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.
Discovery Beggiatoa was originally described as a type of blue-green algae (today known as Cyanobacteria) by the botanist Vittore Trevisan in 1842, who named it in honor of the Italian doctor and botanist Francesco Secondo Beggiato (1806 - 1883), from Venice. Later, it was shown that Beggiatoa in their natural habitat of sulfur springs accumulate sulfur globules in their cells. The Ukrainian microbiologist Sergei Winogradsky, working in the laboratory of Anton de Bary, showed that these intracellular sulfur globules were formed when Beggiatoa oxidized hydrogen sulfide (H2S) as an energy source, with oxygen as the terminal electron acceptor and CO2 used as a carbon source. Winogradsky referred to this form of metabolism as "inorgoxidation" (oxidation of inorganic compounds), today called chemolithotrophy. The finding represented the first discovery of lithotrophy.
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, but 5S rRNA analysis showed that members of Beggiatoa are phylogenetically distant from Cyanobacteria, and are instead members of the phylum Gammaproteobacteria.
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.
The capability to oxidize sulfide and store sulfur are the main features which define Beggiatoa and its close relative Thioploca as filamentous colorless sulfur bacteria, in contrast to other filamentous bacteria like cyanobacteria and the non-sulfur-oxidizing Cytophaga and Flexibacter. PDF. Another defining feature is the ability to store nitrate inside the vacuoles of the wide marine species' cells. 16S rRNA sequences base studies inferred that this characteristic is shared between members of a monophyletic clade nested in the Beggiatoa genera; this clade also includes members of Thioploca and Thiomargarita, both presenting only slight differences with Beggiatoas: whereas the former grows sharing a common slime sheath, the latter has not conserved filamentous growth and forms chains of rounded cells. Since the phylogenic history do not reflect the nomenclature, there is a need for a new denomination of genera and species. The Neo-type strain is the B18LB and it settled the criteria for identification of the freshwater species Beggiatoa alba.
Genetics Because of the lack of a pure culture, little is known about the genetics of Beggiatoa. Beggiatoa alba has a GC content between 40 and 42.7 mol%, two or three similar plasmids, and a genome size of about 3 Megabase (Mbp) (strain B18LD). In a study on Beggiatoa genome sequences obtained from two single filaments of a vacuolated strain, optical mapping showed that the genome size was about 7.4 Mbp; pathways for sulfur oxidation, nitrate and oxygen respiration, and CO2 fixation were detected, confirming its chemolithoautotrophic physiology. Furthermore, comparative genomics indicated horizontal gene transfer between Beggiatoa and Cyanobacteria of storage, metabolic, and gliding abilities.
Morphology and motility
Beggiatoa spp. can be divided into three morphological categories (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.
Although they are Gram-negative bacteria, Beggiatoa show unusual cell-wall and membrane organization. A variable number of further membranes that cover the peptidoglycan layer are sometimes present. Their presence may be due to the harsh conditions in which some of these organisms live. Intracellular granules can also be covered by membranous structures. In addition to sulfur granules, Beggiatoa cells often contain granules of polyhydroxybutyrate and polyphosphate. Large marine vacuolated Beggiatoa commonly have cells with a narrow cytoplasm surrounding a large central vacuole used to store nitrate.
Beggiatoa move via gliding motility, using the excretion of mucus. The exact mechanisms of this gliding motility are unknown. 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. Beggiatoa gliding motility is induced via chemotaxis, which allows filaments to direct themselves away from high oxygen, sulfide, and light levels. 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.
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.
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.
Metabolism Beggiatoa group is mainly composed by chemolithotrophic, sulfide-oxidizing bacteria. However, the range of possible metabolic pathways is very diversified, varying from the heterotrophy to the chemolithoautotrophy. Because of this huge variability the diverse bacteria of this genus can differ greatly from each other.
Carbon metabolism In Beggiatoa group are present both autotrophic and heterotrophic metabolisms. Autotrophic Beggiatoa carry out the CO2 fixation through the Calvin cycle and the employment of the RuBisCO enzyme. The latter shows different regulation levels in obligated and facultative autotrophs. For instance, in the obligately autotrophic strain MS-81-1c RuBisCO cannot be repressed, while in the facultatively autotrophic strain MS-81-6 it is tightly regulated to switch from autotrophic to heterotrophic growth and vice versa. Beside the autotrophic strains, most of the freshwater Beggiatoa strains are heterotrophic, requiring organic substrates for growth. Specifically, many of them can be considered mixotrophs, because they grow heterotrophically, oxidizing organic compounds, but they can also use sulfide or other reduced sulfur compounds as electron donors. By this strategy, the organic carbon skeletons are saved for the purpose of increasing biomass and the CO2 autotrophic fixation is not required. Mixotrophy has been suspected to be the trophic modality for many freshwater strains, but it has only been found in one marine strain of Beggiatoa, MS-81-6. Also a metabolic pathway of C-1 compounds utilization has been revealed in Beggiatoa leptomitoformis strain D-402, through comprehensive analysis of its genomic, biochemistry, physiology and molecular biology.
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).
Sulfur metabolism One of the defining features of the genus Beggiatoa is the production of intracellular inclusions of sulfur resulting from the oxidation of reduced sulfur sources (e.g. hydrogen sulfide). In autotrophic Beggiatoa, sulfide is a source of energy and electrons for carbon fixation and growth. The oxidation of sulfide can be aerobic or anaerobic, in fact it can be coupled with the reduction of oxygen or with the reduction of nitrate. Sulfur produced by the oxidation of sulfide is stored into internal globules and can be used when the concentration of sulfide decreases. Thus, the temporarily storing of elemental sulfur (S0) increase the adaptability of an organism and its tolerance to changes in the concentrations of sulfide and oxygen.
Sulfide aerobic oxidation: H2S + 1/2O2 -> S^0 + H2O
Sulfide anaerobic oxidation: 4H2S + NO3^- + 2H+ -> 4S^0 + NH4^+ + 3H2O
There are some cases of chemoorganotrophy, too. For instance, the strain Beggiatoa sp. 35Flor usually do an aerobic respiration coupled with the oxidation of sulfide, but in anoxic condition a different type of respiration is activated. The energy is gained chemoorganotrophically from oxidation of PHA (polyhydroxyalkanoates), organic compounds previously synthesized through CO2 fixation during chemolithotrophic growth on oxygen and sulfide. In this case electron acceptor is the sulfur stored into the cell, so the final product is hydrogen sulfide.
Anaerobic respiration: PHA + S^0 -> CO2 + H2S
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.
Hydrogen oxidation: H2 + S^0 -> H2S
Phosphorus metabolism