High temperature and solar radiation in the Red Sea enhance the dissolution of crude oil from surface films.

The Red Sea is a hotspot of biodiversity susceptible to oil pollution. Besides, it is one of the warmest seas on the Earth with highly transparent waters. In this study, we estimated the oil dissolution rates under natural sunlight spectra and temperature conditions using coastal oil slicks collected after the 2019 Sabiti oil spill in the Red Sea. Optical analyses revealed the significant interactive effect of sunlight and temperature in enhancing the dissolution of oil into dissolved organic matter (DOM). The highest oil dissolution rate (38.68 g C m-3 d-1) was observed in full-spectrum sunlight. Oil dissolution significantly enhanced total organic carbon (TOC) and polycyclic aromatic hydrocarbons (PAHs) in seawater. High nucleic acid (HNA) bacteria, likely the oil degraders, proliferated from 30 to 70 - 90% after 4 days. The heavier stable carbon isotopic composition of methane (δ13C-CH4) and lighter stable carbon isotopic composition of carbon dioxide (δ13C-CO2) indicate the putative role of bacterial processes in the natural degradation of crude oil. The results indicated that the combined effect of temperature and solar radiation enhanced the biological and photochemical dissolution of oil on the Red Sea surface.

Tracking the early signals of crude oil in seawater and plankton after a major oil spill in the Red Sea.

Understanding the immediate impacts of oil spills is essential to recognizing their long-term consequences on the marine environment. In this study, we traced the early (within one week) signals of crude oil in seawater and plankton after a major oil spill in October 2019 in the Red Sea. At the time of sampling, the plume had moved eastward, but we detected significant signs of incorporation of oil carbon into the dissolved organic carbon pool, resulting in a 10-20% increase in the ultraviolet (UV) absorption coefficient (a254) of chromophoric dissolved organic matter (CDOM), elevated oil fluorescence emissions, and depletion of the carbon isotope composition (δ13C) of the seawater. The abundance of the picophytoplankton Synechococcus was not affected, but the proportion of low nucleic acid (LNA) bacteria was significantly higher. Moreover, specific bacterial genera (Alcanivorax, Salinisphaera, and Oleibacter) were enriched in the seawater microbiome. Metagenome-assembled genomes (MAGs) suggested that such bacteria presented pathways for growing on oil hydrocarbons. Traces of polycyclic aromatic hydrocarbons (PAHs) were also detected in zooplankton tissues, revealing the rapid entry of oil pollutants into the pelagic food web. Our study emphasizes the early signs of short-lived spills as an important aspect of the prediction of long-term impacts of marine oil spills.

Contrasting sensitivity among oligotrophic marine microbial communities to priority PAHs.

Oligotrophic areas represent a large proportion of the oceans, wherein microbial food webs largely determine carbon flux dynamics and biogeochemical cycles. However, little is known regarding the sensitivity of microbial planktonic communities to pollutants in such areas. Organic pollutants such as polycyclic aromatic hydrocarbons (PAH/s) are toxic oil derivatives that occur as complex mixtures and reach marine environments through different sources. Therefore, our study analyzed the PAH tolerance of natural photosynthetic and heterotrophic bacteria and eukaryotes from the oligotrophic Red Sea, which is uniquely susceptible to high oil contamination. Natural communities sampled from the surface layer were exposed to a concentration gradient of a mixture of 16 priority PAHs at in situ conditions for 48 h. The populations of the dominant picocyanobacteria Synechococcus sp., picophytoeukaryotes, and low nucleic acid (LNA) bacteria decreased upon exposure to PAHs in a strong dose-dependent manner. Chlorophyll-a, which was measured as an indicator of the total autotrophic community response, also decreased substantially. High nucleic acid (HNA) bacteria, however, exhibited lower growth inhibition (<50%). The lethal concentration (LC10) thresholds to the 16-PAH mixture demonstrated contrasting sensitivities among the microbial communities studied increasing from picoeukaryotes (5.98 ± 2.08 µg L-1) < chlorophyll-a (19.51 ± 8.11 µg L-1) < LNA bacteria (23.63 ± 10.64 µg L-1) < Synechococcus sp. (26.77 ± 13.34 µg L-1) < HNA bacteria (97.13 ± 17.28 µg L-1). The sensitivity of Red Sea Synechococcus and picophytoeukaryotes to the 16-PAH mixture was between 2 and 6.5 times higher compared to single PAH compounds tested previously. However, some populations of HNA bacteria and Synechococcus sp., were highly tolerant, suggesting an adaptation to chronic pollution. Concerningly, the LC10 toxicity thresholds approached the ambient PAH concentrations in the Red Sea, suggesting that environmental oil pollution actively shapes the microbial community structures in the region.

Food-chain length determines the level of phenanthrene bioaccumulation in corals.

Exposure from the dissolved-phase and through food-chains contributes to bioaccumulation of polycyclic aromatic hydrocarbons (PAHs) in organisms such as fishes and copepods. However, very few studies have investigated the accumulation of PAHs in corals. Information on dietary uptake contribution to PAHs accumulation in corals is especially limited. Here, we used Cavity-Ring-Down Spectroscopy (CRDS) to investigate the uptake rates and accumulation of a 13C-labeled PAH, phenanthrene, in Acropora millepora corals over 14 days. Our experiment involved three treatments representing exposure levels of increasing food-chain length. In Level W, corals were exposed to 13C-phenanthrene directly dissolved in seawater. In Level 1 representing herbivory, Dunaliella salina microalgal culture pre-exposed to 13C-phenanthrene for 48 h was added to the coral treatment jars. In Level 2 representing predation, corals were provided a diet of copepod (Parvocalanus crassirostris) nauplii fed on D. salina pre-exposed to 13C-phenanthrene. Bioconcentration factors (BCF) and bioaccumulation factors (BAF) were calculated as appropriate for all organisms, and biomagnification factors (BMF) were calculated for A. millepora. We found that while phenanthrene uptake rates were not significantly different for the treatments, the accumulated concentration in corals was significantly higher in Level W (33.5 ± 2.83 mg kg-1) than in Level 1 (27.55 ± 2.77 mg kg-1) and Level 2 (29.36 ± 3.84 mg kg-1). Coral log BAF values increased with food-chain length; Level 2 log BAF (6.45) was higher than Level W log BCF (4.18) and Level 1 log BAF (4.5). Coral BMF was also higher for Level 2 than for Level 1. Exposure to dissolved or diet-bound phenanthrene had no significant effect on the coral symbionts' photosynthetic efficiency (Fv/Fm) as monitored by pulse-amplitude-modulation (PAM) fluorometry, indicating the PAH can be accumulated without toxic effects to their Photosystem II. Our study highlights the critical role of dietary exposure for pollutant accumulation in corals.

Accumulation of 13C-labelled phenanthrene in phytoplankton and transfer to corals resolved using cavity ring-down spectroscopy.

Polycyclic aromatic hydrocarbons (PAHs) are widespread pollutants in marine ecosystems including threatened and potentially sensitive coral reefs. Lower organisms such as phytoplankton, known to bioconcentrate PAHs, could serve as potential entry points for these chemicals into higher trophic levels. Here, we present a novel method using a 13C-labelled PAH and cavity ring-down spectroscopy (CRDS) to investigate accumulation, uptake rates and trophic transfer of PAHs in corals, which are key organisms to sustain biodiversity in tropical seas. We quantified the accumulation of 13C-phenanthrene in the marine microalga Dunaliella salina, and in the coral Acropora millepora after diffusive uptake from seawater or dietary uptake via labelled D. salina. Additionally, we monitored the photophysiological health of D. salina and A. millepora during phenanthrene exposure by pulse-amplitude modulation (PAM) fluorometry. Dose-dependent accumulation of 13C-phenanthrene in the microalga showed a mean bioconcentration factor (BCF) of 2590 ± 787 L kg-1 dry weight. Corals accumulated phenanthrene from both exposure routes. While uptake of 13C-phenanthrene in corals was faster through aqueous exposure than dietary exposure, passive diffusion showed larger variability between individuals and both routes resulted in accumulation of similar concentrations of phenanthrene. The 13C-PAH labelling and analysis by CRDS proved to be a highly sensitive method. The use of stable isotopic label eliminated additional toxicity and risks by radioactive isotopic-labelling, and CRDS reduced the analytical complexity of PAH (less biomass, no extraction, fast analysis). The simultaneous, precise quantification of both carbon content and 13C/12C ratio (δ13C) enabled accurate determination of 13C-phenanthrene accumulation and uptake rate. This is the first study to provide empirical evidence for accumulation of phenanthrene in a phytoplankton-coral food chain.

Accelerated burial of petroleum hydrocarbons in Arabian Gulf blue carbon repositories.

Massive consumption of petroleum since the past century has led to considerable emissions into marine ecosystems. Marine sediments may accumulate substantial quantities of petroleum and associated contaminants in oil-producing areas. Here, we report accelerated accumulation of total petroleum hydrocarbons (TPH) in 'blue carbon' vegetated ecosystems of the Arabian Gulf - the world's most important region for oil production. In addition to increased accumulation with the onset of oil exploitation, sediment records reflect a large depositional event associated with the 1991 Gulf War, with the magnitude of these maxima varying across habitats, depending on their elevation along the shoreline. Blue carbon ecosystems of the Arabian Gulf currently bury about 2300 megagrams (Mg) of TPHs annually and have accumulated TPH stocks of 59,799 Mg over the past 25 years alone. Massive burial and sequestration of TPH by blue carbon ecosystems is an important, but thus far unrecognized, removal mechanism in the Arabian Gulf. Conserving these ecosystems is important to avoid possible remobilization of sequestered TPH into the surrounding environment.

Assessing the effects of iron enrichment across holobiont compartments reveals reduced microbial nitrogen fixation in the Red Sea coral Pocillopora verrucosa.

The productivity of coral reefs in oligotrophic tropical waters is sustained by an efficient uptake and recycling of nutrients. In reef-building corals, the engineers of these ecosystems, this nutrient recycling is facilitated by a constant exchange of nutrients between the animal host and endosymbiotic photosynthetic dinoflagellates (zooxanthellae), bacteria, and other microbes. Due to the complex interactions in this so-called coral holobiont, it has proven difficult to understand the environmental limitations of productivity in corals. Among others, the micronutrient iron has been proposed to limit primary productivity due to its essential role in photosynthesis and bacterial processes. Here, we tested the effect of iron enrichment on the physiology of the coral Pocillopora verrucosa from the central Red Sea during a 12-day experiment. Contrary to previous reports, we did not see an increase in zooxanthellae population density or gross photosynthesis. Conversely, respiration rates were significantly increased, and microbial nitrogen fixation was significantly decreased. Taken together, our data suggest that iron is not a limiting factor of primary productivity in Red Sea corals. Rather, increased metabolic demands in response to iron enrichment, as evidenced by increased respiration rates, may reduce carbon (i.e., energy) availability in the coral holobiont, resulting in reduced microbial nitrogen fixation. This decrease in nitrogen supply in turn may exacerbate the limitation of other nutrients, creating a negative feedback loop. Thereby, our results highlight that the effects of iron enrichment appear to be strongly dependent on local environmental conditions and ultimately may depend on the availability of other nutrients.