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1. Diel oscillations in the feeding activity of heterotrophic and mixotrophic nanoplankton in the North Pacific Subtropical Gyre

   https://doi.org/10.3354/ame01950  

   Connell, PE; Ribalet, F; Armbrust, EV; White, A; Caron, DA (December 2020, Aquatic Microbial Ecology)

   null (Ed.)

   Daily oscillations in photosynthetically active radiation strongly influence the timing of metabolic processes in picocyanobacteria, but it is less clear how the light-dark cycle affects the activities of their consumers. We investigated the relationship between marine picocyanobacteria and nanoplanktonic consumers throughout the diel cycle to determine whether heterotrophic and mixotrophic protists (algae with phagotrophic ability) display significant periodicity in grazing pressure. Carbon biomass of Prochlorococcus and Synechococcus was estimated continuously from abundances and cell size measurements made by flow cytometry. Picocyanobacterial dynamics were then compared to nanoplankton abundances and ingestion of fluorescently labeled bacteria measured every 4 h during a 4 d survey in the North Pacific Subtropical Gyre. Grazing of the labeled bacteria by heterotrophic nanoplankton was significantly greater at night than during the day. The grazing activity of mixotrophic nanoplankton showed no diel periodicity, suggesting that they may feed continuously, albeit at lower rates than heterotrophic nanoplankton, to alleviate nutrient limitation in this oligotrophic environment. Diel changes in Prochlorococcus biomass indicated that they could support substantial growth of nanoplankton if those grazers are the main source of picocyanobacterial mortality, and that grazers may contribute to temporally stable abundances of picocyanobacteria. 

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2. Prochlorococcus Exudate Stimulates Heterotrophic Bacterial Competition with Rival Phytoplankton for Available Nitrogen

   https://doi.org/10.1128/mbio.02571-21  

   Calfee, Benjamin C.; Glasgo, Liz D.; Zinser, Erik R. (February 2022, mBio)

   Martiny, Jennifer B. (Ed.)

   ABSTRACT The marine cyanobacterium Prochlorococcus numerically dominates the phytoplankton community of the nutrient-limited open ocean, establishing itself as the most abundant photosynthetic organism on Earth. This ecological success has been attributed to lower cell quotas for limiting nutrients, superior resource acquisition, and other advantages associated with cell size reduction and genome streamlining. In this study, we tested the prediction that Prochlorococcus outcompetes its rivals for scarce nutrients and that this advantage leads to its numerical success in nutrient-limited waters. Strains of Prochlorococcus and its sister genus Synechococcus grew well in both mono- and cocultures when nutrients were replete. However, in nitrogen-limited medium, Prochlorococcus outgrew Synechococcus but only when heterotrophic bacteria were also present. In the nitrogen-limited medium, the heterotroph Alteromonas macleodii outcompeted Synechococcus for nitrogen but only if stimulated by the exudate released by Prochlorococcus or if a proxy organic carbon source was provided. Genetic analysis of Alteromonas suggested that it outcompetes Synechococcus for nitrate and/or nitrite, during which cocultured Prochlorococcus grows on ammonia or other available nitrogen species. We propose that Prochlorococcus can stimulate antagonism between heterotrophic bacteria and potential phytoplankton competitors through a metabolic cross-feeding interaction, and this stimulation could contribute to the numerical success of Prochlorococcus in nutrient-limited regions of the ocean. IMPORTANCE In nutrient-poor habitats, competition for limited resources is thought to select for organisms with an enhanced ability to scavenge nutrients and utilize them efficiently. Such adaptations characterize the cyanobacterium Prochlorococcus , the most abundant photosynthetic organism in the nutrient-limited open ocean. In this study, the competitive superiority of Prochlorococcus over a rival cyanobacterium, Synechococcus , was captured in laboratory culture. Critically, this outcome was achieved only when key aspects of the open ocean were simulated: a limited supply of nitrogen and the presence of heterotrophic bacteria. The results indicate that Prochlorococcus promotes its numerical dominance over Synechococcus by energizing the heterotroph’s ability to outcompete Synechococcus for available nitrogen. This study demonstrates how interactions between trophic groups can influence interactions within trophic groups and how these interactions likely contribute to the success of the most abundant photosynthetic microorganism. 

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3. Growth and mortality of aerobic anoxygenic phototrophs in the North Pacific Subtropical Gyre

   https://doi.org/10.1128/aem.00032-24  

   Koblížek, Michal; Ferrera, Isabel; Kolářová, Eva; Duhamel, Solange; Popendorf, Kimberly J; Gasol, Josep M; Van_Mooy, Benjamin_A S (April 2024, Applied and Environmental Microbiology)

   Biddle, Jennifer F (Ed.)

   ABSTRACT Aerobic anoxygenic phototrophic (AAP) bacteria harvest light energy using bacteriochlorophyll-containing reaction centers to supplement their mostly heterotrophic metabolism. While their abundance and growth have been intensively studied in coastal environments, much less is known about their activity in oligotrophic open ocean regions. Therefore, we combinedin situsampling in the North Pacific Subtropical Gyre, north of O'ahu island, Hawaii, with two manipulation experiments. Infra-red epifluorescence microscopy documented that AAP bacteria represented approximately 2% of total bacteria in the euphotic zone with the maximum abundance in the upper 50 m. They conducted active photosynthetic electron transport with maximum rates up to 50 electrons per reaction center per second. Thein situdecline of bacteriochlorophyll concentration over the daylight period, an estimate of loss rates due to predation, indicated that the AAP bacteria in the upper 50 m of the water column turned over at rates of 0.75–0.90 d⁻¹. This corresponded well with the specific growth rate determined in dilution experiments where AAP bacteria grew at a rate 1.05 ± 0.09 d⁻¹. An amendment of inorganic nitrogen to obtain N:P = 32 resulted in a more than 10 times increase in AAP abundance over 6 days. The presented data document that AAP bacteria are an active part of the bacterioplankton community in the oligotrophic North Pacific Subtropical Gyre and that their growth was mostly controlled by nitrogen availability and grazing pressure.IMPORTANCEMarine bacteria represent a complex assembly of species with different physiology, metabolism, and substrate preferences. We focus on a specific functional group of marine bacteria called aerobic anoxygenic phototrophs. These photoheterotrophic organisms require organic carbon substrates for growth, but they can also supplement their metabolic needs with light energy captured by bacteriochlorophyll. These bacteria have been intensively studied in coastal regions, but rather less is known about their distribution, growth, and mortality in the oligotrophic open ocean. Therefore, we conducted a suite of measurements in the North Pacific Subtropical Gyre to determine the distribution of these organisms in the water column and their growth and mortality rates. A nutrient amendment experiment showed that aerobic anoxygenic phototrophs were limited by inorganic nitrogen. Despite this, they grew more rapidly than average heterotrophic bacteria, but their growth was balanced by intense grazing pressure. 

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4. Taxon-specific phytoplankton growth, nutrient utilization and light limitation in the oligotrophic Gulf of Mexico

   https://doi.org/10.1093/plankt/fbab028  

   Yingling, Natalia; Kelly, Thomas B; Shropshire, Taylor A; Landry, Michael R; Selph, Karen E; Knapp, Angela N; Kranz, Sven A; Stukel, Michael R (April 2021, Journal of Plankton Research)

   Abstract The highly stratified, oligotrophic regions of the oceans are predominantly nitrogen limited in the surface ocean and light limited at the deep chlorophyll maximum (DCM). Hence, determining light and nitrogen co-limitation patterns for diverse phytoplankton taxa is crucial to understanding marine primary production throughout the euphotic zone. During two cruises in the deep-water Gulf of Mexico, we measured primary productivity (H13CO3−), nitrate uptake (15NO3−) and ammonium uptake (15NH4+) throughout the water column. Primary productivity declined with depth from the mixed layer to the DCM, averaging 27.1 mmol C m−2 d−1. The fraction of growth supported by NO3− was consistently low, with upper euphotic zone values ranging from 0.01 to 0.14 and lower euphotic zone values ranging from 0.03 to 0.44. Nitrate uptake showed strong diel patterns (maximum during the day), whereas ammonium uptake exhibited no diel variability. To parameterize taxon-specific phytoplankton nutrient and light utilization, we used a data assimilation approach (Bayesian Markov Chain Monte Carlo) including primary productivity, nutrient uptake and taxon-specific growth rate measurements. Parameters derived from this analysis define distinct niches for five phytoplankton taxa (Prochlorococcus, Synechococcus, diatoms, dinoflagellates and prymnesiophytes) and may be useful for constraining biogeochemical models of oligotrophic open-ocean systems. 

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5. Inorganic and organic carbon and nitrogen uptake strategies of picoplankton groups in the northwestern Atlantic Ocean

   https://doi.org/10.1002/lno.11909  

   Berthelot, Hugo; Duhamel, Solange; L'Helguen, Stéphane; Maguer, Jean‐François; Cassar, Nicolas (August 2021, Limnology and Oceanography)

   Abstract Picoplankton populations dominate the planktonic community in the surface oligotrophic ocean. Yet, their strategies in the acquisition and the partitioning of organic and inorganic sources of nitrogen (N) and carbon (C) are poorly described. Here, we measured at the single‐cell level the uptake of dissolved inorganic C (C‐fixation), C‐leucine, N‐leucine, nitrate (NO₃⁻), ammonium (NH₄⁺), and N‐urea in pigmented and nonpigmented picoplankton groups at six low‐N stations in the northwestern Atlantic Ocean. Our study highlights important differences in trophic strategies betweenProchlorococcus,Synechococcus, photosynthetic pico‐eukaryotes, and nonpigmented prokaryotes. Nonpigmented prokaryotes were characterized by high leucine uptake rates, nonsignificant C‐fixation and relatively low NH₄⁺, N‐urea, and NO₃⁻uptake rates. Nonpigmented prokaryotes contributed to 7% ± 3%, 2% ± 2%, and 9% ± 5% of the NH₄⁺, NO₃⁻, and N‐urea community uptake, respectively. In contrast, pigmented groups displayed relatively high C‐fixation rates, NH₄⁺and N‐urea uptake rates, but lower leucine uptake rates than nonpigmented prokaryotes.Synechococcusand photosynthetic pico‐eukaryotes NO₃⁻uptake rates were higher thanProchlorococcusones. Pico‐sized pigmented groups accounted for a significant fraction of the community C‐fixation (63% ± 27%), NH₄⁺uptake (47% ± 27%), NO₃⁻uptake (62% ± 49%), and N‐urea uptake (81% ± 35%). Interestingly,Prochlorococcusand photosynthetic pico‐eukaryotes showed a greater reliance on C‐ and N‐leucine thanSynechococcuson average, suggesting a greater reliance on organic C and N sources. Taken together, our single‐cell results decipher the wide diversity of C and N trophic strategies between and within marine picoplankton groups, but a clear partitioning between pigmented and nonpigmented groups still remains. 

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