Beggiatoa
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Genus: | Beggiatoa Trevisan 1842[1]
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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.[3] 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.
Discovery
Beggiatoa was originally described as a type of blue-green algae (today known as
Taxonomy
The genus Beggiatoa is diverse, with representatives occupying several habitats and niches, both in fresh and salt water. In the past, they have been confused as close relatives of Oscillatoria spp. (phylum Cyanobacteria) because they have similar morphology and motility,[8] but 5S rRNA analysis showed that members of Beggiatoa are phylogenetically distant from Cyanobacteria, and are instead members of the phylum Gammaproteobacteria.[9]
Despite their diversity, only two species of Beggiatoa have been formally described: the type species Beggiatoa alba and Beggiatoa leptomitoformis, the latter of which was only published in 2017.[2][10]
The capability to oxidize
Genetics
Because of the lack of a
Morphology and motility
Beggiatoa spp. can be divided into three morphological categories[15] (with some exceptions):
- Freshwater strains, characterized by narrow filaments with no vacuoles;
- Narrow marine strains, without vacuoles (filaments' diameter of about 4.4 μm);
- Larger marine strains, with vacuoles for nitrate storing (filaments' diameter vary between 5 and 140 μm)
Narrow filaments are usually composed of cylindrical cells whose length is about 1.5 to 8 times their thickness; in wider filaments, cells are instead disk-shaped with cell lengths from 0.10 to 0.90 times their cell width. In all of the cultured strains the terminal cells of the filaments appear rounded.[15]
Although they are
Beggiatoa move via gliding motility, using the excretion of mucus.[16] The exact mechanisms of this gliding motility are unknown.[17] In the species Beggiatoa alba, this trail of mucus is composed of mannose and glucose, two types of neutral polysaccharide. String-like structures on the outer membrane and trans-peptidoglycan channels have been observed on the surface layer, which also may play a role.[15][17] Beggiatoa gliding motility is induced via chemotaxis, which allows filaments to direct themselves away from high oxygen, sulfide, and light levels.[15] Beggiatoa filaments reverse their gliding direction to reach more suitable conditions for their metabolism. Long filaments moving in opposite directions may split in two by killing an intermediate cell, referred to as a necrida, which then cuts off communication and coordinated movement between the two segments.[15]
Cell growth
Beggiatoa use fragmentation as a reproductive strategy. A colony can develop into a mat through alternating filament elongation and breakage. Breakage can happen in the middle of a stretched filament, at the tip of a filament loop, or where a tip of a loop was once placed. Sacrificial cells interrupt the communication between two parts of one filament; in this way each section can change its gliding direction causing the split.[citation needed]
The average filament length achieved through this process is also result of gene-environment interactions as, for instance, the growth and position of the filament is function of vertical gradients of oxygen and sulfide. Therefore, it is proposed that good environmental conditions will paradoxically cause cell death in order to enhance filament breakage, thus reproduction.[18]
Metabolism
Beggiatoa group is mainly composed by
Carbon metabolism
In Beggiatoa group are present both
Nitrogen metabolism
Beggiatoa group shows substantial versatility in utilizing nitrogen compounds. Nitrogen can be a source for growth or, in the case of nitrate, it can be an electron acceptor for anaerobic respiration. Heterotrophic freshwater Beggiatoa spp. assimilate nitrogen for growth. Nitrogen sources include nitrate, nitrite, ammonia, amino acids, urea, aspartate, asparagine, alanine and thiourea, depending on the capability of specific strains.
Autotrophic vacuolated Beggiatoa are able to store nitrate in their vacuoles 20.000 times the concentration of the surrounding sea water, and use it as terminal electron acceptor in anoxic conditions. This process, called Dissimilatory Nitrate Reduction to Ammonium (DNRA), reduces nitrate to ammonium. The capability of using nitrate as electron acceptor allows the colonization of anoxic environments, such as microbial mats and sediments. Several species are able to fix nitrogen using nitrogenase enzyme (e.g. Beggiatoa alba).[3][15]
Sulfur metabolism
Sulfide aerobic oxidation:
Sulfide anaerobic oxidation:
There are some cases of
Anaerobic respiration:
Hydrogen metabolism
The strain Beggiatoa sp. 35Flor is able to use hydrogen as alternative electron donor to sulfide. This oxidation process can provide energy for maintenance and assimilatory purposes and is helpful to reduce stored sulfur when it becomes excessive, but it can't provide growth to the strain.[21]
Hydrogen oxidation:
Phosphorus metabolism
Beggiatoa's metabolism include the use of phosphorus in the polyphosphate form. The regulation of this metabolism relies on the environmental conditions. Oxygenated surroundings cause an accumulation of polyphosphate, while anoxia (coupled with an increasing concentration of sulfide) produces a breakdown of polyphosphate and its subsequent release from the cells. The released phosphate can then be deposited as phosphorite minerals in the sediments or stay dissolved in the water.[15]
Ecology
Filaments have been observed to form dense mats on sediments in a very huge variety of environments. They appear as a whitish layer and since they are present and flourish in
Beggiatoa live at the oxic/anoxic interface, where they benefits from the presence of both hydrogen sulfide and oxygen. The chemolithoautotrophic strains of Beggiatoa are also considered important primary producers in dark environments.[3]
Habitat
The incredible number of adaptations and
Vacuolated Beggiatoa can be very common in coastal upwelling regions (for example Peru and Chile coasts), deep sea hydrothermal vents and cold vents; in these environments the floc mats (hair-like breast) can grow up and cover large areas and reach the height of 30 cm. In deep sea hydrothermal vents and cold-seeps Beggiatoa can grow in filaments that can be up to 200 micrometres in diameter, which makes these ones the largest prokaryotes currently known. Vacuolated Beggiatoa can be found also in hypoxic seafloor, where the filaments can live inside the sediments at the depth of few cm (from 2 to 4 cm); in same cases the Beggiatoa bacterial filaments can be the most abundant part of the microbial biomass in the sediments.[3]
Beggiatoa is also found in salt marshes, saline, and geothermally active underwater caves. Some studies on these environments have been carried out in the underwater caves of dolomitized limestone in Capo Palinuro, Salerno, (Italy). Here there are hydrothermal sulphidic springs and microbial biofilm is associated with the flow of hydrothermal fluids, whose activity is intermittent and starts during low tide. Mats found in the caves were composed by filaments resembling in most part Beggiatoa, Thiothrix and Flexibacter, and this Beggiatoa-like filaments were morphologically close to those found attached to rocks and the byssus of the mussels from Lucky Strike Hydrothermal vents on the Mid-Atlantic Ridge.[3]
Interactions with other organisms
Beggiatoa can form complex microbial mats in association with other filamentous bacteria, such as cyanobacteria. The cyanobacteria usually occupy the surface layer of the mat, and produce a great amount of oxygen during the day through photosynthesis. Conversely, Beggiatoa grow beneath the phototrophs, along an oxic/anoxic (oxygen/sulfide) interface, where they produce white patches.[3] However, during dark acclimation, the mat became anoxic, so the Beggiatoa moved to the mat surface, to avoid the high levels of H2S and remain at the oxygen/sulfide interface, while cyanobacteria remained in a dense layer below.[29] Sometimes Beggiatoa mats are enriched by the presence of diatoms and green euglenoids too,[23] but also protists as ciliates and dinoflagellates have been found associated with the mats at the Guaymas Basin hydrothermal vent ecosystem and they likely consume a large amount of bacterial biomass.[30]
As the microbial mats can reach 3 cm in width, they can be a food source for many grazers. This trophic connection has been observed in
Furthermore, many
Role in biogeochemical cycles
Several species of white sulfur bacteria in the family Beggiatoaceae can accumulate and transport
- On the one hand, the regulation of free H2S concentration in marine sediments is fundamental because sulfide-depleted surface sediments are essential for survival of benthic infauna, in fact sulfide is highly toxic to bottom fauna and other organisms living in the sediment;
- On the other hand, NO3− reduction is important for the control of eutrophication in nitrogen-limited coastal waters.[34]
Beggiatoa can also accumulate phosphorus as polyphosphate, which it subsequently releases as phosphate under anoxic conditions. This might increase the availability of phosphorus to primary producers if the phosphate is released from the sediment to the water column. Studies on phosphorus cycling and phosphorus release Beggiatoa in Baltic Sea have found that the oxidation of sulfide by these bacteria may decrease the rate of iron sulfide formation in the sediments, and thus increase the phosphorus retention capability of the sediment.[15]
Cultivation
Selective Enrichments
The most successful
Pure culture isolation
There are three different possible techniques to obtain isolated Beggiatoa strains in pure culture:
- Isolation on agar plates
- Isolation using liquid media
- Isolation and cultivation in gradient media
Isolation on agar plates
The procedure to isolate a heterotrophic strain requires an agar plate containing dilute organic substrates such as small amount of peptone. Then, tufts of Beggiatoa filaments are collected from the environment, washed with sterile washing solution and placed on the agar plate. In this way, there will be some growing filaments moving away from the central inoculum that can be used as inoculum for a new agar plate.[3]
For the isolation of marine Beggiatoa strains (that show autotrophic growth), since they are obligate microaerophiles it is essential to provide micro-oxic conditions and to use particular agar plates made with filtered seawater and supplemented with sodium sulfide and sodium acetate. In comparison, for freshwater strains, isolation must be performed under oxic conditions (air atmosphere) using a variety of media containing a low concentration of single organic compound such as acetate, Na2S or thiosulfate.[3]
Isolation using liquid media
Liquid media are often used for enrichment, most probable number (MPN) enumeration and bulk cultivation of Beggiatoa. To successfully cultivate heterotrophic or mixotrophic freshwater Beggiatoa, liquid media has to contain little amounts of carbon substrate, either soil extracts or acetate. The type species and strain (Beggiatoa alba str. B18LD) and related strains are generally grown in media that include a salt base, acetate as carbon source, and variable yeast extract and sulfide additions.[35] Some marine autotrophic Beggiatoa strains are also been cultured on defined liquid mineral medium with thiosulfate, CO2, and micro-oxic conditions under aeration with 0.25% O2 (v/v) in the gas phase.[3]
Isolation and cultivation in gradient media
Autotrophic strains coming from a single filament isolation on agar can easily be maintained and propagated in sulfide gradient tubes in which sulfide-rich agar plugs are overlaid with sulfide-free soft agar. Tubs are loosely closed in order to permit the exchange of headspace gasses with the atmosphere. As result, two opposite layers are formed, one that contains sulfide while the other one oxygen: this allows the growth of a well-defined Beggiatoa layer at the sulfide-oxygen interface. The gradient medium construction requires different amounts of J3 medium (made by agar and NaHCO3) supplemented with neutralized Na2S placed in a screw-capped tube. Here, the sulfur source is provided by the flux of sulfide. Another "layer" is made by NaHCO3 without sulfide or thiosulfate: all of the sulfide will be below the interface between the sulfidic agar plug and the sulfide-free overlay agar while there will be another layer in the top of the tube that represents the oxygen reservoir. It begins to form a gradient shape due to the reaction between sulfide and oxygen: as a result, the filaments rapidly proliferate at the sulfide-oxygen interface, forming a marked layer, or "plate", of 1 mm but it is also possible to appreciate that these bacteria can track the interface and slowly descend owing to the gradual depletion of the sulfide reservoir.[3]
References
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- ^ a b de Albuquerque, Julia Peixoto; Keim, Carolina Neumann; Lins, Ulysses (July 2010). "Comparative analysis of Beggiatoa from hypersaline and marine environments". Micron. 41 (5): 507–517 – via Elsevier Science Direct.
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