Single-cell measurements and modelling reveal substantial organic carbon acquisition by Prochlorococcus

Marine phytoplankton are responsible for about half of the photosynthesis on Earth. Many are mixotrophs, combining photosynthesis with heterotrophic assimilation of organic carbon, but the relative contribution of these two lifestyles is unclear. Here single-cell measurements reveal that Prochlorococcus at the base of the photic zone in the Eastern Mediterranean Sea obtain only ~20% of carbon required for growth by photosynthesis. This is supported by laboratory-calibrated calculations based on photo-physiology parameters and compared with in situ growth rates. Agent-based simulations show that mixotrophic cells could grow tens of metres deeper than obligate photo-autotrophs, deepening the nutricline by ~20 m. Time series from the North Atlantic and North Pacific indicate that, during thermal stratification, on average 8–10% of the Prochlorococcus cells live without enough light to sustain obligate photo-autotrophic populations. Together, these results suggest that mixotrophy underpins the ecological success of a large fraction of the global Prochlorococcus population and its collective genetic diversity.


March 2021
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Estimation of the amount of organic carbon taken up and utilized by Prochlorococcus, using a combination of field analyses and mathematical modeling. Field analysis included oceanographic measurements from the Eastern Mediterarnea, including flow cytometry, genetic and nanoSIMS analyses (detailed below) .
An oceanographic profile was taken during August 2017 from the Eastern Mediterranean (station N1200, 32.45°N, 34.37°E). Discrete samples from 11 depths were used for cell counts using flow cytometry and for genetic analyses of the picoplankton population structure by amplicon sequening of the ITS. An in-situ bottle incubation was performed using 13C-bicarbonate and 15N-ammonium. Prochlorococcus cells from two of the samples were FACS-sorted and isotopic enrichment was measured using nanoSIMS. The samples for nanoSIMS analysis were chosen based on their depth and (for the 115m sample) the presence of multiple Prochlorococcus populations.
Sampling was performed using Niskin bottles. Sample size (number of cells for nanoSIMS analysis) depended on the number of sorted cells available for nanoSIMS analysis (multiple fields, n=45-55 cells/sample). No sample size calculation was performed.
CTD data were collected on-board and analyzed post-hoc by DS. During the cruise, a log was maintained by DS and made available as a scanned pdf. Cruise log contains detailed description of time of sample collection for each depth, time to sample fixation, etc. Genetic data were obtained by DA as described in the materials and methods. FACS-sorting was performed by DA, DRR and TLK, nanoSIMS acquisition was performed by AV and cells were analyzed by DA, DRR, TLK with the assistance of AV, FE and MV. Modelling was performed by ZW and MJF, and reanalysis of published time series was performed by DS.
Sampling was performed on a single cruise on August 7th, 2017. All relevant data are rcorded in the manuscript. Sampling location was 32.45°N, 34.37°E.
No data were excluded from the analysis Multiple depths were analyzed to verify reproducibility of nanoSIMS measurements. Attempts for perform flow-sorting of cells from shallower depths were unsuccessful due to limit of sensitivity of FACS sorter. Results of oceanographic cruises (e.g. flow cytometry, ITS sequencing, nanoSIMS) represent a "snap-shot" of a single timepoint, but were consistent with other studies as described in the text.
Not relevant for this study (no distinct study groups).
Blinding was not relevant to the study during data acquisition. Analysis of nanoSIMS ROIs was performed blind to the sample.
Field work was performed during summer in the oligotrophic Eastern Mediterranean. The water column was stratified and nutriens were depleted. These information are included in the mansucript. Samples were collected on oceanographic cruise as per common practices. The location sampled is not protected (e.g. not a nature reserve), and no permits were required. Samples for nanoSIMS analysis were sent from Israel to Germany as fixed cells in accordance with all regulations.
The study resulted in no disturbance.