Thiomargarita namibiensis

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Thiomargarita namibiensis
Sulphide bacteria crop.jpg
Stained micrograph of Thiomargarita namibiensis
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Bacteria
Phylum: Pseudomonadota
Class: Gammaproteobacteria
Order: Thiotrichales
Family: Thiotrichaceae
Genus: Thiomargarita
Species:
T. namibiensis
Binomial name
Thiomargarita namibiensis
Schulz et al., 1999

Thiomargarita namibiensis is a harmless, gram-negative, facultative anaerobic, coccoid bacterium found in the ocean sediments of the continental shelf of Namibia. [1] The genus name Thiomargarita means "sulfur pearl." This refers to the appearance of the cells as they contain microscopic sulfur granules that scatter incident light, lending the cell a pearly luster. This causes the cells to form chains, resembling strings of pearls. [2] The species name namibiensis means "of Namibia", which is an ode to their country of discovery and existence. Together, Thiomargarita namibiensis means “Sulfur pearl of Namibia". [1]

It is the second largest bacterium ever discovered, at 0.1–0.3 mm (100–300 μm) in diameter on average, but can attain up to 0.75 mm (750 μm), [3] [4] making it large enough to be visible to the naked eye. Thiomargarita namibiensis is nonpathogenic.

Thiomargarita namibiensis is categorized as a mesophile [5] because of its preference for moderate temperatures, which typically range between 20-45 degrees Celsius. The organism shows neutrophilic characteristics by favoring environments with neutral pH levels like 6.5-7.5. This highlights the bacterium's unique strategies to maintain its survival and grow. [6]

Discovery

The species Thiomargarita namibiensis was collected in 1997 and discovered in 1999 by Heide N. Schulz and her colleagues from the Max Planck Institute for Marine Microbiology. [7] It was discovered in coastal sediments on the Namibian coast of West Africa. Schulz and her colleagues were aboard the Russian research vessel Petr Kottsov off the coast of Namibia in search of Beggiatoa and Thioploca , other recently discovered sulfide-eating marine bacteria, because the team had done previous research on these bacteria of the Pacific coast of South America, an area with similar hydrography. [8] Schulz's team found small quantities of Beggiatoa and Thioploca in sediment samples, but large quantities of the previously undiscovered Thiomargarita namibiensis. [9] [3] Researchers suggested the species be named Thiomargarita namibiensis, which means "sulfur pearl of Namibia". [1] The previously largest known bacterium was Epulopiscium fishelsoni , at 0.5 mm long. [10] The current largest known bacterium is Thiomargarita magnifica, described in 2022, at an average length of 10 mm. [9] [11]

Distribution of Thiomargarita Namibiensis in Namibia DistributionThiomargaritaNamibiensisNamibia.jpg
Distribution of Thiomargarita Namibiensis in Namibia

In 2002 a strain exhibiting 99% identity with Thiomargarita namibiensis was found in sediment cores taken from the Gulf of Mexico during a research expedition. [12] This similar strain either occurs in single cells or clusters of 2, 4, and 8 cells, as opposed to the Namibian strain which occurs in single chains of cells separated by a thin mucus sheath. [13]

Occurrence

Thiomargarita namibiensis was found in the continental shelf off the coast of Namibia, an area with high plankton productivity, low oxygen concentrations between 0-3 μM, and nitrate concentrations of 5-28 μM. [2] The most bacteria were obtained from the upper 3 cm of sediment in the sample, with concentrations decreasing exponentially past this point. [14] In this section of sediment, there were sulfide concentrations of 100-800 μM. [2] Although previously undiscovered, T. namibiensis is not uncommon by any means in its environment. It is by far the most common benthos bacterium of the Namibian shelf, comprising almost 0.8% of the sediment volume. [15] The Namibian coastal environmental experiences strong upwelling, resulting in low oxygen levels in the lower waters with large amounts of plankton. Thiomargarita namibiensis is most prevalent in the Walvis Bay area at 300 feet deep, [1] but they are distributed along the coast of Namibia from Palgrave Point to Lüderitzbucht. [16] The highest number of Thiomargarita namibiensis is present in the sediment's uppermost three centimeters; they form a film on top of the sediment, detoxifying the sulfide so that it is able to enter the water column. [17] Since the Thiomargarita namibiensis are immobile, they are unable to seek more a more ideal environment when sulfide and nitrate levels are low in this environment. [12] They simply remain in position and wait for levels to increase once again so that they can undergo respiration and other processes. [1] The organism also has a direct impact on its environment. Apatite, a mineral high in phosphorite, is correlated with the abundance of T. namibiensis through phosphogenesis. [18] Internal polyphosphate and nitrate are used as external electron acceptors in the presence of acetate, releasing enough phosphate to cause precipitation. While the amount directly created by T. namibiensis cannot be calculated, it is a significant contribution to the large amounts of hydroxyapatite in solid-phase shelf sediment. [14] The Mexican strain was primarily found in the top centimeter of sediment sampled from cold seeps in the Gulf of Mexico. The top 3 cm of sediment from the Gulf of Mexico locations contained sulfide concentrations of 200-1900 μM. [13]

Thiomargarita namibiensis, collecting nitrate and oxygen in water above the bottom in case of being resuspended and collecting sulfide in the sediments ThiomargaritaFeeding.jpg
Thiomargarita namibiensis, collecting nitrate and oxygen in water above the bottom in case of being resuspended and collecting sulfide in the sediments

Structure

Although Thiomargarita are closely related to Thioploca and Beggiatoa in function, their structures are different. Thioploca and Beggiatoa cells are much smaller and grow tightly stacked on each other in long filaments. [14] Their shape is necessary for them to shuttle down into the ocean sediments to find more sulfide and nitrate. [19] In contrast, Thiomargarita grow in rows of separate single ball-shaped cells, so they lack the range of mobility that Thioploca and Beggiota have. [14] Thiomargarita can also grow in barrel shapes. The spherical shaped Thiomargarita can join together to create chains of 4-20 cells, while the barrel shaped Thiomargarita can form chains of more than 50 cells. [20] These chains are not linked together by filaments, but connected by a mucus sheath. [5] Each cell appears reflective and white as a result of their sulfur content. [21]

With their lack of movement, Thiomargarita have adapted by evolving very large nitrate-storing bubbles, called vacuoles, allowing them to survive long periods of nitrate and sulfide starvation. [22] However, new studies have shown that although there are no present motility features, the individual spherical cells can move slightly in a “slow jerky rolling motion,”  but this does not give them free-range motion as traditional motility features would. [23] The vacuoles give them the ability to stay immobile, just waiting for nitrate-rich waters to sweep over them once again. [24] These vacuoles are what account for the size that scientists had previously thought impossible, and account for roughly 98% of the cell volume. [25] Because of the vast size of the liquid central vacuole, the cytoplasm separating the vacuole and the cell membrane is a very thin layer reported to be around 0.5-2 micrometers thick. This cytoplasm, however, is non-homogenous. The cytoplasm contains small bubbles of sulfur, polyphosphate, and glycogen. These bubbles give the cytoplasm a “sponge-like” resemblance. [5]

Scientists disregarded large bacteria, because bacteria rely on chemiosmosis and cellular transport processes across their membranes to make ATP. [26] As the cell size increases, they make proportionately less ATP, thus energy production limits their size. [2] Thiomargarita are an exception to this size constraint, as their cytoplasm forms along the periphery of the cell, while the nitrate-storing vacuoles occupy the center of the cell. [24] As these vacuoles swell, they greatly contribute to the record sizes of Thiomargarita cells. T. namibiensis holds the record for the world's second largest bacteria, with a volume three million times more than that of the average bacteria. [27]

Being that areas of nitrate and hydrogen sulfide do not mix together and T. namibiensis cells are immobile, the storage vacuoles in the cell provide a solution to this problem. [24] Because of these storage vacuoles, cells are able to stay viable without growing (or dividing), with low relative amounts of cellular protein, and large amounts of nitrogen in the vacuoles. The storage vacuoles provide a novel solution which allows cells to wait for changing conditions while staying alive. [2] These vacuoles are packed with sulfur granules that can be used for energy and contribute to their chemolithotrophic metabolism. The vacuoles of Thiomargarita namibiensis contribute to their gigantism, allowing them to store nutrients for asexual reproduction of their complex genome. [28]

Metabolism

The bacterium is chemolithotrophic and is capable of using nitrate as the terminal electron acceptor in the electron transport chain. [29] Chemo refers to the way the microbe obtains its energy, which is done so by using oxidation-reduction reactions of organic material. [14] Litho defines an organism's way of getting energy, which is done so by using inorganic molecules as a source of electrons. This would be useful in an environment with not a lot of nutrients, such as soil or in a place with lots of sulfur. The final part of this metabolism characterization is how the bacterium obtains carbon, which in this case is done so in an autotrophic way. This means the organism uses carbon dioxide (CO2) from its environment as a carbon source and then synthesizes organic compounds from it. [12] In addition to being a chemolithoautotroph, this bacterium uses anaerobic respiration due to its environment not suppling ample oxygen. In order to survive in such a harsh environment, Thiomargarita namibeiensis uses what is known as the reverse or reductive TCA cycle to convert CO2 into usable energy. [6] This adaptation shows how the bacterium has learned to survive in specific environments where usual metabolic pathways might not work well enough. The organism will oxidize hydrogen sulfide (H2S) into elemental sulfur (S). [14] This is deposited as granules in its periplasm and is highly refractile and opalescent, making the organism look like a pearl.There is still much unknown about the metabolism and phylogeny of the sulfur bacteria. [29]

The large vacuole mainly stores nitrate for sulfur oxidation, the main energy source for T. namibiensis. [30] Large amounts of nitrogen must be stored as a terminal electron acceptor in the electron transport chain. Because of this and the organism's size, large amounts of sulfur are required which are then stored as cyclooctasulfur. [24] The large amount of nitrogen helps T. namibiensis produce large amounts of energy, something that is necessary with the large size of the organism.

While the sulfide is available in the surrounding sediment, produced by other bacteria from dead microalgae that sank down to the sea bottom, the nitrate comes from the above seawater. Since the bacterium is sessile, and the concentration of available nitrate fluctuates considerably over time, it stores nitrate at high concentration (up to 0.8 molar [2] ) in a large vacuole like an inflated balloon, which is responsible for about 80% of its size. [13] When nitrate concentrations in the environment are low, the bacterium uses the contents of its vacuole for respiration. T. namibiensis cells possess elevated nitrate concentrations making them able to exhibit the capacity to absorb oxygen both when nitrate is present and when it is not. Thus, the presence of a central vacuole in its cells enables a prolonged survival in sulfidic sediments. The non-motility of Thiomargarita cells is compensated by its large cellular size. [5] This immobility suggests that they rely on shifting chemical conditions. [17]

Cyclooctasulfur is stored in the globules of sulfur in the vacoules of T. namibiensis, aiding in their metabolism. [31] After the oxidation of sulfide, T. namibiensis stores sulfur as cyclooctasulfur, the most thermodynamically stable form of sulfur at standard temperature and pressure. [12] With these sulfur globules in the cell, the organism uses it as storage of elemental sulfur in usually anoxic conditions to reduce the toxicity of various sulfur compounds (can also survive in atmospheric oxygen conditions as it is not toxic). The sulfur globules are stored in the thin outer layer of the cytoplasm, presumably after their use as a source of electrons in the electron transport chain through oxidation of sulfide. [31] The ability to oxidize hydrogen sulfide provides nutrients to other organisms living near it. [32]

The bacterium is a facultatively anaerobic rather than obligately anaerobic, and thus capable of respiring with oxygen if it is plentiful. [33] While not much is known about the exact metabolism the bacterium performs, it is known to exist in environments of high sulfur and little to no oxygen present. [7]

Reproduction

T. namibiensis reproduces mainly through binary fission. [17] Reproduction of T. namibiensis occurs on a single plane. [13] This means that the cocci (a spherical bacterial cell) divide into diplococcus or streptococcus arrangement. [34] A diplococcus is a pair of cocci cells that can form chains, and streptococcus is a grape-like cluster of cells. [35] In the case of T. namibiensis, a diplococci structure is observed. Despite this, its cells remain connected, forming chains within a common mucus matrix. In addition to helping with essential functions including food exchange and cell-to-cell communication, this matrix can give the bacteria protection and structural support. [30] During the process of binary fission, a single bacterial cell divides into two identical daughter cells, representing a comparatively basic form of asexual reproduction. [12] The cells that make up the filamentous chain may then separate into smaller segments, and each of those segments may go on to produce a new filament. [36]

Genome

The genome of this organism is complex. Instead of being distributed in a nucleoid region within the cytoplasm, T. namibiensis cells have their DNA concentrated in small masses around the inner side of the cell membrane. [6] This could be used to regulate the processes of these large bacteria, as diffusion of protein and other material would take a long time in these large cells. [17] This way of constructing its genome is very similar to the bacteria Epulopiscium . [5] There is not much known about the genomic abilities of Thiomargarita nambiensis, making it difficult to study. [37]

Significance

Thiomargarita namibiensis is unique due to its gigantism, which is usually a disadvantage for bacteria. [38] Bacteria obtain their nutrients via diffusion and cellular transport processes across their cell membrane, as they lack the sophisticated nutrient uptake mechanisms such as endocytosis found in eukaryotes. [17] A bacterium of large size would imply a lower ratio of cell membrane surface area to cell volume. [6] This would limit the rate of uptake of nutrients to threshold levels. [25] Large bacteria might starve easily unless they have a different backup mechanism. [6] Since T. namibiensis is immobile in the sediments it is found in, it must survive long periods of time without nitrate. [6] T. namibiensis overcomes this problem by harboring large vacuoles that can be filled up with life-supporting nitrates. [39] Gigantism likely evolved to increase the bacterium's nitrate storage space, which makes up about 98% of its volume. This also allows T. namibiensis to hold its breath for months. [7]

T. namibiensis plays a vital role in the sulfur and nitrogen cycles. In their sulfur rich environment, oxygen is scarcely available and cannot be used as an electron acceptor. In turn, T. namibiensis uses nitrate as the electron acceptor, which they consume at the sediment surface and condense in a vacuole. From this, they can oxidize the sulfide that inhabits the sediment. This acts as a detoxifier which removes poisonous gas from the water. This keeps the environment affable for fish and other marine living beings. This bacteria also plays an essential role in the phosphorus cycle of the sediment. T. namibiensis can release phosphate in anoxic sediments that possess high rates which contribute to the spontaneous precipitation of phosphorus-containing material. This plays an important role in the removal of phosphorus in the biosphere. [5] It functions to oxidize and detoxify sulfide, which is usually poisonous to the human body and surrounding environment. [1]

See also

Related Research Articles

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References

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