Bolaños
Luis M.
Bolaños
Luis M.
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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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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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ArticleSeasonal mixed layer depth shapes phytoplankton physiology, viral production, and accumulation in the North Atlantic(Nature Research, 2021-11-17) Diaz, Ben P. ; Knowles, Benjamin ; Johns, Christopher T. ; Laber, Christien P. ; Bondoc, Karen Grace V. ; Haramaty, Liti ; Natale, Frank ; Harvey, Elizabeth L. ; Kramer, Sasha J. ; Bolaños, Luis M. ; Lowenstein, Daniel P. ; Fredricks, Helen F. ; Graff, Jason R. ; Westberry, Toby K. ; Mojica, Kristina D. A. ; Haëntjens, Nils ; Baetge, Nicholas ; Gaube, Peter ; Boss, Emmanuel S. ; Carlson, Craig A. ; Behrenfeld, Michael J. ; Van Mooy, Benjamin A. S. ; Bidle, Kay D.Seasonal shifts in phytoplankton accumulation and loss largely follow changes in mixed layer depth, but the impact of mixed layer depth on cell physiology remains unexplored. Here, we investigate the physiological state of phytoplankton populations associated with distinct bloom phases and mixing regimes in the North Atlantic. Stratification and deep mixing alter community physiology and viral production, effectively shaping accumulation rates. Communities in relatively deep, early-spring mixed layers are characterized by low levels of stress and high accumulation rates, while those in the recently shallowed mixed layers in late-spring have high levels of oxidative stress. Prolonged stratification into early autumn manifests in negative accumulation rates, along with pronounced signatures of compromised membranes, death-related protease activity, virus production, nutrient drawdown, and lipid markers indicative of nutrient stress. Positive accumulation renews during mixed layer deepening with transition into winter, concomitant with enhanced nutrient supply and lessened viral pressure.
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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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ArticleToward a synthesis of phytoplankton communities composition methods for global-scale application(Association for the Sciences of Limnology and Oceanography (ASLO), 2024-02-23) Kramer, Sasha J. ; Bolanos, Luis M. ; Catlett, Dylan ; Chase, Alison P. ; Behrenfeld, Michael J. ; Boss, Emmanuel S. ; Crockford, E. Taylor ; Giovannoni, Stephen J. ; Graff, Jason R. ; Haentjens, Nils ; Karp-Boss, Lee ; Peacock, Emily E. ; Roesler, Collin S. ; Sosik, Heidi M. ; Siegel, David A.The composition of the marine phytoplankton community has been shown to impact many biogeochemical processes and marine ecosystem services. A variety of methods exist to characterize phytoplankton community composition (PCC), with varying degrees of taxonomic resolution. Accordingly, the resulting PCC determinations are dependent on the method used. Here, we use surface ocean samples collected in the North Atlantic and North Pacific Oceans to compare high-performance liquid chromatography pigment-based PCC to four other methods: quantitative cell imaging, flow cytometry, and 16S and 18S rRNA amplicon sequencing. These methods allow characterization of both prokaryotic and eukaryotic PCC across a wide range of size classes. PCC estimates of many taxa resolved at the class level (e.g., diatoms) show strong positive correlations across methods, while other groups (e.g., dinoflagellates) are not well captured by one or more methods. Since variations in phytoplankton pigment concentrations are related to changes in optical properties, this combined dataset expands the potential scope of ocean color remote sensing by associating PCC at the genus- and species-level with group- or class-level PCC from pigments. Quantifying the strengths and limitations of pigment-based PCC methods compared to PCC assessments from amplicon sequencing, imaging, and cytometry methods is the first step toward the robust validation of remote sensing approaches to quantify PCC from space.
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ArticleRecurring 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.