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 between
NanoSIMS single cell analyses reveal the contrasting nitrogen sources for small phytoplankton
Nitrogen (N) is a limiting nutrient in vast regions of the world’s oceans, yet the sources of N available to various phytoplankton groups remain poorly understood. In this study, we investigated inorganic carbon (C) fixation rates and nitrate (NO3−), ammonium (NH4+) and urea uptake rates at the single cell level in photosynthetic pico-eukaryotes (PPE) and the cyanobacteria Prochlorococcus and Synechococcus. To that end, we used dual 15N and 13C-labeled incubation assays coupled to flow cytometry cell sorting and nanoSIMS analysis on samples collected in the North Pacific Subtropical Gyre (NPSG) and in the California Current System (CCS). Based on these analyses, we found that photosynthetic growth rates (based on C fixation) of PPE were higher in the CCS than in the NSPG, while the opposite was observed for Prochlorococcus. Reduced forms of N (NH4+ and urea) accounted for the majority of N acquisition for all the groups studied. NO3− represented a reduced fraction of total N uptake in all groups but was higher in PPE (17.4 ± 11.2% on average) than in Prochlorococcus and Synechococcus (4.5 ± 6.5 and 2.9 ± 2.1% on average, respectively). This may in part explain the contrasting biogeography of these picoplankton groups. Moreover, single cell analyses reveal that cell-to-cell heterogeneity within picoplankton groups was significantly greater for NO3− uptake than for C fixation and NH4+ uptake. We hypothesize that cellular heterogeneity in NO3− uptake within groups facilitates adaptation to the fluctuating availability of NO3− in the environment.
more » « less- PAR ID:
- 10224579
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 13
- Issue:
- 3
- ISSN:
- 1751-7362
- Format(s):
- Medium: X Size: p. 651-662
- Size(s):
- p. 651-662
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Prochlorococcus ,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.Synechococcus and photosynthetic pico‐eukaryotes NO3−uptake rates were higher thanProchlorococcus ones. 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,Prochlorococcus and photosynthetic pico‐eukaryotes showed a greater reliance on C‐ and N‐leucine thanSynechococcus on 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. -
Johnson, Karyn N. (Ed.)ABSTRACT Coral reefs are possible sinks for microbes; however, the removal mechanisms at play are not well understood. Here, we characterize pelagic microbial groups at the CARMABI reef (Curaçao) and examine microbial consumption by three coral species: Madracis mirabilis , Porites astreoides , and Stephanocoenia intersepta . Flow cytometry analyses of water samples collected from a depth of 10 m identified 6 microbial groups: Prochlorococcus , three groups of Synechococcus , photosynthetic eukaryotes, and heterotrophic bacteria. Minimum growth rates (μ) for Prochlorococcus , all Synechococcus groups, and photosynthetic eukaryotes were 0.55, 0.29, and 0.45 μ day −1 , respectively, and suggest relatively high rates of productivity despite low nutrient conditions on the reef. During a series of 5-h incubations with reef corals performed just after sunset or prior to sunrise, reductions in the abundance of photosynthetic picoeukaryotes, Prochlorococcus and Synechococcus cells, were observed. Of the three Synechococcus groups, one decreased significantly during incubations with each coral and the other two only with M. mirabilis. Removal of carbon from the water column is based on coral consumption rates of phytoplankton and averaged between 138 ng h −1 and 387 ng h −1 , depending on the coral species. A lack of coral-dependent reduction in heterotrophic bacteria, differences in Synechococcus reductions, and diurnal variation in reductions of Synechococcus and Prochlorococcus , coinciding with peak cell division, point to selective feeding by corals. Our study indicates that bentho-pelagic coupling via selective grazing of microbial groups influences carbon flow and supports heterogeneity of microbial communities overlying coral reefs. IMPORTANCE We identify interactions between coral grazing behavior and the growth rates and cell abundances of pelagic microbial groups found surrounding a Caribbean reef. During incubation experiments with three reef corals, reductions in microbial cell abundance differed according to coral species and suggest specific coral or microbial mechanisms are at play. Peaks in removal rates of Prochlorococcus and Synechococcus cyanobacteria appear highest during postsunset incubations and coincide with microbial cell division. Grazing rates and effort vary across coral species and picoplankton groups, possibly influencing overall microbial composition and abundance over coral reefs. For reef corals, use of such a numerically abundant source of nutrition may be advantageous, especially under environmentally stressful conditions when symbioses with dinoflagellate algae break down.more » « less
-
Diatom–diazotroph associations (DDAs) are one of the most important symbiotic dinitrogen (N2) fixing groups in the oligotrophic ocean. Despite their capability to fix N2, ammonium (NH4+) remains a key nitrogen (N) source for DDAs, and the effect of NH4+ on their metabolism remains elusive. Here, we developed a coarse-grained, cellular model of the DDA with NH4+ uptake and quantified how the level of extracellular NH4+ influences metabolism and nutrient exchange within the symbiosis. The model shows that, under a fixed growth rate, an increased NH4+ concentration may lower the required level of N2 fixation and photosynthesis, and decrease carbon (C) and N exchange. A low-NH4+ environment leads to more C and N in nutrient exchange and more fixed N2 to support a higher growth rate. With higher growth rates, nutrient exchange and metabolism increased. Our study shows a strong effect of NH4+ on metabolic processes within DDAs, and thus highlights the importance of in situ measurement of NH4+ concentrations.more » « less
-
Marine phytoplankton play a central role in global biogeochemical cycling, carbon export, and the overall functioning of marine ecosystems. While chlorophyll a (Chl a ) is widely used as a proxy for phytoplankton biomass, identifying the proportion of Chl a attributable to different phytoplankton groups remains a major challenge in oceanography, especially for the picophytoplankton groups that often represent the majority of phytoplankton biomass in the open ocean. We describe a method for measuring picophytoplankton per-cell Chl a in field samples using fluorescence-activated cell sorting followed by solvent-based Chl a extraction and fluorescence quantification. Applying this method to surface samples from the Gulf of Mexico, we determined per-cell Chl a to be 0.24 ± 0.07, 0.6 ± 0.33, and 26.36 ± 20.9 fg Chl a cell -1 for Prochlorococcus , Synechococcus , and PPE, respectively (mean ± SD). Measurements of per-cell Chl a using this method are precise to within 1.7, 2.1, and 3.1% for Prochlorococcus , Synechococcus , and PPE, respectively. We demonstrate that this approach can be used to obtain estimates of group-specific Chl a for Prochlorococcus , Synechococcus , and picophytoeukaryotes, the latter two of which cannot be captured by existing methods. We also demonstrate that measurements of per-cell Chl a made using this method in field samples are sufficiently precise to capture relationships between per-cell Chl a and cytometer red fluorescence, providing a bridge between biomass estimates from cell counts and bulk measurements of total Chl a .more » « less
-
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.more » « less
