Seasonality of top-down control of bacterioplankton at two central Red Sea sites with different trophic status.

The role of bottom-up (nutrient availability) and top-down (grazers and viruses mortality) controls on tropical bacterioplankton have been rarely investigated simultaneously from a seasonal perspective. We have assessed them through monthly samplings over 2 years in inshore and offshore waters of the central Red Sea differing in trophic status. Flow cytometric analysis allowed us to distinguish five groups of heterotrophic bacteria based on physiological properties (nucleic acid content, membrane integrity and active respiration), three groups of cyanobacteria (two populations of Synechococcus and Prochlorococcus), heterotrophic nanoflagellates (HNFs) and three groups of viruses based on nucleic acid content. The dynamics of bacterioplankton and their top-down controls varied with season and location, being more pronounced in inshore waters. HNFs abundances showed a strong preference for larger prey inshore (r = -0.62 to -0.59, p = 0.001-0.002). Positive relationships between viruses and heterotrophic bacterioplankton abundances were more marked inshore (r = 0.67, p < 0.001) than offshore (r = 0.44, p = 0.03). The negative correlation between HNFs and viruses abundances (r = -0.47, p = 0.02) in shallow waters indicates a persistent seasonal switch between protistan grazing and viral lysis that maintains the low bacterioplankton stocks in the central Red Sea area.

Growth dynamics and transcriptional responses of a Red Sea Prochlorococcus strain to varying temperatures.

Prochlorococcus play a crucial role in the ocean's biogeochemical cycling, but it remains controversial how they will respond to global warming. Here we assessed the response to temperature (22-30°C) of the growth dynamics and gene expression profiles of a Red Sea Prochlorococcus strain (RSP50) in a non-axenic culture. Both the specific growth rate (0.55-0.80 day-1 ) and cell size (0.04-0.07 µm3 ) of Prochlorococcus increased significantly with temperature. The primary production released extracellularly ranged from 20% to 34%, with humic-like fluorescent compounds increasing up to fivefold as Prochlorococcus reached its maximum abundance. At 30°C, genes involved in carbon fixation such as CsoS2 and CsoS3 and photosynthetic electron transport including PTOX were downregulated, suggesting a cellular homeostasis and energy saving mechanism response. In contrast, PTOX was found upregulated at 22°C and 24°C. Similar results were found for transaldolase, related to carbon metabolism, and citrate synthase, an important enzyme in the TCA cycle. Our data suggest that in spite of the currently warm temperatures of the Red Sea, Prochlorococcus can modulate its gene expression profiles to permit growth at temperatures lower than its optimum temperature (28°C) but is unable to cope with temperatures exceeding 30°C.

Single chamber Mg/Ca analyses of Globigerinoides ruber for paleo-proxy calibration using femtosecond LA-ICP-MS.

Mg/Ca is an independent proxy in paleoceanography to reconstruct past seawater temperature. Femtosecond Laser Ablation Inductively Coupled Plasma Mass Spectrometry (fs-LA-ICP-MS) was employed to determine the Mg/Ca composition of tests (shells) of the planktic foraminifer species Globigerinoides ruber albus (white chromotype) and G. ruber ruber (red/pink chromotype) sampled alive from the temperate to subtropical eastern North Atlantic with the research sailing yacht Eugen Seibold. Mg/Ca data are compared to (i) the measured in-situ temperature of ambient seawater, (ii) average mixed layer temperature, and (iii) sea surface temperature (SST). The pooled mean chamber Mg/Ca from each plankton tow site exhibits a positive relationship with SST. Two chamber-specific calibrations are derived, which are consistent with previous calibration equations for comparable paleo-archives. The results confirm fs-LA-ICP-MS as reliable method for determining Mg/Ca in G. ruber, and both the penultimate and antepenultimate chambers of adult specimens may provide comprehensible Mg/Ca temperatures of the surface ocean.

Diel dynamics of dissolved organic matter and heterotrophic prokaryotes reveal enhanced growth at the ocean's mesopelagic fish layer during daytime.

Contrary to epipelagic waters, where biogeochemical processes closely follow the light and dark periods, little is known about diel cycles in the ocean's mesopelagic realm. Here, we monitored the dynamics of dissolved organic matter (DOM) and planktonic heterotrophic prokaryotes every 2 h for one day at 0 and 550 m (a depth occupied by vertically migrating fishes during light hours) in oligotrophic waters of the central Red Sea. We additionally performed predator-free seawater incubations of samples collected from the same site both at midnight and at noon. Comparable in situ variability in microbial biomass and dissolved organic carbon concentration suggests a diel supply of fresh DOM in both layers. The presence of fishes in the mesopelagic zone during daytime likely promoted a sustained, longer growth of larger prokaryotic cells. The specific growth rates were consistently higher in the noon experiments from both depths (surface: 0.34 vs. 0.18 d-1, mesopelagic: 0.16 vs. 0.09 d-1). Heterotrophic prokaryotes in the mesopelagic layer were also more efficient at converting extant DOM into new biomass. These results suggest that the ocean's twilight zone receives a consistent diurnal supply of labile DOM from the diel vertical migration of fishes, enabling an unexpectedly active community of heterotrophic prokaryotes.

Localized effects of offshore aquaculture on water quality in a tropical sea.

Aquaculture production has increased steadily in many tropical countries over the past few decades, although impact assessments have been frequently neglected. We investigated the impacts of an offshore barramundi fish farm on water quality in the southern-central Red Sea, a traditionally understudied tropical, oligotrophic, and semi-enclosed basin. Inorganic nutrients, particulate matter, chlorophyll-a, and heterotrophic bacteria were measured periodically over 8 months around the farm. Water down-current from the farm had, on average, more heterotrophic bacteria and chlorophyll-a than up-current (11% and 34% higher, respectively). Ratios of dissolved inorganic nitrogen:phosphorus down-current from the farm were lower than ratios up-current (mean 9.8 vs 16.0, respectively). Phosphate, inorganic nitrogen, and particulate matter showed patterns of enrichment associated with the farm after a fish feeding event. Strategies such as feed optimization and considering hydrodynamics in site selection may improve water quality for future fish farms in Saudi Arabia and other tropical countries.

Heterotrophic bacterioplankton responses in coral- and algae-dominated Red Sea reefs show they might benefit from future regime shift.

In coral reefs, dissolved organic matter (DOM) cycling is a critical process for sustaining ecosystem functioning. However, global and local stressors have caused persistent shifts from coral- to algae-dominated benthic communities. The influence of such phase shifts on DOM nature and its utilization by heterotrophic bacterioplankton remains poorly studied. Every second month for one year, we retrieved seawater samples enriched in DOM produced by coral- and algae-dominated benthic communities in a central Red Sea reef during a full annual cycle. Seawater incubations were conducted in the laboratory under in situ temperature and light conditions by inoculating enriched DOM samples with bacterial assemblages collected in the surrounding waters. Dissolved organic carbon (DOC) concentrations were higher in the warmer months (May-September) in both communities, resulting in higher specific growth rates and bacterial growth efficiencies (BGE). However, these high summer values were significantly enhanced in algal-DOM relative to coral-DOM, suggesting the potential for bacterioplankton biomass increase in reefs with algae replacing healthy coral cover under warmer conditions. The potential exacerbation of heterotrophic bacterial activity in the ongoing widespread regime shift from coral- to algae-dominated communities may have detrimental consequences for the overall health of tropical coral reefs.

Heterotrophic Bacterioplankton Growth and Physiological Properties in Red Sea Tropical Shallow Ecosystems With Different Dissolved Organic Matter Sources.

Despite the key role of heterotrophic bacterioplankton in the biogeochemistry of tropical coastal waters, their dynamics have been poorly investigated in relation to the different dissolved organic matter (DOM) pools usually available. In this study we conducted four seasonal incubations of unfiltered and predator-free seawater (Community and Filtered treatment, respectively) at three Red Sea coastal sites characterized by different dominant DOM sources: Seagrass, Mangrove, and Phytoplankton. Bacterial abundance, growth and physiological status were assessed by flow cytometry and community composition by 16S rRNA gene amplicons. The Seagrass site showed the highest initial abundances (6.93 ± 0.30 × 105 cells mL-1), coincident with maximum DOC concentrations (>100 µmol C L-1), while growth rates peaked at the Mangrove site (1.11 ± 0.09 d-1) and were consistently higher in the Filtered treatment. The ratio between the Filtered and Community maximum bacterial abundance (a proxy for top-down control by protistan grazers) showed minimum values at the Seagrass site (1.05 ± 0.05) and maximum at the Phytoplankton site (1.24 ± 0.30), suggesting protistan grazing was higher in open waters, especially in the first half of the year. Since the Mangrove and Seagrass sites shared a similar bacterial diversity, the unexpected lack of bacterial response to predators removal at the latter site should be explained by differences in DOM characteristics. Nitrogen-rich DOM and fluorescent protein-like components were significantly associated with enhanced specific growth rates along the inshore-offshore gradient. Our study confirms the hypotheses that top-down factors control bacterial standing stocks while specific growth rates are bottom-up controlled in representative Red Sea shallow, oligotrophic ecosystems.

Fine-scale metabolic discontinuity in a stratified prokaryote microbiome of a Red Sea deep halocline.

Deep-sea hypersaline anoxic basins are polyextreme environments in the ocean's interior characterized by the high density of brines that prevents mixing with the overlaying seawater, generating sharp chemoclines and redoxclines up to tens of meters thick that host a high concentration of microbial communities. Yet, a fundamental understanding of how such pycnoclines shape microbial life and the associated biogeochemical processes at a fine scale, remains elusive. Here, we applied high-precision sampling of the brine-seawater transition interface in the Suakin Deep, located at 2770 m in the central Red Sea, to reveal previously undocumented fine-scale community structuring and succession of metabolic groups along a salinity gradient only 1 m thick. Metagenomic profiling at a 10-cm-scale resolution highlighted spatial organization of key metabolic pathways and corresponding microbial functional units, emphasizing the prominent role and significance of salinity and oxygen in shaping their ecology. Nitrogen cycling processes are especially affected by the redoxcline with ammonia oxidation processes being taxa and layers specific, highlighting also the presence of novel microorganisms, such as novel Thaumarchaeota and anammox, adapted to the changing conditions of the chemocline. The findings render the transition zone as a critical niche for nitrogen cycling, with complementary metabolic networks, in turn underscoring the biogeochemical complexity of deep-sea brines.

Nutrient pollution enhances productivity and framework dissolution in algae- but not in coral-dominated reef communities.

Ecosystem services provided by coral reefs may be susceptible to the combined effects of benthic species shifts and anthropogenic nutrient pollution, but related field studies are scarce. We thus investigated in situ how dissolved inorganic nutrient enrichment, maintained for two months, affected community-wide biogeochemical functions of intact coral- and degraded algae-dominated reef patches in the central Red Sea. Results from benthic chamber incubations revealed 87% increased gross productivity and a shift from net calcification to dissolution in algae-dominated communities after nutrient enrichment, but the same processes were unaffected by nutrients in neighboring coral communities. Both community types changed from net dissolved organic nitrogen sinks to sources, but the increase in net release was 56% higher in algae-dominated communities. Nutrient pollution may, thus, amplify the effects of community shifts on key ecosystem services of coral reefs, possibly leading to a loss of structurally complex habitats with carbonate dissolution and altered nutrient recycling.

High summer temperatures amplify functional differences between coral- and algae-dominated reef communities.

Shifts from coral to algal dominance are expected to increase in tropical coral reefs as a result of anthropogenic disturbances. The consequences for key ecosystem functions such as primary productivity, calcification, and nutrient recycling are poorly understood, particularly under changing environmental conditions. We used a novel in situ incubation approach to compare functions of coral- and algae-dominated communities in the central Red Sea bimonthly over an entire year. In situ gross and net community primary productivity, calcification, dissolved organic carbon fluxes, dissolved inorganic nitrogen fluxes, and their respective activation energies were quantified to describe the effects of seasonal changes. Overall, coral-dominated communities exhibited 30% lower net productivity and 10 times higher calcification than algae-dominated communities. Estimated activation energies indicated a higher thermal sensitivity of coral-dominated communities. In these communities, net productivity and calcification were negatively correlated with temperature (>40% and >65% reduction, respectively, with +5°C increase from winter to summer), whereas carbon losses via respiration and dissolved organic carbon release more than doubled at higher temperatures. In contrast, algae-dominated communities doubled net productivity in summer, while calcification and dissolved organic carbon fluxes were unaffected. These results suggest pronounced changes in community functioning associated with coral-algal phase shifts. Algae-dominated communities may outcompete coral-dominated communities because of their higher productivity and carbon retention to support fast biomass accumulation while compromising the formation of important reef framework structures. Higher temperatures likely amplify these functional differences, indicating a high vulnerability of ecosystem functions of coral-dominated communities to temperatures even below coral bleaching thresholds. Our results suggest that ocean warming may not only cause but also amplify coral-algal phase shifts in coral reefs.

Seasonal variability and vertical distribution of autotrophic and heterotrophic picoplankton in the Central Red Sea.

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.

Dissolved organic carbon contribution to oxygen respiration in the central Red Sea.

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.

Factors Regulating the Relationship Between Total and Size-Fractionated Chlorophyll-a in Coastal Waters of the Red Sea.

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, C p m and C p , n m , respectively) and the fractional contribution of these two size classes to total chlorophyll-a as it tends to zero (D p and D p,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 C p m and C p , n m and a positive relationship between temperature and parameters D p and D p,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.

Major hydrogeochemical processes in an acid mine drainage affected estuary.

This study provides geochemical data with the aim of identifying and quantifying the main processes occurring in an Acid Mine Drainage (AMD) affected estuary. With that purpose, water samples of the Huelva estuary were collected during a tidal half-cycle and ion-ion plots and geochemical modeling were performed to obtain a general conceptual model. Modeling results indicated that the main processes responsible for the hydrochemical evolution of the waters are: (i) the mixing of acid fluvial water with alkaline ocean water; (ii) precipitation of Fe oxyhydroxysulfates (schwertmannite) and hydroxides (ferrihydrite); (iii) precipitation of Al hydroxysulfates (jurbanite) and hydroxides (amorphous Al(OH)3); (iv) dissolution of calcite; and (v) dissolution of gypsum. All these processes, thermodynamically feasible in the light of their calculated saturation states, were quantified by mass-balance calculations and validated by reaction-path calculations. In addition, sorption processes were deduced by the non-conservative behavior of some elements (e.g., Cu and Zn).