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Swarr, G. J.

Publications and source records attributed to Swarr, G. J..

7 recordsLinked to original sources

Habitat and Hydrodynamics Influence Coral Reef and Seagrass Microbial and Exometabolite Dynamics

Coral reef and seagrass ecosystems provide critical storm protection and economic revenue to tropical coastal communities. Effective monitoring and restoration strategies are essential given increasing impacts from climate change and human development. Microorganisms, and the metabolites they produce and consume, are key drivers of coastal ecosystem function. However, microbially-mediated metabolite recycling remains poorly understood, limiting its inclusion in conservation and restoration strategies. Here we examine how seawater exometabolites and microorganisms in coastal ecosystems vary in relation to habitat (seagrass or coral reef), temporal scales and hydrodynamics. We characterized benthic seawater from two St. John, U.S. Virgin Islands coral reefs (Yawzi and Tektite) and one seagrass meadow at dawn and mid-day over four consecutive days. Using quantitative metabolomics and SSU rRNA gene amplicon sequencing, we found that habitat served as the primary driver of exometabolite and microbial community composition, while daily changes and hydrodynamics strongly influenced system variability. Hydrodynamic modeling indicated offshore water intrusion at mid-day at Yawzi reef, likely driving exometabolite and microbial shifts towards oligotrophic taxa (e.g., SAR11, SAR86). In contrast, a high percentage of coastal source water in the seagrass habitat maintained stable exometabolite pools and supported diverse microbial communities. These findings demonstrate that coastal habitat and hydrodynamics strongly influence exometabolite and microbial assemblages, with lesser contributions from temporal changes. Integrating exometabolites, microorganisms, and hydrodynamics provides new insights into coastal ecosystem functioning useful for habitat monitoring and restoration strategies.

ecology↗

Characterization of Phytoplankton-Excreted Metabolites Mediating Carbon Flux through the Surface Ocean

The marine labile dissolved organic carbon (DOC) pool is a dynamic reservoir of thousands of molecules that cycles approximately one-quarter of Earths primary production within days to weeks. After excretion by phytoplankton and other microbes, metabolites are rapidly consumed, resulting in low standing concentrations (picomolar to low nanomolar). Despite the decades-long search for labile DOC sources and molecular identities, marine phytoplankton exometabolomes are not well characterized, largely due to difficulties in measuring small polar molecules in saline water. Here, we profiled the exometabolomes of six axenic phytoplankton species representing key functional groups including a diatom (Thalassiosira pseudonana CCMP1335), a picoeukaryote (Micromonas commoda RCC299), a coccolithophore (Gephyrocapsa huxleyi CCMP371), a diazotrophic cyanobacterium (Crocosphaera watsonii WH8501), and two picocyanobacteria (Prochlorococcus marinus MIT 9301 and Synechococcus WH8102). From these cultures, we quantified 56 amine- and alcohol-containing exometabolites representing 11 compound classes which in sum comprised up to 23.4% of phytoplankton-excreted DOC. We estimated that these phytoplankton-derived exometabolites could supply up to 5% of the daily carbon quota of the dominant heterotrophic bacterium SAR11 in the surface ocean. Substantial variations in exometabolite identity and concentration across phytoplankton taxa underscore taxonomic diversity as a key driver in the supply and composition of labile DOC. This taxonomic variation predicts geographic and seasonal differences in the distribution of marine dissolved metabolites that underpin the cycling of labile DOC back to CO2. Overall, our work suggests that phytoplankton exometabolites are key chemical currencies that mediate significant carbon fluxes within the oceans carbon cycle. Significance StatementPhytoplankton exometabolites are key components of the marine labile dissolved organic carbon (DOC) pool, which drives major a fraction of the oceanic carbon flux. Yet, their composition and flux are poorly constrained. Leveraging new methods, we quantified amine- and alcohol-containing exometabolites in diverse phytoplankton and found they varied taxonomically. These exometabolites accounted for up to 23.4% of excreted DOC, potentially supporting a sizable fraction of the global heterotrophic growth. Integrating our results with ecological models suggest that exometabolite composition varies geographically and seasonally in response to changing phytoplankton community structures. Our findings illuminate the long-standing "black box" of labile DOC and link taxonomic diversity to the chemical currencies underpinning the microbe-metabolite networks at the heart of the marine carbon cycle.

ecology↗

Seasonal exometabolites are regulated by essential microbial metabolisms in the oligotrophic ocean

Predictions of how the biogeochemical reservoir of marine dissolved organic matter (DOM) will respond to future ocean changes require an improved understanding of the thousands of individual microbe-molecule interactions which regulate the transformation and fate of DOM. Bulk characterizations of organic matter can mask this complex network of interactions comprised of rich chemical and taxonomic diversity. Here, we present a three-year, depth-resolved time-series of the seasonal dynamics of the exometabolome and the bacterioplankton community at the Bermuda Atlantic Time-series Study (BATS) site. We find both time-series to be highly structured and compositionally distinct across sampling depths. Putative exometabolite identifications (gonyol, glucose 6-sulfate, succinate, and trehalose) indicate that at least a portion of the exometabolome contains rapidly remineralized, labile molecules. We hypothesize that apparent seasonal accumulation of these labile molecules could result from environmental conditions that alter community composition on a seasonal timescale and thus shift the relative proportions of microbial functions that produce and consume the substrates. Critically, we found the composition of seasonal DOM features was more stable interannually than the microbial community structure. By estimating redundancy of metabolic functions responsible for cycling these molecules in BATS metagenomes, we propose a paradigm whereby core microbial metabolisms, either those utilized by all or by a subset of marine microbes, are better predictors of DOM composition than microbial taxonomies. The molecular-level characterization of DOM achieved herein highlights the metabolic imprint of microbial activity in DOM composition and greatly enhances our understanding of the dynamics regulating Earths largest reservoir of organic carbon. Significance statementMarine dissolved organic matter (DOM) is a major carbon reservoir that acts as a critical control on Earths climate. DOM dynamics are largely regulated by a complex web of microbial interactions, but the mechanisms underpinning these processes are not well understood. In a three-year time-series, we found thousands of DOM molecules and microbial taxa exhibited seasonal patterns. Critically, the identity of the microbes was more variable between years than the composition of the DOM molecules. We suggest that shared metabolisms encoded by genes that conduct core microbial functions are responsible for the more stable composition of DOM. This work links DOM molecules with microbial biodiversity, and presents testable predictors of DOM composition in our changing oceans.

microbiology↗

Advancing Reef Monitoring Techniques through Exometabolomics: Quantification of Labile Dissolved Organic Metabolites on Coral Reefs

Extracellular chemical cues constitute much of the language of life among marine organisms from microbes to mammals. These chemical cues shape foraging and feeding strategies, symbiotic interactions, selection of mates and habitats, and the transfer of energy and nutrients within and among ecosystems. Changes in the chemical pool flux within these ecosystems serve as invisible signals of overall ecosystem health and, conversely, disruption to this finely tuned equilibrium. In coral reef systems, the full scope and magnitude of the chemicals involved in maintaining reef equilibria are largely unknown. In particular, processes involving small, polar molecules, which form the majority components of labile dissolved organic carbon (DOC), are often poorly captured using traditional techniques and therefore remain unconstrained. In this study, we employed a recently developed chemical derivatization method and mass spectrometry-based targeted exometabolomics to capture and quantify polar dissolved phase metabolites on five coral reefs in the U.S. Virgin Islands. We detected and quantified 45 polar exometabolites, and further demonstrate their variability across the investigated geographic landscape and contextualize these findings in terms of geographic and benthic cover differences. By comparing our results to previously published coral reef exometabolomes that did not employ chemical derivatization, we show the novel quantification of 23 metabolites which were previously undetected in the coral reef exometabolome, including compounds involved in central carbon metabolism (e.g., glutamate) and novel metabolites such as homoserine betaine. We highlight the immense potential of chemical derivatization-based exometabolomics for quantifying labile chemical cues on coral reefs and measuring molecular level responses to environmental stressors. Overall, improving our understanding of the composition and dynamics of reef exometabolites is vital for effective ecosystem monitoring and management strategies. SynopsisMinimal research exists on the polar exometabolites on coral reefs, an essential component of reef health and the majority component of labile DOC. This study reports 23 newly quantified polar metabolites on coral reefs and highlights significant differences in the exometabolome composition across geographically distinct reefs and bays.

systems biology↗

Seasonal and daily patterns in known dissolved metabolites in the northwestern Sargasso Sea

Organic carbon in seawater plays a significant role in the global carbon cycle. The concentration and composition of dissolved organic carbon, operationally defined in this project as organic carbon that passes through a 0.2 {micro}m filter, 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 meters of the water column. Dissolved metabolite concentrations revealed patterns with depth and time with most metabolites showing surface enrichment and lower concentrations with increasing depth. Select metabolites displayed seasonal patterns throughout the year, and this seasonality was repeated in each of the years 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. Metabolite concentrations over time at BATS showed less variability compared to 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 relatively long time series, we have insights into microbial biogeochemical activity, data which are fundamental to understanding the chemical response of marine systems to future changes in climate.

biochemistry↗

Metabolite diversity among Prochlorococcus strains belonging to divergent ecotypes

Primary AbstractThe euphotic zone of the surface ocean contains distinct physical-chemical regimes that vary inversely in light and nutrient concentrations as a 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 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. Some differences reflect variable genome content across the strains, while others likely reflect variable regulation of genetically-conserved pathways. In the extracellular profiles, we identify molecules that may serve as currencies in Prochlorococcus interactions with neighboring microbes and therefore merit further investigation. ImportanceApproximately half of the annual carbon fixation on Earth occurs in the surface ocean through the photosynthetic activities of phytoplankton such as the ubiquitous picocyanobacterium Prochlorococcus. Ecologically-distinct subpopulations of Prochlorococcus (or ecotypes) are central conduits of organic substrates into the ocean microbiome, thus playing important roles in surface ocean production. By measuring the chemical profile of three cultured ecotype strains, we observed striking differences in the likely chemical impact of Prochlorococcus subpopulations on their surroundings. Subpopulations differ along gradients of temperature, light and nutrient concentrations, suggesting that these chemical differences could affect carbon cycling in different ocean strata and should be considered in models of Prochlorococcus physiology and marine carbon dynamics.

microbiology↗

Harmful Algal Bloom-Forming Organism Responds to Nutrient Stress Distinctly From Model Phytoplankton

O_LIResources such as nitrogen (N) and phosphorus (P) play an important role in primary production and constraining phytoplankton bloom dynamics. Models to predict bloom dynamics require mechanistic knowledge of algal metabolic shifts in response to resource limitation. For well-studied model phytoplankton like diatoms, this information is plentiful. However, for less-studied groups such as the raphidophytes, there remain significant gaps in understanding metabolic changes associated with nutrient limitation. C_LIO_LIUsing a novel combination of metabolomics and transcriptomics, we examined how the harmful algal bloom-forming raphidophyte Heterosigma akashiwo shifts its metabolism under N- and P-stress. We chose H. akashiwo because of its ubiquity within estuarine environments worldwide, where bloom dynamics are influenced by N and P availability. C_LIO_LIOur results show that each stress phenotype is distinct in both the allocation of carbon and the recycling of macromolecules. Further, we identified biomarkers of N- and P-stress that may be applied in situ to help modelers and stakeholders manage, predict, and prevent future blooms. C_LIO_LIThese findings provide a mechanistic foundation to model the metabolic traits and trade-offs associated with N- and P-stress in H. akashiwo, and evaluate the extent to which these metabolic responses can be inferred in other phytoplankton groups. C_LI

ecology↗