In oligotrophic waters, dissolved organic carbon (DOC) is mostly produced in the surface layers by phytoplankton and remineralized by heterotrophic prokaryotes throughout the water column. DOC surface excess is subducted and exported to deeper layers where a semi-labile fraction is further processed contributing to oxygen consumption. How this cycling of DOC occurs in the Red Sea, one of the warmest oligotrophic marine basins, is virtually unknown. We examined DOC vertical and seasonal variability in a mesopelagic station (ca. 700 m depth) of the central Red Sea performing monthly profile samplings over a two-year period. Together with DOC vertical and seasonal distribution we evaluated the interaction with heterotrophic prokaryotes and contribution to oxygen respiration. DOC values ranged from 41.4 to 95.4 µmol C L−1, with concentrations in the epipelagic (70.0 ± 7.5 µmol C L−1) 40% higher on average than in the mesopelagic (50.7 ± 4.1 µmol C L−1). Subduction of seasonally accumulated semi-labile DOC was estimated to be responsible for ∼20% of the oxygen consumption mostly occurring at the low epipelagic-upper mesopelagic boundary layer. Variability in mesopelagic waters was higher than expected (ca. 20 µmol C L−1) evidencing a more active realm than previously thought, with consequences for carbon sequestration.

The ecological status of an ecosystem can be approached by the taxa present but also by the size of individual organisms. In aquatic ecosystems, flow cytometry (FC) allows to study the individual size spectra and broad community composition through the evaluation of cytometric categories. The Red Sea represents a warm oligotrophic environment with a strong diel signal of vertically migrating mesopelagic fish, which feed at night at the surface and release dissolved organic carbon (DOC) at depth during day-time. However, knowledge about how these conditions affect the dynamics of heterotrophic prokaryotes (HP) and their coupling with DOC is lacking. Here, we analyzed a high frequency sampling over 24 h to identify the community structure and compositional changes of HP in the epipelagic and mesopelagic layers of the central Red Sea. Our results show marked vertical and diel changes in HP communities in both layers. Specifically, the relative contribution of high nucleic acid content cells was remarkably linked to changes in DOC concentration and properties. The patterns observed were likely associated to the diel vertical migration of mesopelagic fish. These findings reveal that the structure of microbial communities in warm oligotrophic environments may be more dynamic than previously thought.

The Red Sea is characterized by higher temperatures and salinities than other oligotrophic tropical regions. Here, we investigated the vertical and seasonal variations in the abundance and biomass of autotrophic and heterotrophic picoplankton. Using flow cytometry, we consistently observed five groups of autotrophs (Prochlorococcus, two populations of Synechococcus separated by their relative phycoerythrin fluorescence, low (LF-Syn) and high (HF-Syn), and two differently-sized groups of picoeukaryotes, small (Speuk) and large (Lpeuk)) and two groups of heterotrophic prokaryotes of low and high nucleic acid content (LNA and HNA, respectively). Samples were collected in 15 surveys conducted from 2015 to 2017 at a 700-m depth station in the central Red Sea. Surface temperature ranged from 24.6 to 32.6 °C with a constant value of 21.7 °C below 200 m. Integrated (0–100 m) chlorophyll a concentrations were low, with maximum values in fall (24.0 ± 2.7 mg m−2) and minima in spring and summer (16.1 ± 1.9 and 1.1 mg m−2, respectively). Picoplankton abundance was generally lower than in other tropical environments. Vertical distributions differed for each group, with Synechococcus and LNA prokaryotes more abundant at the surface while Prochlorococcus, picoeukaryotes and HNA prokaryotes peaked at the deep chlorophyll maximum, located between 40 and 76 m. Surface to 100 m depth-weighted abundances exhibited clear seasonal patterns for Prochlorococcus, with maxima in summer (7.83 × 104 cells mL−1, July 2015) and minima in winter (1.39 × 104 cells mL−1, January 2015). LF-Syn (0.32 – 2.70 × 104 cells mL−1 ), HF-Syn (1.11 – 3.20 × 104 cells mL−1) and Speuk (0.99 – 4.81 × 102 cells mL−1) showed an inverse pattern to Prochlorococcus, while Lpeuk (0.16 – 7.05 × 104 cells mL−1) peaked in fall. Synechococcus unexpectedly outnumbered Prochlorococcus in winter and at the end of fall. The seasonality of heterotrophic prokaryotes (2.29 – 4.21×105 cells mL−1 ) was less noticeable than autotrophic picoplankton. The contribution of HNA cells was generally low in the upper layers, ranging from 36% in late spring and early summer to ca. 50% in winter and fall. Autotrophs dominated integrated picoplankton biomass in the upper 100 m, with 1.4-fold higher values in summer than in winter (mean 387 and 272 mg C m–2, respectively). However, when the whole water column was considered, the biomass of heterotrophic prokaryotes exceeded that of autotrophic picoplankton with an average of 411 mg C m–2. Despite being located in tropical waters, our results show that the picoplankton community seasonal differences in the central Red Sea are not fundamentally different from higher latitude regions.

Phytoplankton biomass and size structure are recognized as key ecological indicators. With the aim to quantify the relationship between these two ecological indicators in tropical waters and understand controlling factors, we analyzed the total chlorophyll-a concentration, a measure of phytoplankton biomass, and its partitioning into three size classes of phytoplankton, using a series of observations collected at coastal sites in the central Red Sea. Over a period of 4 years, measurements of flow cytometry, size-fractionated chlorophyll-a concentration, and physical-chemical variables were collected near Thuwal in Saudi Arabia. We fitted a three-component model to the size-fractionated chlorophyll-a data to quantify the relationship between total chlorophyll and that in three size classes of phytoplankton [pico- (<2 μm), nano- (2–20 μm) and micro-phytoplankton (>20 μm)]. The model has an advantage over other more empirical methods in that its parameters are interpretable, expressed as the maximum chlorophyll-a concentration of small phytoplankton (pico- and combined pico-nanophytoplankton, Cpm and Cp,nm, respectively) and the fractional contribution of these two size classes to total chlorophyll-a as it tends to zero (Dp and Dp,n). Residuals between the model and the data (model minus data) were compared with a range of other environmental variables available in the dataset. Residuals in pico- and combined pico-nanophytoplankton fractions of total chlorophyll-a were significantly correlated with water temperature (positively) and picoeukaryote cell number (negatively). We conducted a running fit of the model with increasing temperature and found a negative relationship between temperature and parameters Cpm and Cp,nm and a positive relationship between temperature and parameters Dp and Dp,n. By harnessing the relative red fluorescence of the flow cytometric data, we show that picoeukaryotes, which are higher in cell number in winter (cold) than summer (warm), contain higher chlorophyll per cell than other picophytoplankton and are slightly larger in size, possibly explaining the temperature shift in model parameters, though further evidence is needed to substantiate this finding. Our results emphasize the importance of knowing the water temperature and taxonomic composition of phytoplankton within each size class when understanding their relative contribution to total chlorophyll. Furthermore, our results have implications for the development of algorithms for inferring size-fractionated chlorophyll from satellite data, and for how the partitioning of total chlorophyll into the three size classes may change in a future ocean.

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