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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Production and cross-feeding of nitrite within Prochlorococcus populations
ABSTRACT Prochlorococcusis an abundant photosynthetic bacterium in the open ocean, where nitrogen (N) often limits phytoplankton growth. In the low-light-adapted LLI clade ofProchlorococcus, nearly all cells can assimilate nitrite (NO2−), with a subset capable of assimilating nitrate (NO3−). LLI cells are maximally abundant near the primary NO2−maximum layer, an oceanographic feature that may, in part, be due to incomplete assimilatory NO3−reduction and subsequent NO2−release by phytoplankton. We hypothesized that someProchlorococcusexhibit incomplete assimilatory NO3−reduction and examined NO2−accumulation in cultures of threeProchlorococcusstrains (MIT0915, MIT0917, and SB) and twoSynechococcusstrains (WH8102 and WH7803). Only MIT0917 and SB accumulated external NO2−during growth on NO3−. Approximately 20–30% of the NO3−transported into the cell by MIT0917 was released as NO2−, with the rest assimilated into biomass. We further observed that co-cultures using NO3−as the sole N source could be established for MIT0917 andProchlorococcusstrain MIT1214 that can assimilate NO2−but not NO3−. In these co-cultures, the NO2−released by MIT0917 is efficiently consumed by its partner strain, MIT1214. Our findings highlight the potential for emergent metabolic partnerships that are mediated by the production and consumption of N cycle intermediates withinProchlorococcuspopulations. IMPORTANCEEarth’s biogeochemical cycles are substantially driven by microorganisms and their interactions. Given that N often limits marine photosynthesis, we investigated the potential for N cross-feeding within populations ofProchlorococcus, the numerically dominant photosynthetic cell in the subtropical open ocean. In laboratory cultures, someProchlorococcuscells release extracellular NO2−during growth on NO3−. In the wild,Prochlorococcuspopulations are composed of multiple functional types, including those that cannot use NO3−but can still assimilate NO2−. We show that metabolic dependencies arise whenProchlorococcusstrains with complementary NO2−production and consumption phenotypes are grown together on NO3−. These findings demonstrate the potential for emergent metabolic partnerships, possibly modulating ocean nutrient gradients, that are mediated by cross-feeding of N cycle intermediates.
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- PAR ID:
- 10492689
- Editor(s):
- Dubilier, Nicole
- Publisher / Repository:
- American Society for Microbiology
- Date Published:
- Journal Name:
- mBio
- ISSN:
- 2150-7511
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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