Red Sea brine pool microbiology

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Topographic map of the Red Sea and the relative location. Red Sea topographic map-en.jpg
Topographic map of the Red Sea and the relative location.

The Red Sea and its extensions of the Gulf of Suez and the Gulf of Aqaba contain the largest recorded concentration of deep-sea brine pools on the planet. These pools have many features that make them uninhabitable to almost all organisms on the planet, yet certain communities of microbes thrive within these extreme environments that have temperatures ranging from 2.0 °C to 75 °C. [1] The Red Sea brine pools have extreme salt concentrations and varying compositions of nutrients and other chemicals that directly affect their microbiomes. There are approximately 25 individual pools in the region, [2] [3] some of which are closely clustered together in groups, leading to their undetermined classification of names. The brine pools originate from hydrothermal vents, the shifting of tectonic plates, and the accumulation of water with properties that make it unsuitable for mixing, leading to its accumulation within faults and divots in the sea floor. Atlantis II Deep, Discovery Deep, and the Kebrit are the most investigated and researched brine pools within the Red Sea. [4] Additionally, many microbial species form beneficial symbiotic relationships with organisms living and feeding in proximity to the pools. These relationships allow for the study of specialized adaptations of microbes to brine pool environments.

Contents

List

In addition to the originally-discovered warm brine pools, recent discoveries have found four smaller warm brine pools named the NEOM Brine Pools located in the Gulf of Aqaba. Furthermore, multiple cold seeps have been identified in the Red Sea (the Thuwal Cold Seeps), consisting of two individual pools. Three of these Red Sea brine pools are unnamed, as they are small and potentially extensions of other nearby larger pools.[ citation needed ]

List of Red Sea brine pools and cold seeps
Brine pool numberWarm brine poolCold seeps
1Albatross Deep
2 Atlantis II Deep
3Chain Deep
4Conrad Deep
5Discovery Deep
6Erba Deep
7Kebrit Deep
8, 9, 10, 11NEOM brine pools
12Nereus Deep
13Oceanographers Deep
14Port Sudan Deep
15Shaban Deep
16Shagara Deep
17Suakin Deep
18Valdiva Deeps
19Wando Basin
20, 21Thuwal Cold Seeps

Viral diversity

Composition

Morphologies of varying Caudovirales including Siphoviridae, Myoviridae, and Podoviridae. Ben Darby Caudovirales illustrations.png
Morphologies of varying Caudovirales including Siphoviridae, Myoviridae, and Podoviridae.

The virus community within the many Red Sea brine pools is largely unexplored. However, with the use of metagenomics, viral communities of the Atlantis II Deep, Discovery Deep, and the Kebrit Deep reveal diverse and distinct viruses within and between the brine pools. Across all three brine pools, double-stranded DNA (dsDNA) are the most dominant viruses. [5] [6] Of the dsDNA viruses investigated, Caudovirales are the most abundant across all three brine pools. Low abundances of Phycodnaviridae and trace amounts of Iridoviridae are also present within the brine-seawater interfaces, and thus may be indicative of a "pickling" effect rather than a host-specific presence. [5]

Stratification of viral communities

Viral species tend to follow their bacterial-host population dynamics. Bacterial and archaeal composition and abundance differ between specific layers of the brine pool, including the overlying brine seawater, the brine-water interface, the brine-pool sediments, and direct brine waters. [7] [8] [9] As a result, the viral community within the brine pools of the Red Sea are stratified across the brine-seawater interface. [10] The Kebrit Deep's brine-seawater interface upper layer is dominated by marine bacteria-infecting viruses, relative to the lower layer brine-seawater interface which is dominated by haloviruses and halophages. [5]

Role of viruses

Deep-sea marine viruses maintain the diversity and abundance of the microbial community, recycling and supplying essential nutrients and biomolecules, and regulating the biogeochemical cycling. [11] [12] [13] [14] In deep, anoxic environments such as the Red Sea brine pools, viral infection of prokaryotes releases cellular DNA. Extracellular DNA released through infection supplies highly labile biomolecules in these water conditions limited by external input supporting microbial communities. [13] Through lysogenic viral infection and horizontal gene transfer, the viral community in the Red Sea brine pools contribute to microbial DNA repair, nucleotide metabolism, [15] and the evolutionary adaptations of the microbial community. [6] [15]

Bacterial and archaeal diversity and adaptations

The Red Sea brine pools were once thought to be inhospitable to life. [7] However, extremophiles have adapted to these environments through the development of novel enzymes and metabolic pathways. [16] [4] [17]

The various brine pools contain somewhat similar diversities of microbes; however, due to the different characteristics of each brine pool, distinct microbe compositions are seen. Similarly to the Gulf of Mexico [18] brine pools, the Red Sea brine pool experiences stratification within each distinct brine pool. [19] Therefore, as a result of the stratification, varying physical and chemical properties occur with respect to depth, ensuing a transition in the microbial community with respect to depth. [16] [7]

Moreover, the stratification causes sharp brine-seawater interfaces, with typically-steep gradients in salinity, temperature, density, oxygen, and pH. These distinct interfaces between layers of well-mixed water are characteristic of liquids that are stabilized by salt but destabilized by heating from below. Heat at the bottom of these stable salinity gradients causes double-diffusive convection events. [1]

Specific bacterial composition

Deep-sea anoxic brines (referred to as DHABs, deep hypersaline anoxic basins) are developed by a process of re-dissolving of evaporitic sediments buried at shallow depths, tectonic ejection of the interstitial brine reacted with the evaporites, or by hydrothermal phase separation. [20]

These are examples of various types of bacteria (Table 1) under the brine pools: [21]

ClassFamilyGenus/species/strain
GammaproteobacteriaPseudomonadaceaePseudomonas sp
DeltaproteobacteriaDesulfovibrionaceaeDesulfovibrio sp.
DeferribacteresDeferrribacteraceaeFlexistipes sinusarabici
GammaproteobacteriaAlteromonadaceaeMarinobacter salsuginis
ClostridiaHalanaerobiaceaeHalanaerobium sp.
Firmicutes/MollicutesHaloplasmataceaeHaloplasma contractile
HalobacteriaHalobacteriaceaeHalorhabdus tiamatea
GammaproteobacteriaAlteromonadaceaeMarinobacter salsuginis
ColwelliaceaeSalinisphaera shabanensis
IdiomarinaceaeHalanaerobium sp.
SalinisphaeraceaeNitrosovibrio sp.

Influence of stratification

Stratification within and around water layers is a characteristic of brine pools due to the highly saline environment. Specifically, in the Red Sea, as a result of this stratification in the deep sea brine pools, microbial communities are subject to differences their vertical distribution and composition. [22] For example, through the use of metagenomics and pyrosequencing, the microbial communities of two deeps (Atlantis II and Discovery) were investigated with respect to vertical distribution. In terms of archaeal communities, both deeps showed similar composition having the upper layer (20–50 m) enriched in Halobacteriales, and as salt concentration increased and oxygen decreased, Desulfurococcales tended to dominate due to physiological adaptations. [22] [23] The bacterial composition in the upper layer consisted of Cyanobacteria due to the presence of light. Deeper in the water column, Proteobacteria, specifically the gamma-subdivision group (orders Thiotrichales , Salinisphaerales, Chromatiales, and Alteromonadales ) were found to dominate the more extreme conditions. [22]

The stratification within the Red Sea Brine Pools therefore allows for a complex composition of the microbial community with depth. Due to the variability between each brine pool, this would account for differences in taxa at each location and at each depth.

Bacterial enzymes

Extremozymes are very prominent in Red Sea brine pools as they have the ability to be able to catalyze reactions under harsh environments. [24]

In general, extremozymes can be separated into categories depending on habitats, such as those that can resist extremes of cold (psychrophiles), heat (thermophiles and hyperthermophiles), acidity (acidophiles), alkalinity (alkaliphiles), and salinity (halophiles). [25] Red Sea brine pools are subject to host a polyextremophilic microbiological community providing the environment with a source of extremozymes.

Moreover, most of the extremozymes are classified into three classes of enzymes: oxidoreductases, transferases, and hydrolases; [21] these are important in terms of metabolic processes for the organisms within this habitat as well as for potential applications. [4]

Symbiotic Relationships

Several anoxic, high-salinity deep-sea basins in the Red Sea generate notably sharp interfaces that produce a variety of physicochemical gradients. [26] By acting as a particle trap for organic and inorganic elements from saltwater, brine pools have the ability to significantly increase the supply of nutrients and the possibility for bacterial growth. [27]   On the other hand, halophilic bacteria are required to evolve specific structures to survive the brine pool habitat. For example, halophilic enzymes have a higher proportion of acidic amino acid residues than non-halophilic homologues. These bacterias accumate high concentrations of KCl in their cytoplasms, which reach saturation. [28]

Potential applications for enzymes

Recently, twelve enzymes have been detected in the Red Sea brine pools (Atlantis II Deep, Discovery Deep, and Kebrit Deep) with specific biochemical properties that are promising in their potential applications. [4] The microbes that inhabit the hot, hypersaline, anoxic, and toxic-metal-contaminated Red Sea brine pools produce or accumulate microbial enzymes known as extremozymes allowing life to survive. [29] The chemical and physical properties, in addition to the stability of the extremozymes, provides potential uses in areas including industrial, biotechnical, and pharmaceutical disciplines. [4] [30] [31]

The different enzymes can be attributed to the different organisms that live within each brine pool due to the environments' variable conditions. The Kebrit Deep, one of the smallest Red Sea brine pools, is at 21-23 °C not considered a hot brine. [4] Other characteristics include a pH of 5.2, an 84-m-thick brine layer, and high levels of hydrogen sulfide. [8] [32] The Atlantis II Deep is among the largest Red Sea brine pools and has high temperatures (~68 °C), a pH of 5.3, and high metal content. [33] [34] While Discovery Deep is similar to Atlantis II Deep, it has differences in metal content and is less extreme overall. [35] [36]

Red Sea Brine Pool Extremozymes and Potential Applications
Brine PoolExtremozymePotential Uses
Atlantis II Deep ADH/A1a [4] Pharmaceuticals and biodegradation [4] [37]
ATII-TrxR [38] Cancer therapy and antibiotics [39] [4]
ATII-LCL MerA [40] [41] Bioremediation and mercury detoxification [4] [41]
ATII-LCL-NH [40] Bioremediation [4]
BR3 pol [42] Biomedical DNA techniques [4] [43]
ATII-APH(3') [44] Biotechnology and antibiotics [4] [45]
EstATII [46] Pharmaceuticals, cosmetics, and biodegradation [47] [4]
ATII-ABL [48] Biotechnology and antibiotics [4] [45]
NItraS-ATII [49] Pharmaceuticals and bioremediation [4]
Discovery DeepADH/D1 [50] Pharmaceutical and biodegradation [4]
CA_D [51] Carbon sequestration [4] [52]
Kebrit DeepK09H MerA [53] Bioremediation and mercury detoxification [4] [41]
K35NH MerA [53] Bioremediation and mercury detoxification [4] [41]

Recent discoveries and future implications

The Thuwal cold seeps were accidentally discovered in the Red Sea at about 850m deep on 7 May 2010 by a remotely-operated vehicle. [54] The scientists were conducting a continental slope survey of the Red Sea as part of the KAUST Red Sea Expedition 2010. [54] These cold seeps occur along the tectonically-active continental margin within the Red Sea where hypersaline brine seeps out of the seabed and associates with brine pool formations. [54] The Thuwal cold seeps are considered "cold" due to their cooler temperature (about 21.7 °C) relative to other brine pools found within the Red Sea.[ citation needed ]

Cold seeps are a component of deep sea ecosystems where chemosynthetic bacteria acting as the base of this community use the methane and hydrogen sulfide in seep water as their energy source. [55] The microbial community acts as a base of the food chain for an ecosystem of organisms that helps sustain and feed bottom- and filter-feeders such as bivalves.[ citation needed ]

Discovery of NEOM Brine Pools

During a 2020 research expedition, with the use of bathymetry and geophysical observations, four complex brine pools were discovered in the northern Gulf of Aqaba, which had not yet been known to harbor brine pools. The discovery consisted of three small brine pools less than 10 m2 and another pool that was 10,000 m2 which were given the name NEOM Brine Pools. [31] The NEOM Brine Pools are distinct from other Red Sea brine pools as they are located much closer to the shore. Due to the brine pools' location at 2 km offshore, they are subject to sediment shed and as a result can preserve geophysical properties that could potentially give insight to historical tsunamis, flash floods, and earthquakes that may have occurred in the Gulf Aqaba. [31]

Within these NEOM brine pools, stratification of the overlaying water, the interface, and the brine water caused stratification of microbial diversity. [31] The upper layer consisted of aerobic microbes such as Gammaproteobacteria , Thaumarchaeota Alphaproteobacteria , and Nitrospira . In the deeper convective layers of the NEOM pools, sulfate-reducing and methanogenic microorganisms were more abundant, given the anaerobic conditions. [31]

Related Research Articles

A halophile is an extremophile that thrives in high salt concentrations. In chemical terms, halophile refers to a Lewis acidic species that has some ability to extract halides from other chemical species.

<span class="mw-page-title-main">Psychrophile</span> Organism capable of growing and reproducing in the cold

Psychrophiles or cryophiles are extremophilic organisms that are capable of growth and reproduction in low temperatures, ranging from −20 °C (−4 °F) to 20 °C (68 °F). They are found in places that are permanently cold, such as the polar regions and the deep sea. They can be contrasted with thermophiles, which are organisms that thrive at unusually high temperatures, and mesophiles at intermediate temperatures. Psychrophile is Greek for 'cold-loving', from Ancient Greek ψυχρός (psukhrós) 'cold, frozen'.

<span class="mw-page-title-main">Salt lake</span> Landlocked body of water which has a high concentration of salts

A salt lake or saline lake is a landlocked body of water that has a concentration of salts and other dissolved minerals significantly higher than most lakes. In some cases, salt lakes have a higher concentration of salt than sea water; such lakes can also be termed hypersaline lakes, and may also be pink lakes on account of their colour. An alkalic salt lake that has a high content of carbonate is sometimes termed a soda lake.

<i>Beggiatoa</i> Genus of bacteria

Beggiatoa is a genus of Gammaproteobacteria belonging to the order Thiotrichales, in the Pseudomonadota phylum. These bacteria form colorless filaments composed of cells that can be up to 200 µm in diameter, and are one of the largest prokaryotes on Earth. Beggiatoa are chemolithotrophic sulfur-oxidizers, using reduced sulfur species as an energy source. They live in sulfur-rich environments such as soil, both marine and freshwater, in the deep sea hydrothermal vents, and in polluted marine environments. In association with other sulfur bacteria, e.g. Thiothrix, they can form biofilms that are visible to the naked eye as mats of long white filaments; the white color is due to sulfur globules stored inside the cells.

<span class="mw-page-title-main">Brine pool</span> Large area of brine on the ocean basin

A brine pool, sometimes called an underwater lake, deepwater or brine lake, is a volume of brine collected in a seafloor depression. The pools are dense bodies of water that have a salinity that is three to eight times greater than the surrounding ocean. Brine pools are commonly found below polar sea ice and in the deep ocean. Those below sea ice form through a process called brine rejection. For deep-sea brine pools, salt is necessary to increase the salinity gradient. The salt can come from one of two processes: the dissolution of large salt deposits through salt tectonics or geothermally heated brine issued from tectonic spreading centers.

<span class="mw-page-title-main">Gammaproteobacteria</span> Class of bacteria

Gammaproteobacteria is a class of bacteria in the phylum Pseudomonadota. It contains about 250 genera, which makes it the most genus-rich taxon of the Prokaryotes. Several medically, ecologically, and scientifically important groups of bacteria belong to this class. All members of this class are Gram-negative. It is the most phylogenetically and physiologically diverse class of the Pseudomonadota.

Hydrogen-oxidizing bacteria are a group of facultative autotrophs that can use hydrogen as an electron donor. They can be divided into aerobes and anaerobes. The former use hydrogen as an electron donor and oxygen as an acceptor while the latter use sulphate or nitrogen dioxide as electron acceptors. Species of both types have been isolated from a variety of environments, including fresh waters, sediments, soils, activated sludge, hot springs, hydrothermal vents and percolating water.

A chemocline is a type of cline, a layer of fluid with different properties, characterized by a strong, vertical chemistry gradient within a body of water. In bodies of water where chemoclines occur, the cline separates the upper and lower layers, resulting in different properties for those layers. The lower layer shows a change in the concentration of dissolved gases and solids compared to the upper layer.

Haloplasma contractile is a halophilic, cell wall-less bacterium. It is the only known representative of a deep lineage, and is classified in its own family (Haloplasmataceae) and order (Haloplasmatales), in the class Mollicutes. In terms of genetics, the bacterium Haloplasma contractile contains a dcw gene cluster is responsible for containing all the genes of the organism and promoting peptidoglycan synthesis. Also, MreB/Mbl are specific homologous parts of this bacterium that are vital in the contractility of the cell. Regarding its physical attributes, this organism consists of a spherical body with approximately two protrusions which alternate between straight and contracted forms.

<span class="mw-page-title-main">Blood Falls</span> Red-colored seep of saltwater flowing from Taylor Glacier in Antarctica

Blood Falls is an outflow of an iron oxide–tainted plume of saltwater, flowing from the tongue of Taylor Glacier onto the ice-covered surface of West Lake Bonney in the Taylor Valley of the McMurdo Dry Valleys in Victoria Land, East Antarctica.

L'Atalante basin is a hypersaline brine lake at the bottom of the Mediterranean Sea about 192 km (119 mi) west of the island of Crete. It is named for the French L'Atalante, one of the oceanographic research vessels involved in its discovery in 1993. L'Atalante and its neighbors the Urania and Discovery deep hyper saline anoxic basins (DHABs) are at most 35,000 years old. They were formed by Messinian evaporite salt deposits dissolving out of the Mediterranean Ridge and collecting in abyssal depressions about 3,000 m (9,800 ft) deep. L'Atalante is the smallest of the three; its surface begins at about 3,500 m (11,500 ft) below sea level.

<span class="mw-page-title-main">Soda lake</span> Lake that is strongly alkaline

A soda lake or alkaline lake is a lake on the strongly alkaline side of neutrality, typically with a pH value between 9 and 12. They are characterized by high concentrations of carbonate salts, typically sodium carbonate, giving rise to their alkalinity. In addition, many soda lakes also contain high concentrations of sodium chloride and other dissolved salts, making them saline or hypersaline lakes as well. High pH and salinity often coincide, because of how soda lakes develop. The resulting hypersaline and highly alkalic soda lakes are considered some of the most extreme aquatic environments on Earth.

<span class="mw-page-title-main">Zetaproteobacteria</span> Class of bacteria

The class Zetaproteobacteria is the sixth and most recently described class of the Pseudomonadota. Zetaproteobacteria can also refer to the group of organisms assigned to this class. The Zetaproteobacteria were originally represented by a single described species, Mariprofundus ferrooxydans, which is an iron-oxidizing neutrophilic chemolithoautotroph originally isolated from Kamaʻehuakanaloa Seamount in 1996 (post-eruption). Molecular cloning techniques focusing on the small subunit ribosomal RNA gene have also been used to identify a more diverse majority of the Zetaproteobacteria that have as yet been unculturable.

<span class="mw-page-title-main">Brinicle</span> Sea ice formation

A brinicle is a downward-growing hollow tube of ice enclosing a plume of descending brine that is formed beneath developing sea ice.

Sulfurimonas is a bacterial genus within the class of Campylobacterota, known for reducing nitrate, oxidizing both sulfur and hydrogen, and containing Group IV hydrogenases. This genus consists of four species: Sulfurimonas autorophica, Sulfurimonas denitrificans, Sulfurimonas gotlandica, and Sulfurimonas paralvinellae. The genus' name is derived from "sulfur" in Latin and "monas" from Greek, together meaning a “sulfur-oxidizing rod”. The size of the bacteria varies between about 1.5-2.5 μm in length and 0.5-1.0 μm in width. Members of the genus Sulfurimonas are found in a variety of different environments which include deep sea-vents, marine sediments, and terrestrial habitats. Their ability to survive in extreme conditions is attributed to multiple copies of one enzyme. Phylogenetic analysis suggests that members of the genus Sulfurimonas have limited dispersal ability and its speciation was affected by geographical isolation rather than hydrothermal composition. Deep ocean currents affect the dispersal of Sulfurimonas spp., influencing its speciation. As shown in the MLSA report of deep-sea hydrothermal vents Campylobacterota, Sulfurimonas has a higher dispersal capability compared with deep sea hydrothermal vent thermophiles, indicating allopatric speciation.

<i>Haloquadratum walsbyi</i> Species of halotolerant archaea

Haloquadratum walsbyi is a species of the genus Haloquadratum, within the archaea domain known for its square halophilic nature. First discovered in a brine pool in the Sinai peninsula of Egypt, H. walsbyi is noted for its flat, square-shaped cells, and its unusual ability to survive in aqueous environments with high concentrations of sodium chloride and magnesium chloride. The species' genus name Haloquadratum translates from Greek and Latin as "salt square". This archaean is also commonly referred to as "Walsby's Square Bacterium" because of its identifying square shape which makes it unique. In accordance with its name, Haloquadratum walsbyi are most abundantly observed in salty environments.

<span class="mw-page-title-main">Sea ice microbial communities</span> Groups of microorganisms living within and at the interfaces of sea ice

Sea Ice Microbial Communities (SIMCO) refer to groups of microorganisms living within and at the interfaces of sea ice at the poles. The ice matrix they inhabit has strong vertical gradients of salinity, light, temperature and nutrients. Sea ice chemistry is most influenced by the salinity of the brine which affects the pH and the concentration of dissolved nutrients and gases. The brine formed during the melting sea ice creates pores and channels in the sea ice in which these microbes can live. As a result of these gradients and dynamic conditions, a higher abundance of microbes are found in the lower layer of the ice, although some are found in the middle and upper layers. Despite this extreme variability in environmental conditions, the taxonomical community composition tends to remain consistent throughout the year, until the ice melts.

<span class="mw-page-title-main">Hydrothermal vent microbial communities</span> Undersea unicellular organisms

The hydrothermal vent microbial community includes all unicellular organisms that live and reproduce in a chemically distinct area around hydrothermal vents. These include organisms in the microbial mat, free floating cells, or bacteria in an endosymbiotic relationship with animals. Chemolithoautotrophic bacteria derive nutrients and energy from the geological activity at Hydrothermal vents to fix carbon into organic forms. Viruses are also a part of the hydrothermal vent microbial community and their influence on the microbial ecology in these ecosystems is a burgeoning field of research.

An anchialine system is a landlocked body of water with a subterranean connection to the ocean. Depending on its formation, these systems can exist in one of two primary forms: pools or caves. The primary differentiating characteristics between pools and caves is the availability of light; cave systems are generally aphotic while pools are euphotic. The difference in light availability has a large influence on the biology of a given system. Anchialine systems are a feature of coastal aquifers which are density stratified, with water near the surface being fresh or brackish, and saline water intruding from the coast at depth. Depending on the site, it is sometimes possible to access the deeper saline water directly in the anchialine pool, or sometimes it may be accessible by cave diving.

A sea ice brine pocket is an area of fluid sea water with a high salt concentration trapped in sea ice as it freezes. Due to the nature of their formation, brine pockets are most commonly found in areas below −2 °C (28 °F), where it is sufficiently cold for seawater to freeze and form sea ice. Though the high salinity and low light conditions of brine pockets create a challenging environment for marine mammals, brine pockets serve as a habitat to various microbes. Sampling and studying these pockets requires specialized equipment and alterations to methodologies to accommodate the hyper-saline conditions and subzero temperatures.

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