted conserved amino acid motif in the non-coding regions of each gene. The presence of the conserved motif suggests that these genes may be co-regulated, and the motif may constitute a regulatory element for binding a transcription factor, specifically that of Psr1 (phosphate starvation response). A putative phosphate starvation response gene ( psr1-like) was identified in M. pusilla with homology to well characterized psr1/ phr1 genes in algae and plants, respectively. This gene appears to be present and expressed in other marine algal taxa (e.g. Emiliania huxleyi) in field sites that are chronically P limited. Results from the present study have implications for understanding phytoplankton taxon-specific roles in mediating P cycling in the ocean.
Evidence for quorum sensing and differential metabolite production by a marine bacterium in response to DMSP

(Nature Publishing Group, 2016-02-16) Johnson, Winifred M. ; Kido Soule, Melissa C. ; Kujawinski, Elizabeth B.

Microbes, the foundation of the marine foodweb, do not function in isolation, but rather rely on molecular level interactions among species to thrive. Although certain types of interactions between autotrophic and heterotrophic microorganisms have been well documented, the role of specific organic molecules in regulating inter-species relationships and supporting growth are only beginning to be understood. Here, we examine one such interaction by characterizing the metabolic response of a heterotrophic marine bacterium, Ruegeria pomeroyi DSS-3, to growth on dimethylsulfoniopropionate (DMSP), an abundant organosulfur metabolite produced by phytoplankton. When cultivated on DMSP, R. pomeroyi synthesized a quorum-sensing molecule, N-(3-oxotetradecanoyl)-l-homoserine lactone, at significantly higher levels than during growth on propionate. Concomitant with the production of a quorum-sensing molecule, we observed differential production of intra- and extracellular metabolites including glutamine, vitamin B2 and biosynthetic intermediates of cyclic amino acids. Our metabolomics data indicate that R. pomeroyi changes regulation of its biochemical pathways in a manner that is adaptive for a cooperative lifestyle in the presence of DMSP, in anticipation of phytoplankton-derived nutrients and higher microbial density. This behavior is likely to occur on sinking marine particles, indicating that this response may impact the fate of organic matter.
Targeted metabolomics reveals proline as a major osmolyte in the chemolithoautotroph Sulfurimonas denitrificans

(John Wiley & Sons, 2018-02-09) Götz, Florian ; Longnecker, Krista ; Kido Soule, Melissa C. ; Becker, Kevin W. ; McNichol, Jesse C. ; Kujawinski, Elizabeth B. ; Sievert, Stefan M.

Chemoautotrophic bacteria belonging to the genus Sulfurimonas in the class Campylobacteria are widespread in many marine environments characterized by redox interfaces, yet little is known about their physiological adaptations to different environmental conditions. Here, we used liquid chromatography coupled with tandem mass spectrometry (LC-MS/ MS) in a targeted metabolomics approach to study the adaptations of Sulfurimonas denitrificans to varying salt concentrations that are found in its natural habitat of tidal mudflats. Proline was identified as one of the most abundant internal metabolites and its concentration showed a strong positive correlation with ionic strength, suggesting that it acts as an important osmolyte in S. denitrificans. 2,3-dihydroxypropane- 1- sulfonate was also positively correlated with ionic strength, indicating it might play a previously unrecognized role in osmoregulation. Furthermore, the detection of metabolites from the reductive tricarboxylic acid cycle at high internal concentrations reinforces the importance of this pathway for carbon fixation in Campylobacteria and as a hub for biosynthesis. As the first report of metabolomic data for an campylobacterial chemolithoautotroph, this study provides data that will be useful to understand the adaptations of Campylobacteria to their natural habitat at redox interfaces.
Impact of instrument and experiment parameters on reproducibility of ultrahigh resolution ESI FT-ICR mass spectra of natural organic matter

( 2010-04-09) Kido Soule, Melissa C. ; Longnecker, Krista ; Giovannoni, Stephen J. ; Kujawinski, Elizabeth B.

Natural dissolved organic matter (OM) is a complex heterogeneous mixture of compounds that have defied traditional characterization using standard analytical methods. Electrospray ionization mass spectrometry, particularly ultrahigh resolution mass spectrometry, has provided a new platform for compositional assessment of this important pool of the Earth’s reduced carbon. Here, we propose a framework for optimization of instrument and experiment parameters for high quality data acquisition using Fourier‐transform ion cyclotron resonance mass spectrometry (FT‐ICR‐MS). We report the impact of these parameters on reproducibility of peak detection and repeatability of peak height in replicate injections of Suwannee River fulvic acid (FA), a common terrestrial OM standard. In addition, we examine the variability in peak detection and peak height among different types of experimental replicates of dissolved OM derived from laboratory cultures of Candidatus Pelagibacter ubique, a ubiquitous marine α‐ proteobacterium.
Quantification of amine- and alcohol-containing metabolites in saline samples using pre-extraction benzoyl chloride derivatization and ultrahigh performance liquid chromatography tandem mass spectrometry (UHPLC MS/MS)

(American Chemical Society, 2021-03-10) Widner, Brittany ; Kido Soule, Melissa C. ; Ferrer-González, Frank Xavier ; Moran, Mary Ann ; Kujawinski, Elizabeth B.

Dissolved metabolites serve as nutrition, energy, and chemical signals for microbial systems. However, the full scope and magnitude of these processes in marine systems are unknown, largely due to insufficient methods, including poor extraction of small, polar compounds using common solid-phase extraction resins. Here, we utilized pre-extraction derivatization and ultrahigh performance liquid chromatography electrospray ionization tandem mass spectrometry (UHPLC-ESI-MS/MS) to detect and quantify targeted dissolved metabolites in seawater and saline culture media. Metabolites were derivatized with benzoyl chloride by their primary and secondary amine and alcohol functionalities and quantified using stable isotope-labeled internal standards (SIL-ISs) produced from 13C6-labeled benzoyl chloride. We optimized derivatization, extraction, and sample preparation for field and culture samples and evaluated matrix-derived biases. We have optimized this quantitative method for 73 common metabolites, of which 50 cannot be quantified without derivatization due to low extraction efficiencies. Of the 73 metabolites, 66 were identified in either culture media or seawater and 45 of those were quantified. This derivatization method is sensitive (detection limits = pM to nM), rapid (∼5 min per sample), and high throughput.
Metabolite composition of sinking particles differs from surface suspended particles across a latitudinal transect in the South Atlantic

(Wiley, 2019-07-31) Johnson, Winifred M. ; Longnecker, Krista ; Kido Soule, Melissa C. ; Arnold, William A. ; Bhatia, Maya P. ; Hallam, Steven J. ; Van Mooy, Benjamin A. S. ; Kujawinski, Elizabeth B.

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.
Biogeochemistry, metabolomics, and metagenomics of Florida's Coral Reef from sampling conducted over 15 days in June 2019

(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2023-03-08) Apprill, Amy ; Kujawinski, Elizabeth ; Muller, Erinn ; Sandin, Stuart ; Weber, Laura ; Clark, Abigail ; Kido Soule, Melissa C. ; Longnecker, Krista ; Zgliczynski, Brian ; Sullivan, Chris ; Becker, Cynthia Carroll

This comparative 'omics dataset was collected over 15 days in June 2019 along Florida's Coral Reef. We assessed 85 reefs for the prevalence of stony coral tissue loss disease (SCTLD), nutrients (total organic carbon (TOC), total organic nitrogen (TON), inorganic nutrients), and abundances of microbial functional groups (Prochlorococcus, Synechococcus, picoeukaryotes, and heterotrophic microbes (unpigmented bacteria and archaea)), from reef depth waters. At 45 of the reefs, high-resolution photomosaics were used to examine the composition of benthic organisms. At 13 geographically dispersed reefs, we collected seawater (1.7 liters in biological triplicates) for both targeted and untargeted metabolomics analyses. Seawater (2 liters in duplicate) was collected at 26 sites, including the 13 examined for metabolomics, for taxonomic (bacteria and archaea 16S ribosomal RNA gene) and functional (shotgun metagenome) microbiome analyses, and chlorophyll. Given the stony coral tissue loss disease outbreak, we also targeted healthy and diseased coral tissue and near-coral seawater for taxonomic microbiome (16S rRNA gene) analysis (11 sites). Significance: Microorganisms and the dissolved metabolites they process are central to the functioning of ocean ecosystems. These 'invisible' ocean components are poorly understood in biodiverse and productive coral reef ecosystems, where they contribute to nutrient cycling and signaling cues between reef organisms. Microbes and dissolved metabolites offer a new means to examine reef features and have applications for conservation, monitoring, and restoration efforts in these changing ecosystems. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/890979
Particulate and dissolved metabolite distributions along a latitudinal transect of the western Atlantic Ocean

(Association for the Sciences of Limnology and Oceanography, 2022-12-23) Johnson, Winifred M. ; Kido Soule, Melissa C. ; Longnecker, Krista ; Bhatia, Maya P. ; Hallam, Steven J. ; Lomas, Michael W. ; Kujawinski, Elizabeth B.

Metabolites, or the small organic molecules that are synthesized by cells during metabolism, comprise a complex and dynamic pool of carbon in the ocean. They are an essential currency in interactions at the population and community levels of biological organization. Characterizing metabolite distributions inside microbial cells and dissolved in seawater is essential to understanding the controls on their production and fate, as well as their roles in shaping marine microbial food webs. Here, we apply a targeted metabolomics method to quantify particulate and dissolved distributions of a suite of biologically relevant metabolites including vitamins, amino acids, nucleic acids, osmolytes, and intermediates in biosynthetic pathways along a latitudinal transect in the western Atlantic Ocean. We find that, in the upper 200 m of the water column, most particulate or intracellular metabolites positively covary with the most abundant microbial taxa. In contrast, dissolved metabolites exhibited greater variability with differences in distribution between ocean regions. Although fewer particulate metabolites were detected below 200 m, the particulate metabolites identified in the deep ocean may be linked to adaptive physiological strategies of deep‐sea microbes. Based on the identified metabolite distributions, we propose relationships between certain metabolites and microbial populations, and find that dissolved metabolite distributions are not directly related to their particulate abundances.
Metabolite diversity among representatives of divergent Prochlorococcus ecotypes

(American Society for Microbiology, 2023-10-10) Kujawinski, Elizabeth B. ; Braakman, Rogier ; Longnecker, Krista ; Becker, Jamie W. ; Chisholm, Sallie W. ; Dooley, Keven ; Kido Soule, Melissa C. ; Swarr, Gretchen J. ; Halloran, Kathryn H.

The euphotic zone of the surface ocean contains distinct physical-chemical regimes that vary in light and nutrient concentrations as an inverse function of depth. The most numerous phytoplankter of the mid- and low-latitude ocean is the picocyanobacterium Prochlorococcus, which consists of ecologically distinct subpopulations (i.e., “ecotypes”). Ecotypes have different temperature, light, and nutrient optima and display distinct relative abundances along gradients of these niche dimensions. As a primary producer, Prochlorococcus fixes and releases organic carbon to neighboring microbes as part of the microbial loop. However, little is known about the specific molecules Prochlorococcus accumulates and releases or how these processes vary among its ecotypes. Here, we characterize the metabolite diversity of Prochlorococcus by profiling three ecologically distinct cultured strains: MIT9301, representing a high-light-adapted ecotype dominating shallow tropical and sub-tropical waters; MIT0801, representing a low-light-adapted ecotype found throughout the euphotic zone; and MIT9313, representing a low-light-adapted ecotype relatively most abundant at the base of the euphotic zone. In both intracellular and extracellular metabolite profiles, we observe striking differences across strains in the accumulation and release of molecules, such as the DNA methylating agent S-adenosyl-methionine (intracellular) and the branched-chain amino acids (intracellular) and their precursors (extracellular). While some differences reflect variable genome content across the strains, others likely reflect variable regulation of conserved pathways. In the extracellular profiles, we identify molecules such as pantothenic acid and aromatic amino acids that may serve as currencies in Prochlorococcus’ interactions with neighboring microbes and, therefore, merit further investigation.
Microorganisms and dissolved metabolites distinguish Florida’s Coral Reef habitats

(National Academy of Sciences, 2023-09-05) Becker, Cynthia C. ; Weber, Laura ; Zgliczynski, Brian J. ; Sullivan, Chris ; Sandin, Stuart A. ; Muller, Erinn ; Clark, Abigail S. ; Kido Soule, Melissa C. ; Longnecker, Krista ; Kujawinski, Elizabeth ; Apprill, Amy

As coral reef ecosystems experience unprecedented change, effective monitoring of reef features supports management, conservation, and intervention efforts. Omic techniques show promise in quantifying key components of reef ecosystems including dissolved metabolites and microorganisms that may serve as invisible sensors for reef ecosystem dynamics. Dissolved metabolites are released by reef organisms and transferred among microorganisms, acting as chemical currencies and contributing to nutrient cycling and signaling on reefs. Here, we applied four omic techniques (taxonomic microbiome via amplicon sequencing, functional microbiome via shotgun metagenomics, targeted metabolomics, and untargeted metabolomics) to waters overlying Florida's Coral Reef, as well as microbiome profiling on individual coral colonies from these reefs to understand how microbes and dissolved metabolites reflect biogeographical, benthic, and nutrient properties of this 500-km barrier reef. We show that the microbial and metabolite omic approaches each differentiated reef habitats based on geographic zone. Further, seawater microbiome profiling and targeted metabolomics were significantly related to more reef habitat characteristics, such as amount of hard and soft coral, compared to metagenomic sequencing and untargeted metabolomics. Across five coral species, microbiomes were also significantly related to reef zone, followed by species and disease status, suggesting that the geographic water circulation patterns in Florida also impact the microbiomes of reef builders. A combination of differential abundance and indicator species analyses revealed metabolite and microbial signatures of specific reef zones, which demonstrates the utility of these techniques to provide new insights into reef microbial and metabolite features that reflect broader ecosystem processes.
Seasonal and daily patterns in known dissolved metabolites in the northwestern Sargasso Sea

(Association for the Sciences of Limnology and Oceanography, 2024-01-10) Longnecker, Krista ; Kido Soule, Melissa C. ; Swarr, Gretchen J. ; Parsons, Rachel J. ; Liu, Shuting ; Johnson, Winifred M. ; Widner, Brittany ; Curry, Ruth G. ; Carlson, Craig A. ; Kujawinski, Elizabeth B.

Organic carbon in seawater plays a significant role in the global carbon cycle. The concentration and composition of dissolved organic carbon reflect the activity of the biological community and chemical reactions that occur in seawater. From 2016 to 2019, we repeatedly sampled the oligotrophic northwest Sargasso Sea in the vicinity of the Bermuda Atlantic Time-series Study site (BATS) to quantitatively follow known compounds within the pool of dissolved organic matter in the upper 1000 m of the water column. Most metabolites showed surface enrichment, and 83% of the metabolites had significantly lower concentrations with increasing depth. Dissolved metabolite concentrations most notably revealed temporal variability. Fourteen metabolites displayed seasonality that was repeated in each of the 4 yr sampled. Concentrations of vitamins, including pantothenic acid (vitamin B5) and riboflavin (vitamin B2), increased annually during winter periods when mixed layer depths were deepest. During diel sampling, light-sensitive riboflavin decreased significantly during daylight hours. The temporal variability in metabolites at BATS was less than the spatial variability in metabolites from a previous sample set collected over a broad latitudinal range in the western Atlantic Ocean. The metabolites examined in this study are all components of central carbon metabolism. By examining these metabolites at finer resolution and in a time-series, we begin to provide insights into the chemical compounds that may be exchanged by microorganisms in marine systems, data which are fundamental to understanding the chemical response of marine systems to future changes in climate.

Kido Soule Melissa C.

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