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Review

Cyanoremediation of Polluted Seawater in the Arabian Gulf: Risks and Benefits to Human Health

1
Department of Biological and Environmental Sciences, College of Arts and Sciences, Qatar University, Doha P.O. Box 2713, Qatar
2
Independent Researcher, 8 James Court, Dunstable Road, Luton LU4 0HN, UK
*
Author to whom correspondence should be addressed.
Processes 2024, 12(12), 2733; https://doi.org/10.3390/pr12122733
Submission received: 3 November 2024 / Revised: 19 November 2024 / Accepted: 28 November 2024 / Published: 2 December 2024
(This article belongs to the Section Sustainable Processes)

Abstract

:
Cyanobacteria play a crucial role in marine ecosystems as primary producers of food and oxygen for various organisms while helping remove waste and toxic substances from the environment. They are essential to the carbon cycle and help regulate the climate. These marine autotrophs also aid in the absorption of essential elements and support diverse life forms. They help degrade organic compounds, including petroleum hydrocarbons as well as heavy metals. Fluctuations in cyanobacteria populations can indicate ecosystem health, influencing both human well-being and wildlife. Their significance also extends to potential technological advancements, thus providing valuable resources for fields such as pharmacology, medicine, health care, biofuels, cosmetics, and bioremediation. However, some species produce toxins that pose risks to human health and marine organisms. Consequently, cyanobacteria are a major focus of research aimed at preserving and improving marine ecosystems—especially given the environmental damage caused by past and potential future conflicts. This review highlights their roles in cyanoremediation and other industrial and biotechnological applications with a particular focus on the Arabian Gulf region.

Graphical Abstract

1. Introduction

Plankton are living organisms found in the sea and other large bodies of water drifting with the currents. They are generally divided into two main groups: phytoplankton and zooplankton. Phytoplankton includes a variety of organisms such as cyanobacteria (blue–green algae), microscopic green algae (Chlorophyta), diatoms, dinoflagellates, coccolithophores, and cryptophytes. In contrast, zooplankton are heterotrophic and consist of small crustaceans, protozoans, other microscopic organisms, and the larval stages of larger animals like fish and jellyfish. Phytoplankton are photosynthetic, and thus, they are typically found in the upper layers of marine and freshwater environments. However, only a few studies have examined phytoplankton diversity along the coastal waters and pools of the Rawdahs in Qatar. Cyanobacteria inhabit a wide range of aquatic environments, including freshwater pools, brackish water, sewage from human activities, and seawater in the Arabian Gulf [1,2,3,4]. Certain cyanobacteria genera such as Anabaena, Anacystis, Lyngbya, Oscillatoria, and Spirulina-can indicate environmental quality, especially in polluted areas. This article focuses primarily on cyanobacteria and explores their roles in remediating petroleum hydrocarbons, heavy metals, nitrogen fixation, industrial biotechnological applications, health issues, and their contributions to bloom formation.

1.1. Roles of Phytoplankton in Marine and Freshwater Ecosystems

The roles of these autotrophs have been well-documented in many studies, reports, and monographs as follows:
First, phytoplankton are primary producers and perform photosynthesis to generate organic matter. During this process, CO₂, water, and nutrients are converted into carbohydrates, oxygen (O₂), and other essential organic compounds. These compounds serve as the primary food source for most zooplankton, which in turn supports higher trophic levels, including fish, mammals, and other heterotrophs [5,6]. The oxygen produced by phytoplankton is also crucial for sustaining life, not only in seawater but also globally [7].
Second, phytoplankton help maintain the global carbon cycle; CO₂ is absorbed by marine autotrophs to synthesize organic matter, which becomes embedded in the ocean floor after these organisms die. This process helps maintain the carbon balance and regulate the global climate [8].
Third, phytoplankton are involved in nutrient cycling in the marine environment. Phytoplankton absorb essential elements such as nitrogen and phosphorus, which become part of their biomass. This biomass is then consumed by heterotrophic organisms. After these organisms die, the nutrients are released back into the seawater and become available for other marine life [9].
Fourth, these organisms are a good source of food for a variety of marine heterotrophic organisms such as zooplankton, small fish, and even large whales. Therefore, the health of phytoplankton has a direct effect on these organisms and the overall productivity of the marine ecosystem [10,11].
Fifth, these phytoplankton influence climate change by producing chemicals such as dimethyl sulfide, which lead to the formation of clouds. These clouds can reduce the amount of sunlight reaching the surface of seawater, affecting temperature and climate patterns [12].
Sixth, phytoplankton are adapted to a variety of environmental conditions, and thus, they can support diverse marine ecosystems and enhance their resilience [13,14,15].
Seventh, these marine autotrophs might be used as indicators of environmental conditions. Many factors can affect phytoplankton, such as temperature, light, nutrients, and pollution. Thus, changes in phytoplankton populations might be a consequence of changes in environmental conditions. Therefore, shifts in phytoplankton populations can be considered indicators of the health of the ecosystem [5,16].
Eighth, phytoplankton are sources of useful compounds used in medicine and pharmacology. Recent findings revealed that phytoplankton are sources of bioactive substances and secondary metabolites, including toxins, which can be valuable to pharmaceutical, nutraceutical, and biotechnological industries [17].

1.2. Disadvantages of Phytoplankton

Despite their roles in maintaining the marine ecosystem and sustaining marine life, phytoplankton face numerous threats and can sometimes have negative impacts on the ecosystem. While phytoplankton provide many benefits, such as producing oxygen and serving as a primary food source, they can also have negative effects, i.e., harmful algal blooms. In fact, phytoplankton might have negative impacts under certain environmental conditions. For example, some algae, such as dinoflagellates and cyanobacteria, can proliferate and lead to harmful blooms. These blooms produce toxins that are harmful to marine life, humans, and other marine animals, such as fish and shellfish [18,19]. Oxygen depletion can also occur when dead phytoplankton decompose—this process consumes significant amounts of oxygen. As a result, oxygen levels in seawater can become very low (hypoxia), thus creating ‘dead zones’ where there is insufficient oxygen to sustain fish, shellfish, corals, and other aquatic organisms [20,21,22]. The dense presence of phytoplankton in the sea can also affect water quality and clarity, thus potentially impacting other photoautotrophs such as seagrasses and seaweeds. These organisms may decrease water transparency, which in turn affects the penetration of visible light that supports photosynthesis and ultimately influences the growth of marine autotrophs [23]. This ultimately decreases marine biodiversity [24,25]. Furthermore, the presence of phytoplankton in seawater, oceans, and other bodies of water can either mitigate climate change or exacerbate its effects depending on variations in temperature, salinity, and other environmental factors [26]. While the positive roles of phytoplankton have been discussed above, their negative impacts can result from temperature changes that disrupt the recycling of nutrients from deep water to the surface. The greenhouse effect might negatively impact phytoplankton productivity, partly due to the increase in sea surface temperature. A decline in phytoplankton can lead to higher levels of CO2 in the atmosphere, thus exacerbating the greenhouse effect and worsening climate change. In contrast, an overabundance of phytoplankton can cause blooms that reduce sunlight and oxygen penetration in the water, thus disrupting aquatic ecosystems [27].
The impact of phytoplankton on the economy and human life is another negative factor that requires attention. Harmful algal blooms can adversely affect fisheries and water treatment facilities—particularly in countries that rely on seawater for their livelihoods, such as the Arab countries in the Arabian Gulf region. For example, toxins produced by certain phytoplankton species can cause the closure of shellfish beds, thus leading to economic losses. Furthermore, the Arabian Gulf States have recently initiated programs to store water in strategic reservoirs for use during crises and emergencies. Allowing phytoplankton to thrive could compromise seawater desalination and the treatment of industrial wastewater [28] because these phytoplankton might negatively impact desalination [4,28,29,30]. The Government of Qatar has started a precautionary program that stores water in strategic reservoirs for use during crises and emergencies [28].

2. Methods and Mechanisms of Phycoremediation

Phytoplankton, including cyanobacteria, can remediate seawater from pollutants, e.g., heavy metals and organic components such as petroleum hydrocarbons [31,32,33]. The following are the most common methods and mechanisms reported for phycoremediation:
First, extracellular polymeric substances (EPSs) are high-molecular-weight natural polymers secreted by various microorganisms, including microalgae. These polymers are produced through the metabolic activity of complex biological communities known as biofilms, which form protective layers around these microorganisms [34]. EPSs, along with biofilms, play a crucial role in enhancing the resilience of native plants and crops by providing protection against environmental stresses, including drought and salt stress [35,36]. EPS can degrade persistent organic pollutants via complexation [37].
Second, extracellular biosorption is the ability of biological materials to accumulate heavy metals from wastewater through metabolic and/or non-metabolic pathways or as a property of certain types of inactive microbial materials [38].
Third, intracellular bioaccumulation is a metabolic mechanism in which intracellular accumulation of metalloids such as antimony, arsenic, boron, and silicon occurs through passive or active transport channels across plasma membranes using metabolic energy [39,40].
Fourth, compartmentalization refers to the separation of the cell’s protoplast into distinct compartments, which contain compounds or heavy metals that could potentially damage the cell’s active machinery. This separation helps protect the cell by isolating harmful substances and preventing their negative effects. Algal cells may use a similar method to avoid the harmful impacts of heavy metals or toxic organic compounds. Some algae species may compartmentalize heavy metals from the cytoplasm into vacuoles and cell walls. Certain transporters at the plasma membrane regulate the movement of heavy metals and facilitate their transport into vacuoles, thus preventing them from interfering with key cellular components such as chloroplasts, mitochondria, and the nucleus. This mechanism is an important strategy for reducing environmental stress, including petroleum hydrocarbons and heavy metals [41,42].
Fifth, biomethylation occurs in living organisms when a methyl group is attached to one or two heavy atoms through a carbon atom. This process refers to the formation of volatile and non-volatile methylated compounds of metals and metalloids [43].
Sixth, enzymatic reduction can be employed by various living organisms, such as microalgae, to mitigate negative impacts on human health [32]. Notably, some organic compounds produced or used during industrial processes may have toxic, carcinogenic, or mutagenic effects. Several methods, such as membrane filtration, ion exchange, photochemical oxidation, and nanotechnological approaches, can be used to address these concerns. Living organisms, including microalgae, may play a role in enzymatic processes through the action of enzymes like reductases [44].
Seventh, volatilization is the process of converting a chemical substance from a solid or liquid state into a gaseous or vapor state. Yan et al. [45] briefly discussed this mechanism and noted that many plants can convert elements such as arsenic (As), mercury (Hg), sulfur (S), and selenium (Se) into gaseous forms and release them into the air through transpiration. Phytoplankton, including microalgae, can also carry out this mechanism [46,47]. During the last five years, studies have suggested that some Qatari native plants can volatilize these elements from polluted soils because these elements are very common in the industrial wastewater of gas activities [4,48,49]. Figure S1 illustrates some roles and functions performed by cyanobacteria, which they may share with other phytoplankton.

3. Biodiversity and Functions of Cyanobacteria Under Pollution Stress

Qatar and other countries bordering the Arabian Gulf (also known as the Gulf) have faced frequent oil spills since the 1980s, with incidents occurring during three major regional conflicts (1980–1988, 1990–1991, and 2003). These events resulted in the release of petroleum hydrocarbons and heavy metals, as well as the burning of oil wells and tankers, which caused large quantities of oil to disperse into international waters and accumulate along the shores. This pollution has significantly harmed wildlife and posed serious public health risks [30]. Notably, reports in the 1980s by United Nations organizations and other studies highlighted the contamination of edible marine organisms, such as shrimp, in Qatari seawater during the period between 1968 and 1995. Following the 2003 war, the region experienced a major transformation in the energy sector, with Qatar emerging as a leading gas producer. This growth brought significant industrial and urban expansion across the Gulf region. While these developments have provided substantial benefits to the local population, the associated negative environmental impacts were unavoidable. These consequences require ongoing monitoring and the implementation of radical solutions to mitigate risks to both human health and wildlife (Table 1, [50]) [4,49].
The Gulf is a semi-enclosed sea bordered by eight countries: Iran, the United Arab Emirates, the Kingdom of Saudi Arabia, Qatar, Kuwait, Iraq, Oman, and the Kingdom of Bahrain (Figure 1). Six species of benthic algae were first reported in the mid-19th century, with additional reports in the 20th century and beyond, including those by John and Al-Thani [51]. Notably, data from many studies [4,52,53,54] using general morphology, microscopic examinations, and modern techniques revealed 17 cyanobacteria (blue-green algae) genera.
Further discussions will explore the potential roles of these genera in the phycoremediation of oil and gas components as well as other pollutants resulting from anthropogenic activities. The monograph by Rizk et al. [53] reported only two cyanobacteria genera with four species in the Arabian Gulf near the Qatari peninsula: Calothrix spp., and Oscillatoria spp. However, in 1986, Dorgham and Al-Muftah [52] identified 11 species, and the current number of cyanobacteria species recorded in the seawaters around Qatar has since increased to 26 species. This rise is attributed to the identification of additional species in seawater, brackish water pools, and industrial wastewater of anthropogenic origin. The increase was noted in studies by Al-Khelaifi [54] and Al-Khelaifi et al. [55], as shown in Table 1.
Table 1. Cyanobacteria species found at the coastal line of the Qatari peninsula, features, and roles.
Table 1. Cyanobacteria species found at the coastal line of the Qatari peninsula, features, and roles.
SpeciesFamilyFeaturesRolesReferences
Amphanizomenon sp.AphanizomenonaceaeUnicellular organisms that consolidate into linear (non-branching) chains called trichomes. Inhabits freshwater lakes and can cause dense blooms.Fixes nitrogen, remediates petroleum hydrocarbons, produces anticancer agents, and develops blooms; produces toxic metabolites such as hepatotoxins, neurotoxins, and cytotoxins.[56,57,58]
Anabaena spp. (2 species)NostocaceaeFound in all types of water, including rivers, streams, lakes, and ponds; filamentous, cylindrical, barrel-shaped, or spherical.Fixes nitrogen, remediate crude oil. Water extracts have anticancer activity against breast cancer. Forms symbiotic relationships with some plants; produces neurotoxins; forms blooms.[59,60,61]
Calothrix spp.
(3 species)
RivulariaceaeFound in marine, fresh waters, and terrestrial environments; grow in high-salinity conditions, and form relationships with the roots of plants like rice, tomato, and wheat. Form a black, slick surface on rocks and mud and produce a gelatinous outer layer to prevent drying.Fixes nitrogen, possible remediation of industrial wastewater. Calothrixins are produced; used to cure many diseases including cytotoxicity in cancer; Aplysiatoxins might be produced that cause serious health issues including various dermatitis and promoting tumors.[62,63]
Chroococcus sp.ChroococcaceaeUnicellular ovoid or rod-shaped organisms, irregular to roughly spherical, forming colonies with gelatinous texture, found in water reserves.Uses large amounts of atmospheric CO2 for photosynthesis; produces O2. These were some of the first organisms to use water as asource of electrons and hydrogens for photosynthesis which enables the evolution of other organisms. Remediation of polluted water and soil is very possible; do not fix nitrogen and might produce anticancer agents. [64,65,66]
Croococcidiopsis sp.ChroococcidiopsidaceaeUnicellular with survival in extreme environments; salinity and desiccation, high antioxidant, develop thick mucilage envelopes.Fixes nitrogen, it resists very extreme environments (e.g., endurance to a Mars-like environment), phycoremedes wastewater and contaminated soil, might be used as food and oxygen producers in space, Mars, for example.[67,68,69]
Dermocarpella sp.DermocarpellaceaeGram-negative, thickened ovoid aggregate uniquely exhibits polarity; motile baeocytes result from multiple fission of apical cells; undergo binary and multiple fission.Needs to be tested for nitrogen fixation; might have toxic impact on the ecosystem. Possible role in phycoremediation.[54,70,71]
Euhalothece sp.CyanobacteriaceaeUnicellular, halophilic, not pathogenic, and not known to produce toxins. High concentration of mycosporine-like amino acids, carotenoid-binding proteins, and C-phycocyanin subunits.Needs to be tested for nitrogen fixation; primary producer in hypersaline environments; strong antioxidant and some oxidant compounds protect its cellular machinery from UV-induced oxidative stress; it has β-car. and Zea-dependent ROS scavenging systems to help cells cope with salt stress, helps in biotechnology applications; possible role in phycoremediation.[71,72]
Geitlerinema sp.ColeofasciculaceaeFilamentous, thin, delicate thallus, bright blue–green, violet, or brown; has motile trichomes, active oxygenic and anoxygenic, rich in proteins and phycobiliproteins, contains polyphosphates, starch, and carboxysomes.Fixes nitrogen, oxygenic, and anoxygenic photosynthetic capabilities, biomass feedstock, produces biofuels, produces pro-inflammatory cytokines and adhesion molecules, develops glucocorticoid-resistant asthma, increases the phagocytic ability of monocytes, possible role in phycoremediation.[71,73,74]
Geminocystis sp.GeminocystaceaeSmall, spherical cells, found in colonies, photosynthetically adapted to aquatic environments, can be found in freshwater ecosystems.Needs to be tested for nitrogen fixation and can adjust the wavelengths of light they absorb by remodeling photosynthetic antennae—possible role in phycoremediation.[72,75]
Lyngbya sp.OscillatoriaceaeFilamentous, non-branched or pseudo-branched; macroscopic layered or stratified and brownish-colored sheaths; musty or foul odor, cell division occurs crosswise with reproduction by hormogonium formation; found in high alkaline water.Fixes nitrogen, a rich source of marine natural products; produces extracellular sunscreen scytonemin, indole alkaloid, source of food for some grass carp, forming blooms, possible remediation of heavy metals, and petroleum hydrocarbons. [76,77]
Leptolyngbya sp.LyptolyngbyaceaeFilamentous cells divide by symmetrical crosswise binary fission, produce hormogonia, tolerate severe environmental conditions, have antioxidant activity, scavenge free radicals, act as an iron-chelating agent; applications in food and pharmaceuticals; high in lipids.Some species fix nitrogen, phycoremediation of contaminated of water and soil, and phycoremediation petroleum hydrocarbons. [78,79,80]
Merismopedia sp. MicrocystaceaeFound in fresh and salt water, ovoid or spherical, arranged in rows and flats, forming rectangular colonies held together by a mucilaginous matrix; non-nitrogen-fixing bacteria.Not fixing nitrogen; remediation efficiency needs to be tested; produces lipopolysaccharides; can cause skin irritation and gastrointestinal distress.[81]
Microcystis wesenbergiiMicrocystaceaeSingle cell; cells are small (a few micrometers in diameter) and spherical or hemispherical; cells are light blue–green in color, but appear brown or dark due to the presence of gas-filled vesicles; forms colonies surrounded by a thick mucilage; colonies begin spherical but become irregular over time.Does not fix nitrogen; possible pollution remediation; freshwater forms harmful bloom and hepatotoxins such as microcystin and cyanopeptolin; communities are often a mix of toxin-producing and nonproducing isolates; scum formation with pollution. [6,82,83]
Nodularia spumigeraAphanizomenonaceaeForm solitary filaments or groups of filaments; unipolar, straight, or curved; yellowish, olive green, or blue–green in color; reproduced by the formation of hormogonia, filament breakage, akinetes, salinity, and temperature stress reduce toxin production.Fixes nitrogen and forms blooms; can be toxic to ecosystems and water quality; possible remediation of pollutants produces nodularin (liver toxin) and beta-methylamino L-alanine (nerve toxin), stress might affect toxin production.[80,84,85]
Nostoc linekiaNostocaceaeCylindrical, barrel-shaped, or spherical, thick cell wall; peptidoglycan, various pigments (chlorophyll, phycocyanin, and phycoerythrin); found in a variety of environments, grows symbiotically with plants providing nitrogen.Fixes nitrogen and remediates petroleum hydrocarbons.[81,86,87]
Oscillatoria spp. (3 species)OscillatoriaceaeFilamentous; form bright blue–green mats; motile with a slow rhythmic oscillation motion. Fixes nitrogen, remediates sewage wastewater and crude oil polluted water; heavy metals are eliminated.[81,88,89,90]
Phormidium sp. OscillatoriaceaeHas curved trichomes and unbranched filaments; cells divide crosswise perpendicular to the long axis of the trichome; cells are isodiametric; cells of the filament with rounded or pointed apical cells.Fixes nitrogen, remediates petroleum hydrocarbons and heavy metals.[91]
Richelia sp. NostocaceaeFilamentous trichomes; heterocystous associated within the cell membrane and cell wall of diatoms; exist as an epiphyte and an endophyte.Fixes nitrogen, possible remediation of industrial wastewater. [92,93]
Stanieria sp. DermocarpellaceaeCoccoid sessile on shells or epiphytic on algae and other cyanobacteria, coccoid microfossils, PTB-microbialite, and Permian Triassic. Boundary: calcified sheaths of the extant unicellular endospores are used for identification; anoxia is favorable to the preservation of Stanieria as fossils.Needs to be tested for nitrogen fixation, potential bioremediation of petroleum hydrocarbons.[94,95,96]
Synechococcus sp. SynechococcaceaeUnicellular, spherical, ellipsoidal, rod-shaped, marine environments and fresh water; motile without flagellates; it moves by oscillating its cell surface and grows in a wide range of light intensities; prefers neutral to slightly alkaline pH; contains phycoerthrin, cell wall is peptidoglycan and polysaccharides; can tolerate long periods without nutrient supply.Some species fix nitrogen; remediates petroleum hydrocarbons such as kerosene and other oil and gas compounds.[80,97]
Trichodesmium erythraeumMicrocoleaceaeFound in tropical and subtropical oceans; straight or curved individual filaments form spherical aggregates and large blooms; the red pigments responsible for the color of the red sea. Fixes nitrogen and carbon while undergoing photosynthesis; the close physical contact between genetically identical cells allows cell specialization; and metabolizes some organic compounds and related components.[98,99,100,101]
Table 1 and the discussion above show the advantages and disadvantages of each. Al-Khelaifi [54] provided a better understanding of cyanobacterial biodiversity along the Qatari coastline using modern techniques. The main species reported include Croococcidiopsis sp. (25.0%), Dermocarpella sp. (3.6%), Euhalothece sp. (7.1%), Geitlerinem sp. (21.4%), Geminocystis sp. (7.1%), Leptolyngbya sp. (3.6%), Oscillatoria sp. (3.6%), Stanieria sp. (10.7%), and Synechococcus sp. (10.7%). The study also incorporated genotypic analysis to assess local diversity, thus providing a consistent reference for future comparative studies, biotechnological applications, and monitoring efforts. These species comprised about 93% of the total cyanobacteria identified in the seawater of the Arabian Gulf near Qatar, as well as in pools of brackish water and industrial anthropogenic wastewater. These species play significant roles in the aquatic ecosystem, thus engaging in a variety of activities that can be classified into two main types: (a) positive activities and (b) negative activities. Both types of activities include the following.

3.1. Nitrogen Fixation

This is a light-regulated process that involves the reduction of atmospheric nitrogen into ammonia facilitated by the nitrogenase enzyme complex (E) found in specialized cells called heterocysts. The reactions catalyzed by nitrogenase require ATP as a source of metabolic energy.
N 2 + 12 A T P + 6 e + 8 H + E   2 N H 4 + + + 12 A D P + 12 P i
These microorganisms can metabolize ammonium to produce amino acids, amides, and other nitrogenous compounds [102]. Two enzyme systems operate in cyanobacteria: glutamine synthetase (GS) and glutamate synthase or glutamine oxoglutarate aminotransferase (GOGAT) system. The first one synthesizes glutamine from glutamate and NH4, while the second one synthesizes glutamate from glutamine:
G l u t a m a t e + N H 4 G S   G l u t a m i n e
Glutamine is converted to glutamate through a process called deamination, which is catalyzed by phosphate-activated glutaminase. This reaction produces NH4.
G l u t a m i n e G O G A T   G l u t a m a t e + N H 4
Other groups of enzymes are found in cyanobacteria that involve NH3 in ammonia assimilation, such as alanine dehydrogenase, asparagine synthetase, aspartate dehydrogenase, and aspartase [103,104]. Additionally, heterocysts import carbohydrates from nearby vegetative cells along the filaments, which serve as a source of energy and reductants for nitrogen fixation. Notably, carbohydrate metabolism in heterocysts involves the oxidative pentose phosphate pathway to generate NADPH, which is necessary for the biosynthesis of nucleic acids, proteins, and other essential compounds [105]. To protect nitrogenase from oxygen inactivation, heterocysts create a microoxic environment (an environment with low oxygen levels). They achieve this by producing additional cell walls and extra polysaccharides that limit air diffusion. Furthermore, they upregulate heterocyst-specific respiratory enzymes and degrade photosystem II (the system responsible for oxygen production); their thylakoids are structurally different from those in vegetative cells [106].
Importantly, the number of heterocysts increases under nitrogen starvation conditions because they are more active in anaerobic environments where they fix atmospheric nitrogen. This is supported by studies on cyanobacteria found in the Qatari sabkhas, where the soil is nitrogen-deficient [107,108,109]. Furthermore, polluted soils—particularly those contaminated with petroleum hydrocarbons and heavy metals—may also experience similar conditions of nitrogen deficiency [110]. Substantial evidence has been presented to support the argument that high concentrations of petroleum hydrocarbons increase the C:N ratio in soil and water, thus leading microorganisms such as cyanobacteria to activate the formation of heterocysts to enhance nitrogen fixation [111].

3.2. Cyanoremediation of Oil and Gas Components

Many cyanobacteria species can utilize crude oil as a source of carbon and energy [59,112]. This capability has been discussed in numerous studies, which outline the metabolic pathways involved in the breakdown of petroleum hydrocarbons by various organisms, including bacteria, cyanobacteria, and algae [28,76]. The complete degradation of these compounds leads to the formation of useful metabolites such as acetyl Co-A and fumaric acid. These species participate in the Krebs cycle, fatty acid biosynthesis, and amino acid interconversions [4,30,90]. As discussed in these reports, the degradation of organic compounds occurs during various industrial activities related to oil, gas, and other anthropogenic processes. The following are some examples (Figure 2 and Figure 3) of these processes performed in microorganisms, including cyanobacteria.
The above processes offer degradation of organic petroleum hydrocarbons. However, in some cases, microorganisms or plants might not be able to complete the degradation of organic compounds, which makes some of these compounds less toxic, as reported by Sandermann [113], who demonstrated the transformation of organochlorine pesticides and the hydroxylation of 2,4-D is followed by conjugation with glucose and malonyl residues and subsequent deposition in vacuoles [28].
Another example was reported by Ohtsubo et al. [114] and Van Aken [115], who explained the degradation of polychlorinated biphenyls (PCBs), which results in useful metabolites like succinyl Co-A or acetyl Co-A. Other metabolites are less toxic and can be sequestered in the vacuoles to keep the metabolic machinery safe for plants and the adjacent and/or associated microorganisms [4]. These reactions are crucial in metabolic pathways because they convert toxic compounds into beneficial metabolites. Importantly, these reactions along with the phycoremediation and cyanoremediation of petroleum hydrocarbons and heavy metals—are important from two key perspectives: positive potential and possible negative impacts [30,49]. On the positive side, this process can degrade organic petroleum hydrocarbons, thus preventing these harmful substances from entering the food chain [80]. However, there are significant challenges to consider. Some cyanobacteria species, while metabolizing petroleum hydrocarbons and removing heavy metals, may also accumulate these toxic metals within their cells. This accumulation could pose risks to ecosystems and wildlife because incomplete detoxification of petroleum hydrocarbons might lead to harmful side effects [4]. Additionally, many species of cyanobacteria are consumed by fish and other marine living organisms. If these organisms accumulate heavy metals or toxic compounds then it could seriously disrupt the food chain, thus leading to broader ecological consequences [116]. Early studies also indicated that some autotrophic organisms can absorb pollutants, thus unintentionally introducing some toxic metals and other organic components into the food web [28,117,118,119]. This highlights the challenge of ensuring that heavy metals and other toxic substances are prevented from entering the food chain because this could harm the ecosystem and threaten human health.
One promising species for mitigating this issue is Lyngbya sp., which has shown potential for removing heavy metals and breaking down the organic compounds found in crude oil and gas [76,77]. However, careful action and monitoring are required when employing cyanobacteria and other phytoplankton in industrial processes. It is essential to extract and contain these toxic substances, thus preventing them from re-entering the ecosystem. Methods such as bio-cycling and agro-botanical recycling could help manage the biomass of these organisms and ensure their safe use without disrupting ecosystems [49]. Integrating phytoplankton into projects designed to address pollution from industrial wastewater and oil and gas spills is a promising biological strategy. Success in this approach relies on effective monitoring systems and recycling processes driven by advances in biotechnology. Such systems would help limit the harmful effects of toxic substances produced by energy-related activities. By adopting innovative technologies, we can reduce environmental damage, improve the sustainability of energy production, and enhance waste management practices. Other species of cyanobacteria should be tested to explore the possibility of using them in large-scale projects aimed at protecting the marine environment in the Gulf region. A major challenge in the Gulf is the limited availability of freshwater for agriculture and domestic use due to the absence of natural freshwater sources such as rivers, lakes, or springs. Al-Thani and Yasseen [4] suggested industrial wastewater be an alternative water source in the future, given the ongoing production of oil and gas, political instability, accidents, and military exercises. Substantial efforts have been made to construct strategic reservoirs and desalination plants to meet the population’s needs during emergencies [28,30,120].

3.3. Source of Industrial Biotechnological and Health Applications

The search for novel compounds extracted from cyanobacteria has gained significant attention due to their potential in healthcare [121,122], biofuels [123], cosmetics [124], bioremediation [86], etc. Notably, these extracts have demonstrated a range of bioactive properties such as anti-inflammatory, anticancer [122], antibacterial, antiparasitic, antidiabetic, antiviral, antioxidant, anti-aging, and anti-obesity. This makes them promising candidates for drug development.
Considerable progress has been made with several compounds demonstrating notable antitumor activity. Of these, calothrixin and its derivatives have shown promise in cancer treatment [95,125]. Of note, more than 50% of cultivated cyanobacteria are used to extract bioactive compounds with properties that can treat various serious health issues [60]. Recent findings by Bouyahya et al. [126] revealed that various phytochemicals exhibit significant anticancer effects, e.g., secondary metabolites such as flavonoids, phenolic acids, terpenoids, and tannins. Specific compounds with proven anticancer efficacy, such as lyngbyastatin, curacin A, kalkitoxin, and cryptophycin, have been identified in cyanobacterial extracts from numerous species. However, petroleum hydrocarbon pollution in seawater may negatively impact the ability of cyanobacteria to produce bioactive chemicals, including those with anticancer properties. Limited information and research are available on this topic. Further investigation is needed to clarify the impact of extreme environmental conditions, such as exposure to crude oil, gas, and heavy metals, on the efficacy of cyanobacteria in producing anticancer compounds [127]. More details can be found in recent publications regarding the roles of these phytoplankton to treat disease [17,126,128].

3.4. Bloom Formation

Blooms in water bodies such as lakes, rivers, or oceans refer to large populations of microalgae such as diatoms, dinoflagellates, and cyanobacteria that cause the water to appear colored, e.g., red or brown (Figure 4). These blooms often have septic or musty odors and can make the water look murky, discolored, or covered in scum.
Such algal blooms can produce toxins such as toxic secondary metabolites that affect animals and humans; children are especially at risk [129]. Hu [130] found that the common freshwater cyanobacteria Microcystis rapidly proliferates to form heavy algal blooms on the water surface, especially under severe environmental conditions like pollution. Notably, the massive Microcystis blooms not only destroy ecosystems but can also deteriorate the water quality to produce toxins threatening public health. Furthermore, these blooms might be seen in the oceans and seas and/or under polluted conditions of water bodies. For example, Teikari et al. [131] found that toxic Nodularia spumigena thrived under high salinity in the Baltic Sea. Over decades of wars, military exercises, and accidents during crude oil transport, the Gulf has been under serious anthropogenic disturbances that ended in a substantial increase in the cyanobacteria and dinoflagellates that produce toxins from these blooms and kill marine organisms, potentially impacting the food chain [132]. Al-Muftah et al. [133] reported seven toxic components produced by these microalgae, including paralytic shellfish toxins (PSTs), diarrhetic shellfish toxins (DST), amnesic shellfish toxins (AST), cyclic imines (CIs), and polyether-lactone toxins. These toxins cause harmful effects on human health and marine animals [134], including fish (Figure 5).
Cyanobacterial blooms can significantly harm humans, animals, and ecosystems [135]. These negative impacts include the production of cyanotoxins, which can lead to various health issues such as skin rashes, eye irritation, vomiting, diarrhea, fever, and chronic diseases (such as cancer). Blooms also negatively affect water quality, thus threatening aquatic organisms. Climate change may also exacerbate anthropogenic eutrophication in water bodies worldwide, thus further contributing to these harmful effects. However, cyanobacterial blooms may offer certain positive aspects. For instance, Hassanshahian et al. [136] reported a significant number of microorganisms, including cyanobacteria, isolated from blooms of many genera, such as Phormidium spp., Oscillatoria spp., Aphanothece sp., Dactylococcopsis sp., and some strains of Halothece and Synechocystis. Such blooms can degrade petroleum hydrocarbons like n-alkanes. Moreover, Hamouda et al. [80] found that the blue–green alga Synechococcus sp., along with its consortium, can grow and degrade hydrocarbons such as kerosene. Zeng et al. [137] discussed methods for removing cyanobacteria from polluted water bodies and highlighted the advantages and disadvantages of mitigating large-scale water bodies, including seawater. They reported that while physical methods can be effective, they tend to be expensive. Biological methods, though effective for long-term control, may be slow and unsuitable for responding to sudden blooms such as those that occurred following wars in the Arabian Gulf. Although chemical methods work more quickly, they can cause secondary negative impacts, such as killing non-target organisms and contributing to secondary pollution.

4. Bioactive Compounds in the Arabian Gulf

Approximately 71% of the Earth’s surface is covered by water—most of which is saline. These marine environments contain largely untapped natural resources that can be exploited to obtain novel compounds with bioactive properties. Recent studies have shown that cyanobacteria and other microalgae produce numerous biologically active compounds that have potential applications in various fields, including biotechnology, pharmacology, cosmetology, and biofuels [122]. These studies highlight the diverse properties of these bioactive compounds, making them promising candidates for drug development and the treatment of various health conditions. The notable effects of these compounds include anti-inflammatory, anticancer, antibacterial, antiparasitic, antidiabetic, antiviral, antioxidant, anti-aging, and anti-obesity activities. These compounds are secondary metabolites, including flavonoids, phenolic acids, terpenoids, and tannins, which exhibit remarkable anticancer effects. The promising properties of these compounds have inspired scientists and research centers to investigate their industrialization for addressing human health issues. For instance, Xu et al. [95] demonstrated that certain calothrixins, i.e., metabolites derived from cyanobacteria, were effective as anticancer and antimicrobial agents. Similarly, reviews by Bajpai et al. [138] and Karan and Aydin [139] discussed a range of biologically active and chemically diverse compounds with significant impacts on chronic diseases, including cancer. Qamar et al. [60] also reported that these compounds are efficient sources of bioactive secondary metabolites, noting that over 50% of cyanobacteria are cultivated on commercial platforms for extracting bioactive compounds with anticancer activity; this plays a role in treating various diseases. Finally, Bouyahya et al. [126] provided further support by reporting the presence of various phytochemicals and bioactive compounds with notable anticancer effects—particularly against leukemia and breast cancers. Additional applications were also noted, such as the production of biofuels and cosmetics, as summarized in Table 2.
These positive outcomes also highlighted a range of activities related to the contribution of various chemicals in treating different diseases. Analysis of the data in this table revealed several key findings about the roles that cyanobacteria play in both marine and freshwater environments around Qatar. For example, of 21 genera, approximately 13 were shown to be efficient in nitrogen fixation, while about 10 genera were effective in phycoremediation. In terms of bioactive agents for treating human diseases, producing biofuels, and manufacturing cosmetics, many of these cyanobacteria were found to be either active or promising candidates.

5. Challenges and Future Perspectives

The restoration of habitats, achieving sustainable ecosystem conservation, and maintaining a healthy environment are grounded in five key principles: (1) Information, (2) Problems, (3) Plans, (4) Solutions, and (5) Monitoring. These principles were initially discussed in reports based on a case study by Yasseen and Al-Thani [189] and have been further refined over the past decade [4,28,30,35,48]. This review article highlights a substantial body of work offering valuable insights into the role of phytoplankton. These insights can inform future strategies to address various environmental challenges, including oil and gas pollution, as well as activities related to health, energy demands, and aesthetic considerations.
Notably, phytoplankton, alongside other autotrophs such as seaweeds and seagrasses, demonstrate a remarkable capacity to adapt to pollution stress [49]. This adaptability makes them invaluable experimental models for advanced research in molecular biology and biotechnology [190]. Such research holds significant promise for tackling pollution-related challenges. Furthermore, modern industrial activities must prioritize enhancing human prosperity and well-being while adopting proactive strategies to mitigate the adverse impacts of energy sector expansion. The presence of cyanobacteria in the Arabian Gulf underscores the responsibility of research centers, industrial facilities, and policymakers to support robust research initiatives and promote industrial activities aimed at manufacturing bioactive compounds. It also highlights the urgent need to address current and emerging pollution challenges arising from oil and gas operations.
Biological approaches have recently emerged as environmentally friendly solutions to pollution problems associated with industrial wastewater [4]. These methods provide substantial benefits across diverse sectors, including health, agriculture, the economy, and the pharmaceutical industry. Additionally, advancements in modern biotechnology could amplify the role of autotrophs by enabling the development and application of transgenic organisms capable of remediating polluted soils and waters.
Looking ahead, leveraging cyanobacteria to address various pollution issues and develop industrial activities related to health, the economy, energy, and other essential fields necessitates strategic planning to tackle unforeseen challenges in the Arabian Gulf region. Key factors encouraging such initiatives include: (1) awareness and research capacity: many research centers and universities in the region are well-positioned to pursue such trends, (2) regulatory framework: in Qatar, the Supreme Council for Environment and Nature Reserves (SCENR) enforces laws requiring Environmental Impact Assessments (EIA) for oil and gas companies planning activities that may alter natural habitats, (3) financial status: the Gulf states, with their robust financial resources, are well-placed to lead modern biotechnological research addressing pollution challenges, (4) biodiversity resources: the region’s diverse terrestrial and marine wildlife—including plants, phytoplankton, bacteria, and fungi—represents a genetic repository offering traits to combat various forms of pollution and environmental stress, (5) cyanobacterial efficiency: cyanobacteria and other microorganisms have proven highly effective in nitrogen fixation, particularly in nitrogen-depleted marine environments caused by oil and gas activities. They also contribute to the production of pharmaceutical agents, biofuels, and cosmetics [60,80,140], and (6) promising cyanobacterial genera: specific cyanobacteria, such as Anabaena, Lyngbya, Nostoc, Oscillatoria, and Phormidium, have demonstrated efficiency in cyanoremediation, nitrogen fixation, and the production of anticancer agents, biofuels, and cosmetics. By leveraging these strengths, the region can develop innovative solutions to mitigate pollution and foster sustainable industrial growth.

6. Conclusions

In the Arabian Gulf, future efforts should focus on harnessing the unique properties of marine organisms, particularly cyanobacteria, to drive biotechnological advancements. These organisms hold significant potential for remediating oil and gas pollution and can play a vital role in developing infrastructure across health, energy, and environmental sectors. By leveraging these capabilities, the region can address pressing environmental challenges while fostering progress in areas that support the welfare of its people. The cyanobacteria species discussed in this article are promising candidates for combating pollution, particularly from oil and gas activities, and, also contribute to nitrogen fixation. Furthermore, they offer a rich source of compounds with therapeutic potential, including agents for treating serious diseases such as cancer. Beyond healthcare, bioactive compounds from these species have applications in the biofuel and cosmetics industries. However, it is essential to manage these species carefully, as many cyanobacteria can form blooms that produce toxic metabolites, including hepatotoxins, neurotoxins, and cytotoxins, which pose ecological and health risks.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/pr12122733/s1, Figure S1: Some roles and functions performed by phytoplankton including cyanobacteria; File S1: Review of Harmful Algae Species and Fish Kills in Incidents in the ROPME Sea Area, Al-Muftah, 2004.

Funding

This research received no external funding.

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author.

Acknowledgments

We would like to thank Qatar University for the support provided during the preparation of this article. We thank Nada Abbara for helping in designing and developing a Graphic Abstract and some pathways included in this article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Map of the Arabian Gulf region and its bordering countries.
Figure 1. Map of the Arabian Gulf region and its bordering countries.
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Figure 2. Alkanes degradation.
Figure 2. Alkanes degradation.
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Figure 3. Aromatic compounds degradation.
Figure 3. Aromatic compounds degradation.
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Figure 4. A bloom caused by a substantial increase in cyanobacteria and dinoflagellate populations (File S1).
Figure 4. A bloom caused by a substantial increase in cyanobacteria and dinoflagellate populations (File S1).
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Figure 5. Fish kills result from blooms caused by cyanobacteria and dinoflagellates (File S1).
Figure 5. Fish kills result from blooms caused by cyanobacteria and dinoflagellates (File S1).
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Table 2. Key biotic activities of common cyanobacteria genera found in Qatar [60,80,140].
Table 2. Key biotic activities of common cyanobacteria genera found in Qatar [60,80,140].
GeneraNitrogen Fixation CyanoremediationProduction of Agents
AnticancerBiofuelsCosmetics
Amphanizomenon+++: [141]Needs testP: [140,142]
Anabaena+++: [143]+: [144]+: [140,145]
Calothrix+P+: [146]VP: [142,147]P: [140,148]
ChroococcusVP+: [64]+: [149]P: [150]
Croococcidiopsis++Needs test+: [151]P: [152]
DermocarpellaNeeds testPNeeds test: [60]P: [153]Needs test
EuhalotheceNeeds testPNeeds test: [154]P: [155]P: [124]
Geitlerinema+P+: [156]+: [157]P: [140,158]
GeminocystisNeeds testPP: [159]P: [160]P: [161]
Lyngbya+P+: [162]+: [163,164] +: [140,165]
LeptolyngbyaSome ++P: [125,166]+: [167,168]P: [140,169]
MerismopediaNeeds testP: [126,170]P: [171]P: [140,172]
MicrocystisPP: [130]+: [173]P: [140,174]
Nodularia+PP: [60]+: [175] P: [176]
Nostoc+++: [177,178]+: [179]+: [172,176,180]
Oscillatoria+++: [181,182]+: [163] +: [148]
Phormidium+++: [182] +: [183]+: [172,176,184]
Richelia+PP: [125]P: [145]P: [10,185]
StanieriaNeeds test++: [60]+: [186] P: [172,176]
SynechococcusSome +++: [60]+: [187]P: [150,172]
Trichodesmium++Needs test: [99]+: [188] P: [158]
+: Positive, −: Negative, P: Possible, VP: Very possible.
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Al-Thani, R.F.; Yasseen, B.T. Cyanoremediation of Polluted Seawater in the Arabian Gulf: Risks and Benefits to Human Health. Processes 2024, 12, 2733. https://doi.org/10.3390/pr12122733

AMA Style

Al-Thani RF, Yasseen BT. Cyanoremediation of Polluted Seawater in the Arabian Gulf: Risks and Benefits to Human Health. Processes. 2024; 12(12):2733. https://doi.org/10.3390/pr12122733

Chicago/Turabian Style

Al-Thani, R. F., and B. T. Yasseen. 2024. "Cyanoremediation of Polluted Seawater in the Arabian Gulf: Risks and Benefits to Human Health" Processes 12, no. 12: 2733. https://doi.org/10.3390/pr12122733

APA Style

Al-Thani, R. F., & Yasseen, B. T. (2024). Cyanoremediation of Polluted Seawater in the Arabian Gulf: Risks and Benefits to Human Health. Processes, 12(12), 2733. https://doi.org/10.3390/pr12122733

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