Parsons Rachel J.

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Parsons

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Rachel J.

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0000-0003-3634-8220

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Multifaceted impacts of the stony coral Porites astreoides on picoplankton abundance and community composition

(John Wiley & Sons, 2016-10-12) McNally, Sean ; Parsons, Rachel J. ; Santoro, Alyson E. ; Apprill, Amy

Picoplankton foster essential recycling of nutrients in the oligotrophic waters sustaining coral reef ecosystems. Despite this fact, there is a paucity of data on how the specific interactions between corals and planktonic bacteria and archaea (picoplankton) contribute to nutrient dynamics and reef productivity. Here, we utilized mesocosm experiments to investigate how corals and coral mucus influence picoplankton and nutrients in reef waters. Over 12 days, we tracked nutrient concentrations, picoplankton abundances and taxonomic composition of picoplankton using direct cell-counts, sequencing of SSU rRNA genes and fluorescent in situ hybridization-based abundances of dominant lineages in the presence or absence of Porites astreoides corals and with mucus additions. Our results demonstrate that when corals are present, Synechococcus, SAR11 and Rhodobacteraceae cells are preferentially removed. When corals were removed, their exudates enhanced the growth of diverse picoplankton, including SAR11 and Rhodobacteraceae. A seven-fold increase in nitrate concentration, possibly caused by nitrogen remineralization (ammonification coupled to nitrification) within the coral holobiont, may have further facilitated the growth of these taxa. In contrast, the addition of mucus resulted in rapid initial growth of total picoplankton and Rhodobacteraceae, but no measurable change in overall community structure. This study presents evidence of the multifaceted influences of corals on picoplankton, in which the coral holobiont selectively removes and promotes the growth of diverse picoplankton and remineralizes nitrogen.
Linkages among dissolved organic matter export, dissolved metabolites, and associated microbial community structure response in the northwestern Sargasso Sea on a seasonal scale

(Frontiers Media, 2022-03-08) Liu, Shuting ; Longnecker, Krista ; Kujawinski, Elizabeth B. ; Vergin, Kevin ; Bolaños, Luis M. ; Giovannoni, Stephen J. ; Parsons, Rachel J. ; Opalk, Keri ; Halewood, Elisa ; Hansell, Dennis A. ; Johnson, Rodney J. ; Curry, Ruth G. ; Carlson, Craig A.

Deep convective mixing of dissolved and suspended organic matter from the surface to depth can represent an important export pathway of the biological carbon pump. The seasonally oligotrophic Sargasso Sea experiences annual winter convective mixing to as deep as 300 m, providing a unique model system to examine dissolved organic matter (DOM) export and its subsequent compositional transformation by microbial oxidation. We analyzed biogeochemical and microbial parameters collected from the northwestern Sargasso Sea, including bulk dissolved organic carbon (DOC), total dissolved amino acids (TDAA), dissolved metabolites, bacterial abundance and production, and bacterial community structure, to assess the fate and compositional transformation of DOM by microbes on a seasonal time-scale in 2016–2017. DOM dynamics at the Bermuda Atlantic Time-series Study site followed a general annual trend of DOC accumulation in the surface during stratified periods followed by downward flux during winter convective mixing. Changes in the amino acid concentrations and compositions provide useful indices of diagenetic alteration of DOM. TDAA concentrations and degradation indices increased in the mesopelagic zone during mixing, indicating the export of a relatively less diagenetically altered (i.e., more labile) DOM. During periods of deep mixing, a unique subset of dissolved metabolites, such as amino acids, vitamins, and benzoic acids, was produced or lost. DOM export and compositional change were accompanied by mesopelagic bacterial growth and response of specific bacterial lineages in the SAR11, SAR202, and SAR86 clades, Acidimicrobiales, and Flavobacteria, during and shortly following deep mixing. Complementary DOM biogeochemistry and microbial measurements revealed seasonal changes in DOM composition and diagenetic state, highlighting microbial alteration of the quantity and quality of DOM in the ocean.
Different carboxyl-rich alicyclic molecules proxy compounds select distinct bacterioplankton for oxidation of dissolved organic matter in the mesopelagic Sargasso Sea

(Wiley, 2020-01-23) Liu, Shuting ; Parsons, Rachel J. ; Opalk, Keri ; Baetge, Nicholas ; Giovannoni, Stephen J. ; Bolaños, Luis M. ; Kujawinski, Elizabeth B. ; Longnecker, Krista ; Lu, YueHan ; Halewood, Elisa ; Carlson, Craig A.

Marine dissolved organic matter (DOM) varies in its recalcitrance to rapid microbial degradation. DOM of varying recalcitrance can be exported from the ocean surface to depth by subduction or convective mixing and oxidized over months to decades in deeper seawater. Carboxyl‐rich alicyclic molecules (CRAM) are characterized as a major component of recalcitrant DOM throughout the oceanic water column. The oxidation of CRAM‐like compounds may depend on specific bacterioplankton lineages with oxidative enzymes capable of catabolizing complex molecular structures like long‐chain aliphatics, cyclic alkanes, and carboxylic acids. To investigate the interaction between bacteria and CRAM‐like compounds, we conducted microbial remineralization experiments using several compounds rich in carboxyl groups and/or alicyclic rings, including deoxycholate, humic acid, lignin, and benzoic acid, as proxies for CRAM. Mesopelagic seawater (200 m) from the northwest Sargasso Sea was used as media and inoculum and incubated over 28 d. All amendments demonstrated significant DOC removal (2–11 μmol C L−1) compared to controls. Bacterioplankton abundance increased significantly in the deoxycholate and benzoic acid treatments relative to controls, with fast‐growing Spongiibacteracea, Euryarcheaota, and slow‐growing SAR11 enriched in the deoxycholate treatment and fast‐growing Alteromonas, Euryarcheaota, and Thaumarcheaota enriched in the benzoic acid treatment. In contrast, bacterioplankton grew slower in the lignin and humic acid treatments, with oligotrophic SAR202 becoming significantly enriched in the lignin treatment. Our results indicate that the character of the CRAM proxy compounds resulted in distinct bacterioplankton removal rates of DOM and affected specific lineages of bacterioplankton capable of responding.
Removal of organic carbon by natural bacterioplankton communities as a function of pCO2 from laboratory experiments between 2012 and 2016

(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2016-11-18) Passow, Uta ; Brzezinski, Mark A. ; Carlson, Craig A. ; James, Anna K ; Parsons, Rachel J. ; Trapani, Jennifer N

Factors that affect the removal of organic carbon by heterotrophic bacterioplankton can impact the rate and magnitude of organic carbon loss in the ocean through the conversion of a portion of consumed organic carbon to CO2. Through enhanced rates of consumption, surface bacterioplankton communities can also reduce the amount of dissolved organic carbon (DOC) available for export from the surface ocean. The present study investigated the direct effects of elevated pCO2 on bacterioplankton removal of several forms of DOC ranging from glucose to complex phytoplankton exudate and lysate, and naturally occurring DOC. Elevated pCO2 (1000 – 1500 ppm) enhanced both the rate and magnitude of organic carbon removal by bacterioplankton communities compared to low (pre-industrial and ambient) pCO2 (250 – ~400 ppm). The increased removal was largely due to enhanced respiration, rather than enhanced production of bacterioplankton biomass. For a complete list of measurements, refer to the supplemental document 'Field_names.pdf', and a full dataset description is included in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: http://www.bco-dmo.org/dataset/472032
Dark production of extracellular superoxide by the coral Porites astreoides and representative symbionts

(Frontiers Media, 2016-11-24) Zhang, Tong ; Diaz, Julia M. ; Brighi, Caterina ; Parsons, Rachel J. ; McNally, Sean ; Apprill, Amy ; Hansel, Colleen M.

The reactive oxygen species (ROS) superoxide has been implicated in both beneficial and detrimental processes in coral biology, ranging from pathogenic disease resistance to coral bleaching. Despite the critical role of ROS in coral health, there is a distinct lack of ROS measurements and thus an incomplete understanding of underpinning ROS sources and production mechanisms within coral systems. Here, we quantified in situ extracellular superoxide concentrations at the surfaces of aquaria-hosted Porites astreoides during a diel cycle. High concentrations of superoxide (~10's of nM) were present at coral surfaces, and these levels did not change significantly as a function of time of day. These results indicate that the coral holobiont produces extracellular superoxide in the dark, independent of photosynthesis. As a short-lived anion at physiological pH, superoxide has a limited ability to cross intact biological membranes. Further, removing surface mucus layers from the P. astreoides colonies did not impact external superoxide concentrations. We therefore attribute external superoxide derived from the coral holobiont under these conditions to the activity of the coral host epithelium, rather than mucus-derived epibionts or internal sources such as endosymbionts (e.g., Symbiodinium). However, endosymbionts likely contribute to internal ROS levels via extracellular superoxide production. Indeed, common coral symbionts, including multiple strains of Symbiodinium (clades A to D) and the bacterium Endozoicomonas montiporae LMG 24815, produced extracellular superoxide in the dark and at low light levels. Further, representative P. astreoides symbionts, Symbiodinium CCMP2456 (clade A) and E. montiporae, produced similar concentrations of superoxide alone and in combination with each other, in the dark and low light, and regardless of time of day. Overall, these results indicate that healthy, non-stressed P. astreoides and representative symbionts produce superoxide externally, which is decoupled from photosynthetic activity and circadian control. Corals may therefore produce extracellular superoxide constitutively, highlighting an unclear yet potentially beneficial role for superoxide in coral physiology and health.
Pangenomics analysis reveals diversification of enzyme families and niche specialization in globally abundant SAR202 bacteria

(American Society for Microbiology, 2020-01-07) Saw, Jimmy H. W. ; Nunoura, Takuro ; Hirai, Miho ; Takaki, Yoshihiro ; Parsons, Rachel ; Michelsen, Michelle ; Longnecker, Krista ; Kujawinski, Elizabeth B. ; Stepanauskas, Ramunas ; Landry, Zachary ; Carlson, Craig A. ; Giovannoni, Stephen J.

It has been hypothesized that the abundant heterotrophic ocean bacterioplankton in the SAR202 clade of the phylum Chloroflexi evolved specialized metabolisms for the oxidation of organic compounds that are resistant to microbial degradation via common metabolic pathways. Expansions of paralogous enzymes were reported and implicated in hypothetical metabolism involving monooxygenase and dioxygenase enzymes. In the proposed metabolic schemes, the paralogs serve the purpose of diversifying the range of organic molecules that cells can utilize. To further explore SAR202 evolution and metabolism, we reconstructed single amplified genomes and metagenome-assembled genomes from locations around the world that included the deepest ocean trenches. In an analysis of 122 SAR202 genomes that included seven subclades spanning SAR202 diversity, we observed additional evidence of paralog expansions that correlated with evolutionary history, as well as further evidence of metabolic specialization. Consistent with previous reports, families of flavin-dependent monooxygenases were observed mainly in the group III SAR202 genomes, and expansions of dioxygenase enzymes were prevalent in those of group VII. We found that group I SAR202 genomes encode expansions of racemases in the enolase superfamily, which we propose evolved for the degradation of compounds that resist biological oxidation because of chiral complexity. Supporting the conclusion that the paralog expansions indicate metabolic specialization, fragment recruitment and fluorescent in situ hybridization (FISH) with phylogenetic probes showed that SAR202 subclades are indigenous to different ocean depths and geographical regions. Surprisingly, some of the subclades were abundant in surface waters and contained rhodopsin genes, altering our understanding of the ecological role of SAR202 species in stratified water columns. IMPORTANCE The oceans contain an estimated 662 Pg C in the form of dissolved organic matter (DOM). Information about microbial interactions with this vast resource is limited, despite broad recognition that DOM turnover has a major impact on the global carbon cycle. To explain patterns in the genomes of marine bacteria, we propose hypothetical metabolic pathways for the oxidation of organic molecules that are resistant to oxidation via common pathways. The hypothetical schemes we propose suggest new metabolic pathways and classes of compounds that could be important for understanding the distribution of organic carbon throughout the biosphere. These genome-based schemes will remain hypothetical until evidence from experimental cell biology can be gathered to test them. Our findings also fundamentally change our understanding of the ecology of SAR202 bacteria, showing that metabolically diverse variants of these cells occupy niches spanning all depths and are not relegated to the dark ocean.
Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton

(Inter-Research, 2015-06-04) Apprill, Amy ; McNally, Sean ; Parsons, Rachel ; Weber, Laura

High-throughput sequencing of small subunit ribosomal RNA (SSU rRNA) genes from marine environments is a widely applied method used to uncover the composition of microbial communities. We conducted an analysis of surface ocean waters with the commonly employed hypervariable 4 region SSU rRNA gene primers 515F and 806R, and found that bacteria belonging to the SAR11 clade of Alphaproteobacteria, a group typically making up 20 to 40% of the bacterioplankton in this environment, were greatly underrepresented and comprised <4% of the total community. Using the SILVA reference database, we found a single nucleotide mismatch to nearly all SAR11 subclades, and revised the 806R primer so that it increased the detection of SAR11 clade sequences in the database from 2.6 to 96.7%. We then compared the performance of the original and revised 806R primers in surface seawater samples, and found that SAR11 comprised 0.3 to 3.9% of sequences with the original primers and 17.5 to 30.5% of the sequences with the revised 806R primer. Furthermore, an investigation of seawater obtained from aquaria revealed that SAR11 sequences acquired with the revised 806R primer were more similar to natural cellular abundances of SAR11 detected using fluorescence in situ hybridization counts. Collectively, these results demonstrate that a minor adjustment to the 806R primer will greatly increase detection of the globally abundant SAR11 clade in marine and lake environments, and enable inclusion of this important bacterial lineage in experimental and environmental-based studies.
Methylphosphonate is utilized by commensal microbiota of macroalgae in the oligotrophic Sargasso Sea

(American Geophysical Union, 2023-12-07) Cox, Danielle D. ; Parsons, Rachel J. ; Van Mooy, Benjamin A. S. ; Valentine, David L.

The essential nutrient phosphorus is biologically scarce in the Sargasso Sea, yet the pelagic macroalgae Sargassum, for which this area of the North Atlantic Ocean is named, thrives. We tested the hypothesis that Sargassum holobionts utilize methylphosphonate (MPn) as an alternative source of phosphorus, finding lysis liberated phosphonate-derived methane. The observed activity occurred at concentrations as low as 35 nM MPn and was inhibited by antibiotics, implicating bacterial epibionts of the holobiont capable of MPn lysis at realistic environmental concentrations. Dark incubations resulted in diminished methane production, consistent with commensalism between microbe and host. A survey of macroalgal species inhabiting the Sargasso Sea found ubiquitous capacity for MPn lysis; such capacity was absent in species inhabiting phosphorus-replete waters of the California Current, pointing to phosphorous limitation as a selective pressure. These results suggest that bacterial epibionts of algal communities acquire phosphorus from phosphonates while simultaneously serving as a source of atmospheric methane.
Migratory zooplankton excreta and its influence on prokaryotic communities

(Frontiers Media, 2020-12-01) Maas, Amy E. ; Liu, Shuting ; Bolaños, Luis M. ; Widner, Brittany ; Parsons, Rachel ; Kujawinski, Elizabeth B. ; Blanco-Bercial, Leocadio ; Carlson, Craig A.

Particulate organic matter (POM) (fecal pellets) from zooplankton has been demonstrated to be an important nutrient source for the pelagic prokaryotic community. Significantly less is known about the chemical composition of the dissolved organic matter (DOM) produced by these eukaryotes and its influence on pelagic ecosystem structure. Zooplankton migrators, which daily transport surface-derived compounds to depth, may act as important vectors of limiting nutrients for mesopelagic microbial communities. In this role, zooplankton may increase the DOM remineralization rate by heterotrophic prokaryotes through the creation of nutrient rich “hot spots” that could potentially increase niche diversity. To explore these interactions, we collected the migratory copepod Pleuromamma xiphias from the northwestern Sargasso Sea and sampled its excreta after 12–16 h of incubation. We measured bulk dissolved organic carbon (DOC), dissolved free amino acids (DFAA) via high performance liquid chromatography and dissolved targeted metabolites via quantitative mass spectrometry (UPLC-ESI-MSMS) to quantify organic zooplankton excreta production and characterize its composition. We observed production of labile DOM, including amino acids, vitamins, and nucleosides. Additionally, we harvested a portion of the excreta and subsequently used it as the growth medium for mesopelagic (200 m) bacterioplankton dilution cultures. In zooplankton excreta treatments we observed a four-fold increase in bacterioplankton cell densities that reached stationary growth phase after five days of dark incubation. Analyses of 16S rRNA gene amplicons suggested a shift from oligotrophs typical of open ocean and mesopelagic prokaryotic communities to more copiotrophic bacterial lineages in the presence of zooplankton excreta. These results support the hypothesis that zooplankton and prokaryotes are engaged in complex and indirect ecological interactions, broadening our understanding of the microbial loop.
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.
Recurring seasonality exposes dominant species and niche partitioning strategies of open ocean picoeukaryotic algae

(Nature Research, 2024-05-20) Eckmann, Charlotte A. ; Bachy, Charles ; Wittmers, Fabian ; Strauss, Jan ; Blanco-Bercial, Leocadio ; Vergin, Kevin L. ; Parsons, Rachel J. ; Kudela, Raphael M. ; Johnson, Rod ; Bolanos, Luis M. ; Giovannoni, Stephen J. ; Carlson, Craig A. ; Worden, Alexandra Z.

Ocean spring phytoplankton blooms are dynamic periods important to global primary production. We document vertical patterns of a diverse suite of eukaryotic algae, the prasinophytes, in the North Atlantic Subtropical Gyre with monthly sampling over four years at the Bermuda Atlantic Time-series Study site. Water column structure was used to delineate seasonal stability periods more ecologically relevant than seasons defined by calendar dates. During winter mixing, tiny prasinophytes dominated by Class II comprise 46 ± 24% of eukaryotic algal (plastid-derived) 16S rRNA V1-V2 amplicons, specifically Ostreococcus Clade OII, Micromonas commoda, and Bathycoccus calidus. In contrast, Class VII are rare and Classes I and VI peak during warm stratified periods when surface eukaryotic phytoplankton abundances are low. Seasonality underpins a reservoir of genetic diversity from multiple prasinophyte classes during warm periods that harbor ephemeral taxa. Persistent Class II sub-species dominating the winter/spring bloom period retreat to the deep chlorophyll maximum in summer, poised to seed the mixed layer upon winter convection, exposing a mechanism for initiating high abundances at bloom onset. Comparisons to tropical oceans reveal broad distributions of the dominant sub-species herein. This unparalleled window into temporal and spatial niche partitioning of picoeukaryotic primary producers demonstrates how key prasinophytes prevail in warm oceans.
Suboxic DOM is bioavailable to surface prokaryotes in a simulated overturn of an oxygen minimum zone, Devil’s Hole, Bermuda

(Frontiers Media, 2023-12-19) Parsons, Rachel J. ; Liu, Shuting ; Longnecker, Krista ; Yongblah, Kevin ; Johnson, Carys ; Bolanos, Luis M. ; Comstock, Jacqueline ; Opalk, Keri ; Kido Soule, Melissa C. ; Garley, Rebecca ; Carlson, Craig A. ; Temperton, Ben ; Bates, Nicholas R.

Oxygen minimum zones (OMZs) are expanding due to increased sea surface temperatures, subsequent increased oxygen demand through respiration, reduced oxygen solubility, and thermal stratification driven in part by anthropogenic climate change. Devil’s Hole, Bermuda is a model ecosystem to study OMZ microbial biogeochemistry because the formation and subsequent overturn of the suboxic zone occur annually. During thermally driven stratification, suboxic conditions develop, with organic matter and nutrients accumulating at depth. In this study, the bioavailability of the accumulated dissolved organic carbon (DOC) and the microbial community response to reoxygenation of suboxic waters was assessed using a simulated overturn experiment. The surface inoculated prokaryotic community responded to the deep (formerly suboxic) 0.2 μm filtrate with cell densities increasing 2.5-fold over 6 days while removing 5 μmol L−1 of DOC. After 12 days, the surface community began to shift, and DOC quality became less diagenetically altered along with an increase in SAR202, a Chloroflexi that can degrade recalcitrant dissolved organic matter (DOM). Labile DOC production after 12 days coincided with an increase of Nitrosopumilales, a chemoautotrophic ammonia oxidizing archaea (AOA) that converts ammonia to nitrite based on the ammonia monooxygenase (amoA) gene copy number and nutrient data. In comparison, the inoculation of the deep anaerobic prokaryotic community into surface 0.2 μm filtrate demonstrated a die-off of 25.5% of the initial inoculum community followed by a 1.5-fold increase in cell densities over 6 days. Within 2 days, the prokaryotic community shifted from a Chlorobiales dominated assemblage to a surface-like heterotrophic community devoid of Chlorobiales. The DOM quality changed to less diagenetically altered material and coincided with an increase in the ribulose-1,5-bisphosphate carboxylase/oxygenase form I (cbbL) gene number followed by an influx of labile DOM. Upon reoxygenation, the deep DOM that accumulated under suboxic conditions is bioavailable to surface prokaryotes that utilize the accumulated DOC initially before switching to a community that can both produce labile DOM via chemoautotrophy and degrade the more recalcitrant DOM.

Parsons Rachel J.

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