Richelia

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Richelia
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Bacteria
Phylum: Cyanobacteria
Class: Cyanophyceae
Order: Nostocales
Family: Nostocaceae
Genus: Richelia
J.Schmidt
Species:
R. intracellularis
Binomial name
Richelia intracellularis
C.H.Ostenfeld ex J.Schmidt, 1901

Richelia is a genus of nitrogen-fixing, filamentous, heterocystous and cyanobacteria. It contains the single species Richelia intracellularis. They exist as both free-living organisms as well as symbionts within potentially up to 13 diatoms distributed throughout the global ocean. As a symbiont, Richelia can associate epiphytically and as endosymbionts within the periplasmic space between the cell membrane and cell wall of diatoms.

Contents

Morphology

Richelia are made up of filaments called trichomes, which are fine hair-like structures that grow out of a myriad of plant species, though their presence as free-living organisms in the marine environment is rare. [1] [2] The number of trichomes Richelia have in each diatom host varies. [3] The trichomes serve the purpose of nitrogen fixation as well as nutrient exchange with host diatoms. [2] The location of Richelia within their various diatom symbionts is not fully known, though it is commonly assumed to be within the diatom's periplasmic space between the plasmalemma and the frustule. [4] [5]   Richelia’s trichomes are made up of two cell types: Heterocyst and Vegetative. The heterocyst is a terminal single cell within which nitrogen fixation occurs, while the rest of the trichome is made up of vegetative cells within which photosynthesis occurs. [2] Some Richelia are made up of many vegetative cells and a terminal heterocyst, while others only contain a terminal heterocyst. [3] The heterocyst is characterized by a thick glycolipid layer which minimizes oxygen's ability to interfere with nitrogen fixation. [2] This is important to Richelia’s function as oxygen can bind to nitrogenase and inhibit the cyanobacteria's nitrogen fixing abilities. [2] The heterocyst does not divide, while the vegetative cells do. [2] Richelia also remain photosynthetically active while within their host diatoms, a behaviour that is somewhat uncommon for similar symbionts. [2]

Symbiosis

Nitrogen fixation and symbiosis

Nitrogen fixation is an important biological process in marine ecosystems. In many regions of the world's oceans the availability of inorganic nitrogen such as nitrate and ammonium limits the rate of photosynthesis (primary productivity). Hence, organisms that form symbiotic relationships with other organisms, often cyanobacteria, to fix nitrogen can be at an advantage. In many cyanobacteria, nitrogen fixation is carried out in specialized cells called heterocysts. Cyanobacteria in the genus Richelia are an example of cyanobacteria are capable of fixing nitrogen gas into organic forms of nitrogen. [6] The organic nitrogen can then be transferred from the cyanobacteria to the diatoms with which they have a symbiotic relationship. [6] Evidence of this nitrogen transfer has been observed multiple times, and this relationship has benefits for both the Richelia cells, which exist inside the diatom, and the diatom itself. For example, the growth of cyanobacteria inside the diatom is increased, releasing carbon dioxide through respiration that can be used by the diatom in photosynthesis. The diatom benefits from enhanced growth as a result of the nitrogen fixed by the cyanobacteria. [1] The presence of this symbiosis can allow diatoms to persist through nitrogen limiting conditions. [1]

Host specificity

Richelia's host specificity and location within a host has been linked to the symbiont genome evolution. Even for taxonomically and morphologically related organisms, preference for diatom hosts and locations within a host differ. [7] These differences usually depend on which host a symbiont typically resides in. For example, in the Hemiaulus and Richelia symbiosis, Richelia resides inside the siliceous frustule of Hemiaulus. Richelia lacks principal nitrogen metabolism enzymes and transporters, such as ammonium transporters, nitrate and nitrite reductases as well as glutamate synthase. It also has a reduced genome, likely following the genome streamlining theory. Hemiaulus has genes that code for all of these enzymes and transporters while lacking the nitrogen fixation genes present in Richelia. This allows the host to complement its symbiont and vice versa, resulting in host specificity that follows host and symbiont genome evolution. [7]

Coordination of gene expression

Day-night cycles potentially play a role in coordination of resource exchange and cell division between a diazotroph and its diatom host. Photosynthesis, nitrogen fixation, and resource acquisition related genes show day-night fluctuations in their expression pattern in Richelia. Nitrogen uptake, metabolism, and carbon transport gene expression in diatom hosts seem to be synchronized with nitrogen fixation gene expression in Richelia, suggesting a coordinated exchange of nitrogen and carbon. Symbiont-host cell physiology is thought to be coordinated and strongly dependent on each other, especially with regard to the time of the day. [8]

Taxonomy

The genus name of Richelia is in honour of Andreas du Plessis de Richelieu (1852–1932), who was a Danish naval officer and businessman who became a Siamese admiral and minister of the Royal Thai Navy. [9]

The genus was circumscribed by Ernst Johannes Schmidt in Vidensk. Meddel. Dansk Naturhist. Foren. Kjøbenhavn 1901 on pages 146 and 149 in 1901.

Species associations

While studies have identified Richelia in up to 13 species, there is a debate as to how many of those identifications were accurate. [10]

The diatom-Richelia symbiotic relationships that are confirmed and most well-known are as follows:

Life cycle

Within diatom hosts

Richelia are most commonly found and best understood within host diatoms. For most of its life cycle within diatoms, the orientation of Richelia cells remains unchanged [15] with the orientation of the terminal heterocyst cell fixed towards the closest diatom valve. [4] [15] This orientation only changes during separation and migration of the Richelia trichomes. [15] This separation and migration is presumed to occur synchronously with growth and division of the host diatom as it produces daughter cells, in order to provide new daughter cells with symbionts. While transfer of the Richelia trichome to daughter cells can occur before division, this method will eventually end as it limits vegetative growth due to the progressive reduction in the size of the host diatom. Within diatoms that are dead or dying, some Richelia cells have enlarged and rounded vegetative cells, some begin to disintegrate and die with their host, and some emerge from a trichome-shaped opening in the diatom frustule and presumably become free-living Richelia . [4]

Free-living

While Richelia cells can exist as free-living organisms in the marine environment, it is rarely observed. Additionally, how diatoms without symbionts are colonized by free-living Richelia is unknown; however, a number of mechanisms have been hypothesized, including Richelia cells entering non-colonized diatoms directly. Also hypothesized is that Richelia cells may be affiliated with auxospore cells, or may enter diatoms during sexual reproduction when the trichome is transported to the auxospore. Richelia cells may also colonize diatoms during instances of vegetative cell enlargement. [4]

Distribution

Cyanobacteria in the genus Richelia are primarily found in symbiotic association with diatoms in nitrogen-limited regions of the ocean. [2] This distribution pattern is attributed to the symbiotic relationship that Richelia forms with different species of diatoms in which they provide diatoms with nitrogen that is otherwise limiting for growth. [2] Similar to other diazotrophs, Richelia cells are in low abundances in productive equatorial regions due to nutrient upwelling and in high abundances in non-productive subtropical areas where low concentrations of nitrate limit the growth of diatoms. [16]

Quantitative analyses of the distribution of Richelia is an emerging field of study. [16] Thus far, many observations have been subject to criticism due to issues of misidentifying hosts and the associated diazotrophs, and demonstrating symbiotic relationships overall. [17]

Global ocean

Richelia are found throughout the Pacific Ocean, the Atlantic Ocean, the Amazon River plume, and the Mediterranean Sea. [16] [18] They follow similar distributions to other diazotrophs including cyanobacteria in the genus Trichodesmium , Candidatus Atelocyanobacterium thalassa (formerly known as UCYN-A), and UCYN-B, which are in high abundance throughout much of the tropical oceans, although the relative abundances of the different taxa varies. [16] The abundance of Richelia cells also varies based on different environmental conditions across regions. [16] Richelia, when compared to other diazotrophs, show lower abundances at deeper depths. [16] Warm, silicate-rich conditions, such as those found in the Amazon River plume, allow for high Richelia growth rates. [16] Richelia cells also decrease in abundance as inorganic nitrogen increases because they are at a competitive disadvantage when nitrate concentrations are high. [16] However, unlike other diazotrophs, Richelia cells do not decrease in abundance when phosphate levels are high. [16] The abundances of Richelia cells also depend on the availability of iron, due to the iron requirements of the enzyme nitrogenase that is needed to fix di-nitrogen gas. [16] Grazing is also a factor that may affect the abundances of diazotrophs throughout different regions in the global ocean. [19]

Mediterranean Sea

Richelia is an endosymbiont with diatoms such as Rhizosolenia spp. and Hemiaulus spp. [18] Richelia is found to be highly correlated with the presence of Hemiaulus spp., and sporadically correlated with the presence of Rhizosolenia spp. [18]  The highest counts of Richelia as sampled in 2006 in the Eastern Mediterranean Sea are 50 heterocysts L−1 in June and October in coastal regions, and 50 heterocysts L−1 in June and November in pelagic regions. [18] These peaks occur during a deepening of the mixed layer depth at each region. [18] Richelia and Hemiaulus hauckii are found together in both coastal and pelagic regions year-round in diurnal and nocturnal sampling, and it is suggested that this symbiotic pair has an evolutionary advantage over other host options for Richelia. [3] [18] Because the Eastern Mediterranean Sea has oligotrophic conditions due to a large transport of nutrients out to the North Atlantic Ocean through the Strait of Gibraltar, Richelia provides important nitrogen fixation capabilities for diatoms they form symbiotic relationships with. Free living Richelia are not considered to be present in the Eastern Mediterranean Sea based on the current sampling experiment results available. In the Eastern Mediterranean Sea water columns, Richelia is the primary diurnal organism with an expression of the nifH gene. A case of allopatric speciation is observed between coastal and pelagic water columns in the Eastern Mediterranean Sea. These two regions have different clades of nifH-expressing cells of Richelia, hypothesized to be due to the restriction of the two regions from each other by a hydrological barrier caused by the sloping of the continental shelf. [18]

Western/Southwestern Pacific Ocean

Richelia have been found as epiphytes to Chaetoceros compressus and to Rhizosolenia clevei in the Western Pacific Ocean. It is hypothesized that Richelia filaments can detach from Rhizosolenia clevei and subsequently become symbionts to Chaetoceros compressus. This is suggested as the Richelia and Chaetoceros compressus symbiosis has been found to follow occurrences of the Richelia and Rhizosolenia clevei symbiosis. [17]

Kuroshio Current

The distribution of Richelia in the Kuroshio Current varies based on the section of the current and the time of year. Physical and hydrographical conditions vary throughout the year in the current and create changes to the growth of bacterial and diatom colonies. Conditions in May limit growth to a more narrow region of the current than in July. The region has low concentrations of nitrate throughout both Spring and Summer, with July seeing the least nitrate levels in surface waters. The number of Richelia filaments per colony of Chaetoceros compressus ranges from 4 to 9 during May to November, reaching a maximum in July. The maximum abundance of the Richelia and Chaetoceros compressus symbiosis occurs in July, at 10 colonies L−1. The maximum abundance of the Richelia and Rhizosolenia clevei symbiosis also occurs in July, at 30 colonies L−1.

Sulu Sea

Symbiosis between Richelia and Chaetoceros compressus has also been observed in the Southern Sulu Sea. This is due to the lower than 0.1 μM nitrogen concentrations in surface waters causing nitrogen limiting conditions. [17]

Indian Ocean

Richelia have been found as epiphytes to Chaetoceros compressus in the Indian Ocean. [17]

Western Tropical Atlantic Ocean

Nitrogen fixation and cyanobacteria-diatom symbiosis occur in the freshwater layer of the Amazon River plume due to low surface nitrate conditions. In these nitrogen limited areas, Richelia can be found in symbiosis with Rhizosolenia clevei and Hemiaulus spp. Richelia symbiosis with H. hauckii is found predominantly in this region with depth as well as throughout the surface. The abundance of the symbiosis between Richelia and H. hauckii is higher further northwest from the Amazon River outflow. A positive correlation can be found between salinity and abundances of Richelia symbioses. [17]

Related Research Articles

<span class="mw-page-title-main">Endosymbiont</span> Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is any organism that lives within the body or cells of another organism most often, though not always, in a mutualistic relationship. This phenomenon is known as endosymbiosis. Examples are nitrogen-fixing bacteria, which live in the root nodules of legumes, single-cell algae inside reef-building corals and bacterial endosymbionts that provide essential nutrients to insects.

Nitrogen fixation is a chemical process by which molecular nitrogen (N
2), which has a strong triple covalent bond, is converted into ammonia (NH
3) or related nitrogenous compounds, typically in soil or aquatic systems but also in industry. The nitrogen in air is molecular dinitrogen, a relatively nonreactive molecule that is metabolically useless to all but a few microorganisms. Biological nitrogen fixation or diazotrophy is an important microbe-mediated process that converts dinitrogen (N2) gas to ammonia (NH3) using the nitrogenase protein complex (Nif).

<span class="mw-page-title-main">Cyanobacteria</span> Phylum of photosynthesising prokaryotes that can produce toxic blooms in lakes and other waters

Cyanobacteria, also called Cyanobacteriota or Cyanophyta, are a phylum of autotrophic gram-negative bacteria that can obtain biological energy via photosynthesis. The name 'cyanobacteria' refers to their color, which similarly forms the basis of cyanobacteria's common name, blue-green algae, although they are not scientifically classified as algae. They appear to have originated in a freshwater or terrestrial environment.

<span class="mw-page-title-main">Rhizobia</span> Nitrogen fixing soil bacteria

Rhizobia are diazotrophic bacteria that fix nitrogen after becoming established inside the root nodules of legumes (Fabaceae). To express genes for nitrogen fixation, rhizobia require a plant host; they cannot independently fix nitrogen. In general, they are gram negative, motile, non-sporulating rods.

<span class="mw-page-title-main">Hormogonium</span> Motile filament of cells formed by some cyanobacteria

Hormogonia are motile filaments of cells formed by some cyanobacteria in the order Nostocales and Stigonematales. They are formed during vegetative reproduction in unicellular, filamentous cyanobacteria, and some may contain heterocysts and akinetes.

<i>Trichodesmium</i> Genus of bacteria

Trichodesmium, also called sea sawdust, is a genus of filamentous cyanobacteria. They are found in nutrient poor tropical and subtropical ocean waters. Trichodesmium is a diazotroph; that is, it fixes atmospheric nitrogen into ammonium, a nutrient used by other organisms. Trichodesmium is thought to fix nitrogen on such a scale that it accounts for almost half of the nitrogen fixation in marine systems globally. Trichodesmium is the only known diazotroph able to fix nitrogen in daylight under aerobic conditions without the use of heterocysts.

<span class="mw-page-title-main">Heterocyst</span>

Heterocysts or heterocytes are specialized nitrogen-fixing cells formed during nitrogen starvation by some filamentous cyanobacteria, such as Nostoc, Cylindrospermum, and Anabaena. They fix nitrogen from dinitrogen (N2) in the air using the enzyme nitrogenase, in order to provide the cells in the filament with nitrogen for biosynthesis.

Diazotrophs are bacteria and archaea that fix gaseous nitrogen in the atmosphere into a more usable form such as ammonia.

<span class="mw-page-title-main">Root nodule</span> Plant part

Root nodules are found on the roots of plants, primarily legumes, that form a symbiosis with nitrogen-fixing bacteria. Under nitrogen-limiting conditions, capable plants form a symbiotic relationship with a host-specific strain of bacteria known as rhizobia. This process has evolved multiple times within the legumes, as well as in other species found within the Rosid clade. Legume crops include beans, peas, and soybeans.

<i>Anabaena</i> Genus of bacteria

Anabaena is a genus of filamentous cyanobacteria that exist as plankton. They are known for nitrogen-fixing abilities, and they form symbiotic relationships with certain plants, such as the mosquito fern. They are one of four genera of cyanobacteria that produce neurotoxins, which are harmful to local wildlife, as well as farm animals and pets. Production of these neurotoxins is assumed to be an input into its symbiotic relationships, protecting the plant from grazing pressure.

Symbiotic bacteria are bacteria living in symbiosis with another organism or each other. For example, rhizobia living in root nodules of legumes provide nitrogen fixing activity for these plants.

<i>Geosiphon</i> Monotypic genus of photosynthetic, non-lichen fungi

Geosiphon is a genus of fungus in the family Geosiphonaceae. The genus is monotypic, containing the single species Geosiphon pyriformis, first described by Kützing in 1849 as Botrydium pyriforme. In 1915, Von Wettstein characterized Geosiphon pyriforme as a multinucleate alga containing endosymbiotic cyanobacteria, although he also noted the presence of chitin, a component of fungal cell walls. In 1933, Knapp was the first to suggest the fungal origin of the species and described it as a lichen with endosymbiotic cyanobacteria. It is the only member of the Glomeromycota known to not form a symbiosis with terrestrial plants in the form of arbuscular mycorrhiza.

Cyanobionts are cyanobacteria that live in symbiosis with a wide range of organisms such as terrestrial or aquatic plants; as well as, algal and fungal species. They can reside within extracellular or intracellular structures of the host. In order for a cyanobacterium to successfully form a symbiotic relationship, it must be able to exchange signals with the host, overcome defense mounted by the host, be capable of hormogonia formation, chemotaxis, heterocyst formation, as well as possess adequate resilience to reside in host tissue which may present extreme conditions, such as low oxygen levels, and/or acidic mucilage. The most well-known plant-associated cyanobionts belong to the genus Nostoc. With the ability to differentiate into several cell types that have various functions, members of the genus Nostoc have the morphological plasticity, flexibility and adaptability to adjust to a wide range of environmental conditions, contributing to its high capacity to form symbiotic relationships with other organisms. Several cyanobionts involved with fungi and marine organisms also belong to the genera Richelia, Calothrix, Synechocystis, Aphanocapsa and Anabaena, as well as the species Oscillatoria spongeliae. Although there are many documented symbioses between cyanobacteria and marine organisms, little is known about the nature of many of these symbioses. The possibility of discovering more novel symbiotic relationships is apparent from preliminary microscopic observations.

CandidatusAtelocyanobacterium thalassa, also referred to as UCYN-A, is a diazotrophic species of cyanobacteria commonly found in measurable quantities throughout the world's oceans and some seas. Members of A. thalassa are spheroid in shape and are 1-2µm in diameter, and provide nitrogen to ocean regions by fixing non biologically available atmospheric nitrogen into biologically available ammonium that other marine microorganisms can use. Unlike many other cyanobacteria, the genome of A. thalassa does not contain genes for RuBisCO, photosystem II, or the TCA cycle. Consequently, A. thalassa lacks the ability to fix carbon via photosynthesis. Some genes specific to the cyanobacteria group are also absent from the A. thalassa genome despite being an evolutionary descendant of this group. With the inability to fix their own carbon, A. thalassa are obligate symbionts that have been found within photosynthetic picoeukaryote algae. Most notably, the UCYN-A2 sublineage has been observed as an endosymbiont in the alga Braarudosphaera bigelowii with a minimum of 1-2 endosymbionts per host. A. thalassa fixes nitrogen for the algae, while the algae provide carbon for A. thalassa through photosynthesis. There are many sublineages of A. thalassa that are distributed across a wide range of marine environments and host organisms. It appears that some sublineages of A. thalassa have a preference for oligotrophic ocean waters while other sublineages prefer coastal waters. Much is still unknown about all of A. thalassa's hosts and host preferences.

Chaetoceros pseudocurvisetus is a marine diatom in the genus Chaetoceros. It is an important primary producer in the oceans. C. pseudocurvisetus forms resting spores and resting cells, particularly in the absence of essential nutrients.

Raphidiopsis raciborskii is a freshwater cyanobacterium.

<span class="mw-page-title-main">Marine microbial symbiosis</span>

Microbial symbiosis in marine animals was not discovered until 1981. In the time following, symbiotic relationships between marine invertebrates and chemoautotrophic bacteria have been found in a variety of ecosystems, ranging from shallow coastal waters to deep-sea hydrothermal vents. Symbiosis is a way for marine organisms to find creative ways to survive in a very dynamic environment. They are different in relation to how dependent the organisms are on each other or how they are associated. It is also considered a selective force behind evolution in some scientific aspects. The symbiotic relationships of organisms has the ability to change behavior, morphology and metabolic pathways. With increased recognition and research, new terminology also arises, such as holobiont, which the relationship between a host and its symbionts as one grouping. Many scientists will look at the hologenome, which is the combined genetic information of the host and its symbionts. These terms are more commonly used to describe microbial symbionts.

<i>Crocosphaera watsonii</i> Species of bacterium

Crocosphaera watsonii is an isolate of a species of unicellular diazotrophic marine cyanobacteria which represent less than 0.1% of the marine microbial population. They thrive in offshore, open-ocean oligotrophic regions where the waters are warmer than 24 degrees Celsius. Crocosphaera watsonii cell density can exceed 1,000 cells per milliliter within the euphotic zone; however, their growth may be limited by the concentration of phosphorus. Crocosphaera watsonii are able to contribute to the oceanic carbon and nitrogen budgets in tropical oceans due to their size, abundance, and rapid growth rate. Crocosphaera watsonii are unicellular nitrogen fixers that fix atmospheric nitrogen to ammonia during the night and contribute to new nitrogen in the oceans. They are a major source of nitrogen to open-ocean systems. Nitrogen fixation is important in the oceans as it not only allows phytoplankton to continue growing when nitrogen and ammonium are in very low supply but it also replenishes other forms of nitrogen, thus fertilizing the ocean and allowing more phytoplankton growth.

Trichodesmium thiebautii is a cyanobacteria that is often found in open oceans of tropical and subtropical regions and is known to be a contributor to large oceanic surface blooms. This microbial species is a diazotroph, meaning it fixes nitrogen gas (N2), but it does so without the use of heterocysts. T. thiebautii is able to simultaneously perform oxygenic photosynthesis. T. thiebautii was discovered in 1892 by M.A. Gomont. T. thiebautii are important for nutrient cycling in marine habitats because of their ability to fix N2, a limiting nutrient in ocean ecosystems.

Some types of lichen are able to fix nitrogen from the atmosphere. This process relies on the presence of cyanobacteria as a partner species within the lichen. The ability to fix nitrogen enables lichen to live in nutrient-poor environments. Lichen can also extract nitrogen from the rocks on which they grow.

References

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