Liu
Shuting
Liu
Shuting
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ArticleLinkages 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.
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ArticleInfluence of amino acids on bacterioplankton production, biomass and community composition at Ocean Station Papa in the subarctic Pacific(University of California Press, 2023-05-02) Stephens, Brandon M. ; Fox, James ; Liu, Shuting ; Halsey, Kimberly H. ; Nicholson, David P. ; Traylor, Shawnee ; Carlson, Craig A.Bacterioplankton play a central role in carbon cycling, yet their relative contributions to carbon production and removal can be difficult to constrain. As part of the Export Processes in the Ocean from RemoTe Sensing (EXPORTS) program, this study identifies potential influences of bacterioplankton community and dissolved organic matter (DOM) composition on carbon cycling at Ocean Station Papa in August 2018. Surface (5–35 m) bacterioplankton production rates and stocks spanned a 2- to 3-fold range over the 3-week cruise and correlated positively with the DOM degradation state, estimated using the mole proportion of total dissolved amino acids. When the DOM was more degraded, 16S rRNA gene amplicon data revealed a less diverse bacterioplankton community with a significant contribution from members of the Flavobacteriaceae family. Over the course of 7–10 d, as the DOM quality improved (became less degraded) and bacterioplankton productivity increased, the responding bacterioplankton community became more diverse, with increased relative contributions from members of the SAR86, SAR11 and AEGEAN-169 clades. The cruise mean for mixed layer, depth-integrated bacterioplankton carbon demand (gross bacterioplankton production) was 5.2 mmol C m−2 d−1, representing 60% of net primary production, where the difference between net primary production and bacterioplankton carbon demand was less than sinking flux at 50 m. The concentrations of dissolved organic carbon (cruise average of 58.5 µM C) did not exhibit a systematic change over the cruise period. Therefore, we hypothesize that carbon supplied from gross carbon production, values that were 2- to 3-fold greater than net primary production, provided the carbon necessary to account for the sinking flux and bacterioplankton carbon demand that were in excess of net primary production. These findings highlight the central contributions of bacterioplankton to carbon cycling at Ocean Station Papa, a site of high carbon recycling.
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ArticleDifferent 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.
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Working PaperEXPORTS Measurements and Protocols for the NE Pacific Campaign(NASA STI Program and Woods Hole Oceanographic Institution, 2021-02) Behrenfeld, Michael J. ; Benitez-Nelson, Claudia R. ; Boss, Emmanuel S. ; Brzezinski, Mark A. ; Buck, Kristen N. ; Buesseler, Ken O. ; Burd, Adrian B. ; Carlson, Craig A. ; Cassar, Nicolas ; Cetinić, Ivona ; Close, Hilary G. ; Craig, Susanne E. ; D'Asaro, Eric A. ; Durkin, Colleen A. ; Estapa, Margaret L. ; Fassbender, Andrea ; Fox, James ; Freeman, Scott ; Gifford, Scott M. ; Gong, Weida ; Graff, Jason R. ; Gray, Deric ; Guidi, Lionel ; Halsey, Kim ; Hansell, Dennis A. ; Haëntjens, Nils ; Horner, Tristan J. ; Jenkins, Bethany D. ; Jones, Janice L. ; Karp-Boss, Lee ; Kramer, Sasha J. ; Lam, Phoebe J. ; Lee, Craig M. ; Lee, Jong-Mi ; Liu, Shuting ; Mannino, Antonio ; Maas, Amy E. ; Marchal, Olivier ; Marchetti, Adrian ; McDonnell, Andrew M. P. ; McNair, Heather ; Menden-Deuer, Susanne ; Morison, Francoise ; Nelson, Norman B. ; Nicholson, David P. ; Niebergall, Alexandria K. ; Omand, Melissa M. ; Passow, Uta ; Perry, Mary J. ; Popp, Brian N. ; Proctor, Chris ; Rafter, Patrick ; Roca-Martí, Montserrat ; Roesler, Collin S. ; Rubin, Edwina ; Rynearson, Tatiana A. ; Santoro, Alyson E. ; Siegel, David A. ; Sosik, Heidi M. ; Soto Ramos, Inia ; Stamieszkin, Karen ; Steinberg, Deborah K. ; Stephens, Brandon M. ; Thompson, Andrew F. ; Van Mooy, Benjamin A. S. ; Zhang, XiaodongEXport Processes in the Ocean from Remote Sensing (EXPORTS) is a large-scale NASA-led and NSF co-funded field campaign that will provide critical information for quantifying the export and fate of upper ocean net primary production (NPP) using satellite information and state of the art technology.
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ArticleMigratory 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.
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ArticleSeasonal 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.
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ArticleSuboxic 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.
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ArticleMarine particle size-fractionation indicates organic matter is processed by differing microbial communities on depth-specific particles(Oxford University Press, 2024-07-12) Comstock, Jacqueline ; Henderson, Lillian C. ; Close, Hilary G. ; Liu, Shuting ; Vergin, Kevin L. ; Worden, Alexandra Z. ; Wittmers, Fabian ; Halewood, Elisa ; Giovannoni, Stephen J. ; Carlson, Craig A.Passive sinking flux of particulate organic matter in the ocean plays a central role in the biological carbon pump and carbon export to the ocean’s interior. Particle-associated microbes colonize particulate organic matter, producing “hotspots” of microbial activity. We evaluated variation in particle-associated microbial communities to 500 m depth across four different particle size fractions (0.2–1.2, 1.2–5, 5–20, >20 μm) collected using in situ pumps at the Bermuda Atlantic Time-series Study site. In situ pump collections capture both sinking and suspended particles, complementing previous studies using sediment or gel traps, which capture only sinking particles. Additionally, the diagenetic state of size-fractionated particles was examined using isotopic signatures alongside microbial analysis. Our findings emphasize that different particle sizes contain distinctive microbial communities, and each size category experiences a similar degree of change in communities over depth, contradicting previous findings. The robust patterns observed in this study suggest that particle residence times may be long relative to microbial succession rates, indicating that many of the particles collected in this study may be slow sinking or neutrally buoyant. Alternatively, rapid community succession on sinking particles could explain the change between depths. Complementary isotopic analysis of particles revealed significant differences in composition between particles of different sizes and depths, indicative of organic particle transformation by microbial hydrolysis and metazoan grazing. Our results couple observed patterns in microbial communities with the diagenetic state of associated organic matter and highlight unique successional patterns in varying particle sizes across depth.