Repeta Daniel J.

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Repeta

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Daniel J.

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0000-0003-1927-0599

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Phosphonate cycling supports methane and ethylene supersaturation in the phosphate-depleted western North Atlantic Ocean

(Wiley, 2020-05-20) Sosa, Oscar A. ; Burrell, Timothy J. ; Wilson, Samuel T. ; Foreman, Rhea K. ; Karl, David M. ; Repeta, Daniel J.

In oligotrophic ocean regions, dissolved organic phosphorus (DOP) plays a prominent role as a source of phosphorus (P) to microorganisms. An important bioavailable component of DOP is phosphonates, organophosphorus compounds with a carbon‐phosphorus (C‐P) bond, which are ubiquitous in high molecular weight dissolved organic matter (HMWDOM). In addition to being a source of P, the degradation of phosphonates by the bacterial C‐P lyase enzymatic pathway causes the release of trace hydrocarbon gases relevant to climate and atmospheric chemistry. In this study, we investigated the roles of phosphate and phosphonate cycling in the production of methane (CH4) and ethylene (C2H4) in the western North Atlantic Ocean, a region that features a transition in phosphate concentrations from coastal to open ocean waters. We observed an inverse relationship between phosphate and the saturation state of CH4 and C2H4 in the water column, and between phosphate and the relative abundance of the C‐P lyase marker gene phnJ . In phosphate‐depleted waters, methylphosphonate and 2‐hydroxyethylphosphonate, the C‐P lyase substrates that yield CH4 and C2H4, respectively, were readily degraded in proportions consistent with their abundance and bioavailability in HMWDOM and with the concentrations of CH4 and C2H4 in the water column. We conclude that phosphonate degradation through the C‐P lyase pathway is an important source and a common production pathway of CH4 and C2H4 in the phosphate‐depleted surface waters of the western North Atlantic Ocean and that phosphate concentration can be an important control on the saturation state of these gases in the upper ocean.
Towards integrating evolution, metabolism, and climate change studies of marine ecosystems

(Elsevier, 2019-07-24) Baltar, Federico ; Bayer, Barbara ; Bednarsek, Nina ; Deppeler, Stacy ; Escribano, Ruben ; Gonzalez, Carolina E. ; Hansman, Roberta L. ; Mishra, Rajani Kanta ; Moran, Mary Ann ; Repeta, Daniel J. ; Robinson, Carol ; Sintes, Eva ; Tamburini, Christian ; Valentin, Luis E. ; Herndl, Gerhard J.

Global environmental changes are challenging the structure and functioning of ecosystems. However, a mechanistic understanding of how global environmental changes will affect ecosystems is still lacking. The complex and interacting biological and physical processes spanning vast temporal and spatial scales that constitute an ecosystem make this a formidable problem. A unifying framework based on ecological theory, that considers fundamental and realized niches, combined with metabolic, evolutionary, and climate change studies, is needed to provide the mechanistic understanding required to evaluate and forecast the future of marine communities, ecosystems, and their services.
Ultrasonic nebulization for the elemental analysis of microgram-level samples with offline aerosol mass spectrometry

(European Geosciences Union, 2019-03-14) O'Brien, Rachel E. ; Ridley, Kelsey J. ; Canagaratna, Manjula R. ; Jayne, John T. ; Croteau, Philip L. ; Worsnop, Douglas R. ; Budisulistiorini, Sri Hapsari ; Surratt, Jason D. ; Follett, Christopher L. ; Repeta, Daniel J. ; Kroll, Jesse H.

The elemental composition of organic material in environmental samples – including atmospheric organic aerosol, dissolved organic matter, and other complex mixtures – provides insights into their sources and environmental processing. However, standard analytical techniques for measuring elemental ratios typically require large sample sizes (milligrams of material or more). Here we characterize a method for measuring elemental ratios in environmental samples, requiring only micrograms of material, using a small-volume nebulizer (SVN). The technique uses ultrasonic nebulization of samples to generate aerosol particles (100–300 nm diameter), which are then analyzed using an aerosol mass spectrometer (AMS). We demonstrate that the technique generates aerosol from complex organic mixtures with minimal changes to the elemental composition of the organic material and that quantification is possible using internal standards (e.g., NH154NO3). Sample volumes of 2–4 µL with total solution concentrations of at least 0.2 g L−1 form sufficient particle mass for elemental ratio measurement by the AMS, despite only a small fraction (∼ 0.1 %) of the sample forming fine particles after nebulization (with the remainder ending up as larger droplets). The method was applied to aerosol filter extracts from the field and laboratory, as well as to the polysaccharide fraction of dissolved organic matter (DOM) from the North Pacific Ocean. In the case of aerosol particles, the mass spectra and elemental ratios from the SVN–AMS agree with those from online AMS sampling. Similarly, for DOM, the elemental ratios determined from the SVN–AMS agree with those determined using combustion analysis. The SVN–AMS provides a platform for the rapid quantitative analysis of the elemental composition of complex organic mixtures and non-refractory inorganic salts from microgram samples with applications that include analysis of aerosol extracts and terrestrial, aquatic, and atmospheric dissolved organic matter.
Seasonal occurrence of anoxygenic photosynthesis in Tillari and Selaulim reservoirs, Western India

(Copernicus Publications on behalf of the European Geosciences Union, 2012-07-09) Kurian, S. ; Roy, Rajdeep ; Repeta, Daniel J. ; Gauns, M. U. ; Shenoy, D. M. ; Suresh, T. ; Sarkar, A. ; Narvenkar, G. ; Johnson, Carl G. ; Naqvi, S. W. A.

Phytoplankton and bacterial pigment compositions were determined by high performance liquid chromatography (HPLC) and liquid chromatography-mass spectrometry (LC-MS) in two freshwater reservoirs (Tillari Dam and Selaulim Dam), which are located at the foothills of the Western Ghats in India. These reservoirs experience anoxia in the hypolimnion during summer. Water samples were collected from both reservoirs during anoxic periods while one of them (Tillari Reservoir) was also sampled in winter, when convective mixing results in well-oxygenated conditions throughout the water column. During the period of anoxia (summer), bacteriochlorophyll (BChl) e isomers and isorenieratene, characteristic of brown sulfur bacteria, were dominant in the anoxic (sulfidic) layer of the Tillari Reservoir under low light intensities. The winter observations showed the dominance of small cells of Chlorophyll b-containing green algae and cyanobacteria, with minor presence of fucoxanthin-containing diatoms and peridinin-containing dinoflagellates. Using total BChl e concentration observed in June, the standing stock of brown sulfur bacteria carbon in the anoxic compartment of Tillari Reservoir was estimated to be 2.27 gC m−2, which is much higher than the similar estimate for carbon derived from oxygenic photosynthesis (0.82 gC m−2. The Selaulim Reservoir also displayed similar characteristics with the presence of BChl e isomers and isorenieratene in the anoxic hypolimnion during summer. Although sulfidic conditions prevailed in the water column below the thermocline, the occurrence of photo-autotrophic bacteria was restricted only to mid-depths (maximal concentration of BChl e isomers was detected at 0.2% of the surface incident light). This shows that the vertical distribution of photo-autotrophic sulfur bacteria is primarily controlled by light penetration in the water column where the presence of H2S provides a suitable biogeochemical environment for them to flourish.
Dissolved organic nitrogen hydrolysis rates in axenic cultures of Aureococcus anophagefferens (Pelagophyceae) : comparison with heterotrophic bacteria

(American Society for Microbiology, 2002-01) Berg, Gry M. ; Repeta, Daniel J. ; LaRoche, Julie

The marine autotroph Aureococcus anophagefferens (Pelagophyceae) was rendered axenic in order to investigate hydrolysis rates of peptides, chitobiose, acetamide, and urea as indicators of the ability to support growth on dissolved organic nitrogen. Specific rates of hydrolysis varied between 8 and 700% of rates observed in associated heterotrophic marine bacteria.
Isolation and characterization of bacteria that degrade phosphonates in marine dissolved organic matter

(Frontiers Media, 2017-09-26) Sosa, Oscar A. ; Repeta, Daniel J. ; Ferrón, Sara ; Bryant, Jessica A. ; Mende, Daniel R. ; Karl, David M. ; DeLong, Edward F.

Semi-labile dissolved organic matter (DOM) accumulates in surface waters of the oligotrophic ocean gyres and turns over on seasonal to annual timescales. This reservoir of DOM represents an important source of carbon, energy, and nutrients to marine microbial communities but the identity of the microorganisms and the biochemical pathways underlying the cycling of DOM remain largely uncharacterized. In this study we describe bacteria isolated from the North Pacific Subtropical Gyre (NPSG) near Hawaii that are able to degrade phosphonates associated with high molecular weight dissolved organic matter (HMWDOM), which represents a large fraction of semi-labile DOM. We amended dilution-to-extinction cultures with HMWDOM collected from NPSG surface waters and with purified HMWDOM enriched with polysaccharides bearing alkylphosphonate esters. The HMWDOM-amended cultures were enriched in Roseobacter isolates closely related to Sulfitobacter and close relatives of hydrocarbon-degrading bacteria of the Oceanospirillaceae family, many of which encoded phosphonate degradation pathways. Sulfitobacter cultures encoding C-P lyase were able to catabolize methylphosphonate and 2-hydroxyethylphosphonate, as well as the esters of these phosphonates found in native HMWDOM polysaccharides to acquire phosphorus while producing methane and ethylene, respectively. Conversely, growth of these isolates on HMWDOM polysaccharides as carbon source did not support robust increases in cell yields, suggesting that the constituent carbohydrates in HMWDOM were not readily available to these individual isolates. We postulate that the complete remineralization of HMWDOM polysaccharides requires more complex microbial inter-species interactions. The degradation of phosphonate esters and other common substitutions in marine polysaccharides may be key steps in the turnover of marine DOM.
Daily changes in phytoplankton lipidomes reveal mechanisms of energy storage in the open ocean

(Nature Publishing Group, 2018-12-05) Becker, Kevin W. ; Collins, James R. ; Durham, Bryndan P. ; Groussman, Ryan D. ; White, Angelicque E. ; Fredricks, Helen F. ; Ossolinski, Justin E. ; Repeta, Daniel J. ; Carini, Paul ; Armbrust, E. Virginia ; Van Mooy, Benjamin A. S.

Sunlight is the dominant control on phytoplankton biosynthetic activity, and darkness deprives them of their primary external energy source. Changes in the biochemical composition of phytoplankton communities over diel light cycles and attendant consequences for carbon and energy flux in environments remain poorly elucidated. Here we use lipidomic data from the North Pacific subtropical gyre to show that biosynthesis of energy-rich triacylglycerols (TAGs) by eukaryotic nanophytoplankton during the day and their subsequent consumption at night drives a large and previously uncharacterized daily carbon cycle. Diel oscillations in TAG concentration comprise 23 ± 11% of primary production by eukaryotic nanophytoplankton representing a global flux of about 2.4 Pg C yr−1. Metatranscriptomic analyses of genes required for TAG biosynthesis indicate that haptophytes and dinoflagellates are active members in TAG production. Estimates suggest that these organisms could contain as much as 40% more calories at sunset than at sunrise due to TAG production.
Structural characterization of natural nickel and copper binding ligands along the US GEOTRACES Eastern Pacific Zonal Transect

(Frontiers Media, 2016-11-30) Boiteau, Rene M. ; Till, Claire P. ; Ruacho, Angel ; Bundy, Randelle M. ; Hawco, Nicholas J. ; McKenna, Amy M. ; Barbeau, Katherine A. ; Bruland, Kenneth W. ; Saito, Mak A. ; Repeta, Daniel J.

Organic ligands form strong complexes with many trace elements in seawater. Various metals can compete for the same ligand chelation sites, and the final speciation of bound metals is determined by relative binding affinities, concentrations of binding sites, uncomplexed metal concentrations, and association/dissociation kinetics. Different ligands have a wide range of metal affinities and specificities. However, the chemical composition of these ligands in the marine environment remains poorly constrained, which has hindered progress in modeling marine metal speciation. In this study, we detected and characterized natural ligands that bind copper (Cu) and nickel (Ni) in the eastern South Pacific Ocean with liquid chromatography tandem inductively coupled plasma mass spectrometry (LC-ICPMS), and high-resolution electrospray ionization mass spectrometry (ESIMS). Dissolved Cu, Ni, and ligand concentrations were highest near the coast. Chromatographically unresolved polar compounds dominated ligands isolated near the coast by solid phase extraction. Offshore, metal and ligand concentrations decreased, but several new ligands appeared. One major ligand was detected that bound both Cu2+ and Ni2+. Based on accurate mass and fragmentation measurements, this compound has a molecular formula of [C20H21N4O8S2+M]+ (M = metal isotope) and contains several azole-like metal binding groups. Additional lipophilic Ni complexes were also present only in oligotrophic waters, with masses of 649, 698, and 712 m/z (corresponding to the 58Ni metal complex). Molecular formulae of [C32H54N3O6S2Ni]+ and [C33H56N3O6S2Ni]+ were determined for two of these compounds. Addition of Cu and Ni to the samples also revealed the presence of additional compounds that can bind both Ni and Cu. Although these specific compounds represent a small fraction of the total dissolved Cu and Ni pool, they highlight the compositional diversity and spatial heterogeneity of marine Ni and Cu ligands, as well as variability in the extent to which different metals in the same environment compete for ligand binding.
Revisiting the pink-red pigmented basidiomycete mirror yeast of the phyllosphere

(John Wiley & Sons, 2016-05-10) Cobban, Alec ; Edgcomb, Virginia P. ; Burgaud, Gaëtan ; Repeta, Daniel J. ; Leadbetter, Edward R.

By taking advantage of the ballistoconidium-forming capabilities of members of the genus Sporobolomyces, we recovered ten isolates from deciduous tree leaves collected from Vermont and Washington, USA. Analysis of the small subunit ribosomal RNA gene and the D1/D2 domain of the large subunit ribosomal RNA gene indicate that all isolates are closely related. Further analysis of their physiological attributes shows that all were similarly pigmented yeasts capable of growth under aerobic and microaerophilic conditions, all were tolerant of repeated freezing and thawing, minimally tolerant to elevated temperature and desiccation, and capable of growth in liquid or on solid media containing pectin or galacturonic acid. The scientific literature on ballistoconidium-forming yeasts indicates that they are a polyphyletic group. Isolates of Sporobolomyces from two geographically separated sites show almost identical phenotypic and physiological characteristics and a monophyly with a broad group of differently named Sporobolomyces/Sporidiobolus species based on both small subunit ribosomal RNA (SSU rRNA) and D1/D2 domains of the LSU rRNA gene sequences.
Element-selective targeting of nutrient metabolites in environmental samples by inductively coupled plasma mass spectrometry and electrospray ionization mass spectrometry

(Frontiers Media, 2021-03-13) Li, Jingxuan ; Boiteau, Rene M. ; Babcock-Adams, Lydia ; Song, Zhongchang ; McIlvin, Matthew R. ; Repeta, Daniel J.

Metabolites that incorporate elements other than carbon, nitrogen, hydrogen and oxygen can be selectively detected by inductively coupled mass spectrometry (ICPMS). When used in parallel with chromatographic separations and conventional electrospray ionization mass spectrometry (ESIMS), ICPMS allows the analyst to quickly find, characterize and identify target metabolites that carry nutrient elements (P, S, trace metals; “nutrient metabolites”), which are of particular interest to investigations of microbial biogeochemical cycles. This approach has been applied to the study of siderophores and other trace metal organic ligands in the ocean. The original method used mass search algorithms that relied on the ratio of stable isotopologues of iron, copper and nickel to assign mass spectra collected by ESIMS to metabolites carrying these elements detected by ICPMS. However, while isotopologue-based mass assignment algorithms were highly successful in characterizing metabolites that incorporate some trace metals, they do not realize the whole potential of the ICPMS/ESIMS approach as they cannot be used to assign the molecular ions of metabolites with monoisotopic elements or elements for which the ratio of stable isotopes is not known. Here we report a revised ICPMS/ESIMS method that incorporates a number of changes to the configuration of instrument hardware that improves sensitivity of the method by a factor of 4–5, and allows for more accurate quantitation of metabolites. We also describe a new suite of mass search algorithms that can find and characterize metabolites that carry monoisotopic elements. We used the new method to identify siderophores in a laboratory culture of Vibrio cyclitrophicus and a seawater sample collected in the North Pacific Ocean, and to assign molecular ions to monoisotopic cobalt and iodine nutrient metabolites in extracts of a laboratory culture of the marine cyanobacterium Prochorococcus MIT9215.
Iron depletion in the deep chlorophyll maximum: mesoscale eddies as natural iron fertilization experiments

(American Geophysical Union, 2021-11-17) Hawco, Nicholas J. ; Barone, Benedetto ; Church, Matthew J. ; Babcock-Adams, Lydia ; Repeta, Daniel J. ; Wear, Emma K. ; Foreman, Rhea K. ; Björkman, Karin M. ; Bent, Shavonna M. ; Van Mooy, Benjamin A. S. ; Sheyn, Uri ; DeLong, Edward F. ; Acker, Marianne ; Kelly, Rachel L. ; Nelson, Alexa ; Ranieri, John ; Clemente, Tara M. ; Karl, David M. ; John, Seth G.

In stratified oligotrophic waters, phytoplankton communities forming the deep chlorophyll maximum (DCM) are isolated from atmospheric iron sources above and remineralized iron sources below. Reduced supply leads to a minimum in dissolved iron (dFe) near 100 m, but it is unclear if iron limits growth at the DCM. Here, we propose that natural iron addition events occur regularly with the passage of mesoscale eddies, which alter the supply of dFe and other nutrients relative to the availability of light, and can be used to test for iron limitation at the DCM. This framework is applied to two eddies sampled in the North Pacific Subtropical Gyre. Observations in an anticyclonic eddy center indicated downwelling of iron-rich surface waters, leading to increased dFe at the DCM but no increase in productivity. In contrast, uplift of isopycnals within a cyclonic eddy center increased supply of both nitrate and dFe to the DCM, and led to dominance of picoeukaryotic phytoplankton. Iron addition experiments did not increase productivity in either eddy, but significant enhancement of leucine incorporation in the light was observed in the cyclonic eddy, a potential indicator of iron stress among Prochlorococcus. Rapid cycling of siderophores and low dFe:nitrate uptake ratios also indicate that a portion of the microbial community was stressed by low iron. However, near-complete nitrate drawdown in this eddy, which represents an extreme case in nutrient supply compared to nearby Hawaii Ocean Time-series observations, suggests that recycling of dFe in oligotrophic ecosystems is sufficient to avoid iron limitation in the DCM under typical conditions.
Bacterial quorum-sensing signal arrests phytoplankton cell division and impacts virus-induced mortality

(American Society for Microbiology, 2021-05-12) Pollara, Scott B. ; Becker, Jamie W. ; Nunn, Brook L. ; Boiteau, Rene M. ; Repeta, Daniel J. ; Mudge, Miranda C. ; Downing, Grayton ; Chase, Davis ; Harvey, Elizabeth L. ; Whalen, Kristen E.

Interactions between phytoplankton and heterotrophic bacteria fundamentally shape marine ecosystems by controlling primary production, structuring marine food webs, mediating carbon export, and influencing global climate. Phytoplankton-bacterium interactions are facilitated by secreted compounds; however, linking these chemical signals, their mechanisms of action, and their resultant ecological consequences remains a fundamental challenge. The bacterial quorum-sensing signal 2-heptyl-4-quinolone (HHQ) induces immediate, yet reversible, cellular stasis (no cell division or mortality) in the coccolithophore Emiliania huxleyi; however, the mechanism responsible remains unknown. Using transcriptomic and proteomic approaches in combination with diagnostic biochemical and fluorescent cell-based assays, we show that HHQ exposure leads to prolonged S-phase arrest in phytoplankton coincident with the accumulation of DNA damage and a lack of repair despite the induction of the DNA damage response (DDR). While this effect is reversible, HHQ-exposed phytoplankton were also protected from viral mortality, ascribing a new role of quorum-sensing signals in regulating multitrophic interactions. Furthermore, our data demonstrate that in situ measurements of HHQ coincide with areas of enhanced micro- and nanoplankton biomass. Our results suggest bacterial communication signals as emerging players that may be one of the contributing factors that help structure complex microbial communities throughout the ocean.
Understanding the role of the biological pump in the global carbon cycle : an imperative for ocean science

(The Oceanography Society, 2014-09) Honjo, Susumu ; Eglinton, Timothy I. ; Taylor, Craig D. ; Ulmer, Kevin M. ; Sievert, Stefan M. ; Bracher, Astrid ; German, Christopher R. ; Edgcomb, Virginia P. ; Francois, Roger ; Iglesias-Rodriguez, M. Debora ; Van Mooy, Benjamin A. S. ; Repeta, Daniel J.

Anthropogenically driven climate change will rapidly become Earth's dominant transformative influence in the coming decades. The oceanic biological pump—the complex suite of processes that results in the transfer of particulate and dissolved organic carbon from the surface to the deep ocean—constitutes the main mechanism for removing CO2 from the atmosphere and sequestering carbon at depth on submillennium time scales. Variations in the efficacy of the biological pump and the strength of the deep ocean carbon sink, which is larger than all other bioactive carbon reservoirs, regulate Earth's climate and have been implicated in past glacial-interglacial cycles. The numerous biological, chemical, and physical processes involved in the biological pump are inextricably linked and heterogeneous over a wide range of spatial and temporal scales, and they influence virtually the entire ocean ecosystem. Thus, the functioning of the oceanic biological pump is not only relevant to the modulation of Earth's climate but also constitutes the basis for marine biodiversity and key food resources that support the human population. Our understanding of the biological pump is far from complete. Moreover, how the biological pump and the deep ocean carbon sink will respond to the rapid and ongoing anthropogenic changes to our planet—including warming, acidification, and deoxygenation of ocean waters—remains highly uncertain. To understand and quantify present-day and future changes in biological pump processes requires sustained global observations coupled with extensive modeling studies supported by international scientific coordination and funding.
Sampling of basement fluids via circulation obviation retrofit kits (CORKs) for dissolved gases, fluid fixation at the seafloor, and the characterization of organic carbon

(Elsevier, 2020-08-15) Lin, Huei-Ting ; Hsieh, Chih-Chiang ; Repeta, Daniel J. ; Rappe, Michael S.

The advanced instrumented GeoMICROBE sleds (Cowen et al., 2012) facilitate the collection of hydrothermal fluids and suspended particles in the subseafloor (basaltic) basement through Circulation Obviation Retrofit Kits (CORKs) installed within boreholes of the Integrated Ocean Drilling Program. The main components of the GeoMICROBE can be converted into a mobile pumping system (MPS) that is installed on the front basket of a submersible or remotely-operated-vehicle (ROV). Here, we provide details of a hydrothermal fluid-trap used on the MPS, through which a gastight sampler can withdraw fluids. We also applied the MPS to demonstrate the value of fixing samples at the seafloor in order to determine redox-sensitive dissolved iron concentrations and speciation measurements. To make the best use of the GeoMICROBE sleds, we describe a miniature and mobile version of the GeoMICROBE sled, which permits rapid turn-over and is relatively easy for preparation and operation. Similar to GeoMICROBE sleds, the Mobile GeoMICROBE (MGM) is capable of collecting fluid samples, filtration of suspended particles, and extraction of organics. We validate this approach by demonstrating the seafloor extraction of hydrophobic organics from a large volume (247L) of hydrothermal fluids. • We describe the design of a hydrothermal fluid-trap for use with a gastight sampler, as well as the use of seafloor fixation, through ROV- or submersible assisted mobile pumping systems. • We describe the design of a Mobile GeoMICROBE (MGM) that enhances large volume hydrothermal fluid sampling, suspended particle filtration, and organic matter extraction on the seafloor. • We provide an example of organic matter extracted and characterized from hydrothermal fluids via a MGM.
Phosphorus dynamics in biogeochemically distinct regions of the southeast subtropical Pacific Ocean

(Elsevier, 2016-12-29) Duhamel, Solange ; Björkman, Karin M. ; Repeta, Daniel J. ; Karl, David M.

The southeast subtropical Pacific Ocean was sampled along a zonal transect between the coasts of Chile and Easter Island. This remote area of the world’s ocean presents strong gradients in physical (e.g., temperature, density and light), chemical (e.g., salinity and nutrient concentrations) and microbiological (e.g., cell abundances, biomass and specific growth rates) properties. The goal of this study was to describe the phosphorus (P) dynamics in three main ecosystems along this transect: the upwelling regime off the northern Chilean coast, the oligotrophic area associated with the southeast subtropical Pacific gyre and the transitional area in between these two biomes. We found that inorganic phosphate (Pi) concentrations were high and turnover times were long (>210 nmol l−1 and >31 d, respectively) in the upper water column, along the entire transect. Pi uptake rates in the gyre were low (euphotic layer integrated rates were 0.26 mmol m−2 d−1 in the gyre and 1.28 mmol m−2 d−1 in the upwelling region), yet not only driven by decreases in particle mass or cell abundance (particulate P- and cell- normalized Pi uptake rates in the euphotic layer were ∼1–4 times and ∼3–15 times lower in the gyre than in the upwelling, respectively). However these Pi uptake rates were at or near the maximum Pi uptake velocity (i.e., uptake rates in Pi amended samples were not significantly different from those at ambient concentration: 1.5 and 23.7 nmol l−1 d−1 at 50% PAR in the gyre and upwelling, respectively). Despite the apparent Pi replete conditions, selected dissolved organic P (DOP) compounds were readily hydrolyzed. Nucleotides were the most bioavailable of the DOP substrates tested. Microbes actively assimilated adenosine-5′-triphosphate (ATP) leading to Pi and adenosine incorporation as well as Pi release to the environment. The southeast subtropical Pacific Ocean is a Pi-sufficient environment, yet DOP hydrolytic processes are maintained and contribute to P-cycling across the wide range of environmental conditions present in this ecosystem.
High molecular weight dissolved organic matter enrichment selects for methylotrophs in dilution to extinction cultures

(Nature Publishing Group, 2015-05-15) Sosa, Oscar A. ; Gifford, Scott M. ; Repeta, Daniel J. ; DeLong, Edward F.

The role of bacterioplankton in the cycling of marine dissolved organic matter (DOM) is central to the carbon and energy balance in the ocean, yet there are few model organisms available to investigate the genes, metabolic pathways, and biochemical mechanisms involved in the degradation of this globally important carbon pool. To obtain microbial isolates capable of degrading semi-labile DOM for growth, we conducted dilution to extinction cultivation experiments using seawater enriched with high molecular weight (HMW) DOM. In total, 93 isolates were obtained. Amendments using HMW DOM to increase the dissolved organic carbon concentration 4x (280 μM) or 10x (700 μM) the ocean surface water concentrations yielded positive growth in 4–6% of replicate dilutions, whereas <1% scored positive for growth in non-DOM-amended controls. The majority (71%) of isolates displayed a distinct increase in cell yields when grown in increasing concentrations of HMW DOM. Whole-genome sequencing was used to screen the culture collection for purity and to determine the phylogenetic identity of the isolates. Eleven percent of the isolates belonged to the gammaproteobacteria including Alteromonadales (the SAR92 clade) and Vibrio. Surprisingly, 85% of isolates belonged to the methylotrophic OM43 clade of betaproteobacteria, bacteria thought to metabolically specialize in degrading C1 compounds. Growth of these isolates on methanol confirmed their methylotrophic phenotype. Our results indicate that dilution to extinction cultivation enriched with natural sources of organic substrates has a potential to reveal the previously unsuspected relationships between naturally occurring organic nutrients and the microorganisms that consume them.
Unifying chemical and biological perspectives of carbon accumulation in the environment

(National Academy of Sciences, 2021-03-16) Repeta, Daniel J.

Heterotrophic microorganisms are fiendishly clever at degrading all shapes and sizes of organic compounds to extract the energy they need to build biomass. Every year marine phytoplankton fix ∼50 billion tons of carbon dioxide into organic matter, and every year marine heterotrophs respire nearly all of this organic matter back to carbon dioxide (1). Nearly all, but not all. With each spin of this carbon cycle, a small amount of organic matter escapes respiration and becomes sequestered in seawater, sediments, and soils. Over time, this small “leak” in the system leads to the accumulation of a vast reservoir of carbon; some 5 × 1019 kg of organic matter are thought to be sequestered in sedimentary rocks (2). This carbon sequestration has immense consequences for life on Earth, as illustrated by the change in climate we are now experiencing due in part to the transfer of a minute portion of this inventory from geologic reservoirs into the atmosphere.
Diversity and productivity of photosynthetic picoeukaryotes in biogeochemically distinct regions of the South East Pacific Ocean

(John Wiley & Sons, 2016-01-08) Rii, Yoshimi M. ; Duhamel, Solange ; Bidigare, Robert R. ; Karl, David M. ; Repeta, Daniel J. ; Church, Matthew J.

Picophytoplankton, including photosynthetic picoeukaryotes (PPE) and unicellular cyanobacteria, are important contributors to plankton biomass and primary productivity. In this study, phytoplankton composition and rates of carbon fixation were examined across a large trophic gradient in the South East Pacific Ocean (SEP) using a suite of approaches: photosynthetic pigments, rates of 14C-primary productivity, and phylogenetic analyses of partial 18S rRNA genes PCR amplified and sequenced from flow cytometrically sorted cells. While phytoplankton >10 μm (diatoms and dinoflagellates) were prevalent in the upwelling region off the Chilean coast, picophytoplankton consistently accounted for 55–92% of the total chlorophyll a inventories and >60% of 14C-primary productivity throughout the sampling region. Estimates of rates of 14C-primary productivity derived from flow cytometric sorting of radiolabeled cells revealed that the contributions of PPE and Prochlorococcus to euphotic zone depth-integrated picoplankton productivity were nearly equivalent (ranging 36–57%) along the transect, with PPE comprising a larger share of picoplankton productivity than cyanobacteria in the well-lit (>15% surface irradiance) region compared with in the lower regions (1–7% surface irradiance) of the euphotic zone. 18S rRNA gene sequence analyses revealed the taxonomic identities of PPE; e.g., Mamiellophyceae (Ostreococcus) were the dominant PPE in the upwelling-influenced waters, while members of the Chrysophyceae, Prymnesiophyceae, Pelagophyceae, and Prasinophyceae Clades VII and IX flourished in the oligotrophic South Pacific Subtropical Gyre. Our results suggest that, despite low numerical abundance in comparison to cyanobacteria, diverse members of PPE are significant contributors to carbon cycling across biogeochemically distinct regions of the SEP.
Reconstructing the phytoplankton community of the Cariaco Basin during the Younger Dryas cold event using chlorin steryl esters

(American Geophysical Union, 2004-01-29) Dahl, Kristina A. ; Repeta, Daniel J. ; Goericke, R.

A record of the downcore distribution of chlorin steryl esters (CSEs) through the Younger Dryas was produced from Cariaco Basin sediments in order to assess the potential use of CSEs as recorders of the structure of phytoplankton communities through time. Using an improved high-performance liquid chromatography method for the separation of CSEs, we find significant changes in the distribution of CSEs during the Younger Dryas in the Cariaco Basin. During the Younger Dryas, enhanced upwelling in the Cariaco Basin caused an increase in the diatom population and therefore an increase in the relative abundance of CSEs derived from diatoms. In contrast, the dinoflagellate population, and therefore CSEs derived from dinoflagellates, decreased in response to the climate change during the Younger Dryas. These community shifts agree well with the shifts observed in the present day on a seasonal basis that result from the north-south migration of the Intertropical Convergence Zone over the Cariaco Basin. We also identify changes in the abundance of several CSEs that seem to reflect rapid warming and cooling events. This study suggests that CSEs are useful proxies for reconstructing phytoplankton communities and paleoenvironments.
Phosphonate production by marine microbes: exploring new sources and potential function

(National Academy of Sciences, 2022-03-07) Acker, Marianne ; Hogle, Shane L. ; Berube, Paul M. ; Hackl, Thomas ; Coe, Allison ; Stepanauskas, Ramunas ; Chisholm, Sallie W. ; Repeta, Daniel J.

Phosphonates are organophosphorus metabolites with a characteristic C-P bond. They are ubiquitous in the marine environment, their degradation broadly supports ecosystem productivity, and they are key components of the marine phosphorus (P) cycle. However, the microbial producers that sustain the large oceanic inventory of phosphonates as well as the physiological and ecological roles of phosphonates are enigmatic. Here, we show that phosphonate synthesis genes are rare but widely distributed among diverse bacteria and archaea, including Prochlorococcus and SAR11, the two major groups of bacteria in the ocean. In addition, we show that Prochlorococcus can allocate over 40% of its total cellular P-quota toward phosphonate production. However, we find no evidence that Prochlorococcus uses phosphonates for surplus P storage, and nearly all producer genomes lack the genes necessary to degrade and assimilate phosphonates. Instead, we postulate that phosphonates are associated with cell-surface glycoproteins, suggesting that phosphonates mediate ecological interactions between the cell and its surrounding environment. Our findings indicate that the oligotrophic surface ocean phosphonate pool is sustained by a relatively small fraction of the bacterioplankton cells allocating a significant portion of their P quotas toward secondary metabolism and away from growth and reproduction.

Repeta Daniel J.

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