Cyanobiont

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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. [1] They can reside within extracellular or intracellular structures of the host. [2] 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. [2] The most well-known plant-associated cyanobionts belong to the genus Nostoc . [3] 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. [4] 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. [4] Although there are many documented symbioses between cyanobacteria and marine organisms, little is known about the nature of many of these symbioses. [5] The possibility of discovering more novel symbiotic relationships is apparent from preliminary microscopic observations. [5]

Contents

Currently, cyanobionts have been found to form symbiosis with various organisms in marine environments such as diatoms, dinoflagellates, sponges, protozoans, Ascidians, Acadians, and Echiuroid worms, many of which have significance in maintaining the biogeochemistry of both open ocean and coastal waters. [5] Specifically, symbioses involving cyanobacteria are mostly mutualistic, in which the cyanobionts are responsible for nutrient provision to the host in exchange for attaining high structural-functional specialization. [2] Most cyanobacteria-host symbioses are found in oligotrophic areas where limited nutrient availability may limit the ability of the hosts to acquire carbon (DOC), in the case of heterotrophs and nitrogen in the case of phytoplankton, although a few occur in nutrient-rich areas such as mudflats. [5]

Role in symbiosis

Cyanobionts play a variety of roles in their symbiotic relationships with the host organism. [2] [4] [5] They function primarily as nitrogen- and carbon-fixers. However, they can also be involved in metabolite exchange, as well as in provision of UV protection to their symbiotic partners, since some can produce nitrogen-containing compounds with sunscreen-like properties, such as scytonemin and amino acids similar to mycosporin. [2]

By entering into a symbiosis with nitrogen-fixing cyanobacteria, organisms that otherwise cannot inhabit low-nitrogen environments are provided with adequate levels of fixed nitrogen to carry out life functions. [4] Providing nitrogen is a common role of cyanobionts in many symbiotic relationships, especially in those with photosynthetic hosts. [2] [4] [5] Formation of an anaerobic envelope (heterocyst) to prevent nitrogenase from being irreversibly damaged in the presence of oxygen is an important strategy employed by nitrogen-fixing cyanobacteria to carry out fixation of di-nitrogen in the air, via nitrogenase, into organic nitrogen that can be used by the host. [6] To keep up with the large nitrogen demand of both the symbiotic partner and itself, cyanobionts fix nitrogen at a higher rate, as compared to their free-living counterparts, by increasing the frequency of heterocyst formation. [2]

Cyanobacteria are also photosynthetically active and can therefore meet carbon requirements independently. [7] In symbioses involving cyanobacteria, at least one of the partners must be photoautotrophic in order to generate sufficient amounts of carbon for the mutualistic system. [2] This role is usually allocated to cyanobionts in symbiotic relationships with non-photosynthetic partners such as marine invertebrates. [7]

Maintenance of successful symbioses

In order to maintain a successful symbiosis following host infection, cyanobacteria need to match their life cycles with those of their hosts’. [8] In other words, cyanobacterial cell division must be done at a rate matching their host in order to divide at similar times. As free living organisms, cyanobacteria typically divide more frequently compared to eukaryotic cells, but as symbionts, cyanobionts slow down division times so they do not overwhelm their host. [8] It is unknown how cyanobionts are able to adjust their growth rates, but it is not a result of nutrient limitation by the host. Instead, cyanobionts appear to limit their own nutrient uptake in order to delay cell division, while the excess nutrients are diverted to the host for uptake. [8]

As the host continues to grow and reproduce, the cyanobiont will continue to infect and replicate in the new cells. This is known as vertical transmission, where new daughter cells of the host will be quickly infected by the cyanobionts in order to maintain their symbiotic relationship. This is most commonly seen when hosts reproduce asexually. [9] In the water fern Azolla , cyanobacteria colonize the cavities within dorsal leaves. [8] As new leaves form and begin to grow, the new leaf cavities that develop will quickly become colonized by new incoming cyanobacteria. [8]

An alternative mode of transmission is known as horizontal transmission, where hosts acquire new cyanobacteria from the surrounding environment between each host generation. [10] This mode of transmission is commonly seen when hosts reproduce sexually, as it tends to increase the genetic diversity of both host and cyanobiont. [9] Hosts that use horizontal transmission in order to obtain cyanobacteria will typically acquire a large and diverse cyanobiont population. [9] This may be used as a survival strategy in open oceans as indiscriminate uptake of cyanobacteria may guarantee capture of appropriate cyanobionts for each successive generation. [10]

Genetic modifications within host

Following infection and establishment of an endosymbiotic relationship, the new cyanobionts will no longer be free living and autonomous, but rather begin to dedicate their physiological activities in tandem with their hosts'. [11] Over time and evolution, the cyanobiont will begin to lose portions of their genome in a process known as genome erosion. As the relationship between the cyanobacteria and host evolves, the cyanobiont genome will develop signs of degradation, particularly in the form of pseudogenes. [11] A genome undergoing reduction will typically have a large proportion of pseudogenes and transposable elements dispersed throughout the genome. [11] Furthermore, cyanobacteria involved in symbiosis will begin to accumulate these mutations in specific genes, particularly those involved in DNA repair, glycolysis, and nutrient uptake. [11] These gene sets are critical for organisms that live independently, however as cyanobionts living in symbiosis with their hosts, there may not be any evolutionary need to continue maintaining the integrity of these genes. As the major function of a cyanobiont is to provide their host with fixed nitrogen, genes involved in nitrogen fixation or cell differentiation are observed to remain relatively untouched. [11] This may suggest that cyanobacteria involved in symbiotic relationships can selectively stream line their genetic information in order to best perform their functions as cyanobiont-host relationships continue to evolve over time. [11]

Examples of symbioses

Cyanobacteria have been documented to form symbioses with a large range of eukaryotes in both marine and terrestrial environments. Cyanobionts provide benefit through dissolved organic carbon (DOC) production or nitrogen fixation but vary in function depending on their host. [12] Organisms that depend on cyanobacteria often live in nitrogen-limited, oligotrophic environments and can significantly alter marine composition leading to blooms. [12] [13]

Diatoms

Commonly found in oligotrophic environments, diatoms within the genera Hemiaulus and Rhizosolenia form symbiotic associations with filamentous cyanobacteria in the species Richelia intracellularis. As an endophyte in up to 12 species of Rhizosolenia, R. intracellularis provides fixed nitrogen to its host via the terminally-located heterocyst. [14] Richella-Rhizosolenia symbioses have been found to be abundant within the nitrogen-limited waters of the Central-Pacific Gyre. [15] Several field studies have linked the occurrence of phytoplankton blooms within the gyre to an increase in nitrogen fixation from Richella-Rhizosolenia symbiosis. [14] [15] A dominant organism in warm oligotrophic waters, five species within the genus Hemiaulus receive fixed nitrogen from R. intracellularis. [16] [14] Hemiaulus-Richella symbioses are up to 245 times more abundant than the former, with 80–100% of Hemilalus cells containing the cyanobiont. [17] [18] [19] Nitrogen fixation in the Hemiaulus-Richella symbiosis is 21 to 45 times greater than in the Richella-Rhizosolenia symbiosis within the southwestern Atlantic and Central Pacific Gyre, respectively. [16]

Other genera of diatoms can form symbioses with cyanobacteria; however, their relationships are less known. Nitrogen fixing cyanobacterial symbionts have been found within the diatoms in the genus Epithemia and have been found to possess genes for nitrogen fixation, but have lost genes required for both photosystems and the required pigments to perform photosynthesis. [20] [21] [22]

Dinoflagellates

Cyanobionts of Ornithocercus dinoflagellates Live cyanobionts belonging to Ornithocercus dinoflagellate host consortium (a) O. magnificus with numerous cyanobionts present in the upper and lower girdle lists (black arrowheads) of the cingulum termed the symbiotic chamber. (b) O. steinii with numerous cyanobionts inhabiting the symbiotic chamber. (c) Enlargement of the area in (b) showing two cyanobionts that are being divided by binary transverse fission (white arrows). Cyanobacterial symbionts of Ornithocercus dinoflagellate 2.png
Cyanobionts of Ornithocercus dinoflagellates 
Live cyanobionts belonging to Ornithocercus dinoflagellate host consortium
(a) O. magnificus with numerous cyanobionts present in the upper and lower girdle lists (black arrowheads) of the cingulum termed the symbiotic chamber.
(b) O. steinii with numerous cyanobionts inhabiting the symbiotic chamber.
(c) Enlargement of the area in (b) showing two cyanobionts that are being divided by binary transverse fission (white arrows).

Heterotrophic dinoflagellates can form symbioses with cyanobacteria (phaeosomes), most often in tropical marine environments. [12] The function of the cyanobiont depends on its host species. Abundant marine cyanobacteria in the genus Synechococcus form symbionts with dinoflagellates in the genera Ornithocercus, Histionesis and Citharistes , where it is hypothesized to benefit its host through the provision of fixed nitrogen in oligotrophic, subtropical waters. [24] Increased instances of phaeosome symbiosis have been documented in a stratified, nitrogen-limited environment, and living within a host can provide an anaerobic environment for nitrogen fixation to occur. [25] However, there is conflicting evidence of this. One study on phaeosomes in cells of Ornithocercus spp. has provided evidence that symbionts belonging to the genus Synechococcus, supply organic carbon rather than nitrogen, due to the absence of nitrogenase within these cyanobacteria. [26]

Sponges

One hundred species within the classes Calcarea and Demospongiae form symbioses with cyanobacteria in the genera Aphanocapsa, Synechocystis, Oscillatoria and Phormidium . [12] [27] Cyanobacteria benefit their hosts through providing glycerol and organic phosphates through photosynthesis and supply up to half of their required energy and a majority of their carbon budget. [28] Two groups of sponges with photosynthetic symbionts have been described; these are the "cyanosponges" and "phototrophs". Cyanosponges are mixotrophic and therefore obtain energy through heterotrophic feeding as well as photosynthesis. The latter group receives almost all of their energy requirements through photosynthesis, and therefore have a larger surface area in order increase exposure to sunlight. [29] The most common cyanobionts found in sponges belong to the genus Synechococcus with the species Candidatus Synechococcus spongiarum inhabiting a majority of symbiotic sponges within the Caribbean. [30] Another widely distributed species of cyanobacteria Oscillatoria spongeliae is found within the sponge Lamellodysidea herbacea, alongside ten other species. [27] Oscillatoria spongeliae benefits its host by providing carbon as well as a variety of chlorinated amino derivatives, depending on the host strain. [31]

Lichens

Lichens are the result of a symbiosis between a mycobiont and an autotroph, usually green algae or cyanobacteria. About 8% of lichen species contain a cyanobiont, most commonly members of the genus Nostoc as well as the genera Calothrix, Scytonema and Fischerella. All cyanobionts inhabiting lichens contain heterocysts to fix nitrogen, which can be distributed throughout the host in specific regions (heteromerous) or randomly throughout the thallus (homoiomerous). Additionally, some lichen species are tripartite, containing both a cyanobacterial and green algal symbiont. [32]

Bryophytes

Bryophytes are non-vascular plants encompassing mosses, liverworts, and hornworts, which most often form symbioses with members from the cyanobacterial genus Nostoc . [33] Depending on the host, the cyanobiont can be inside (endophytic) or outside the host (epiphytic). [33] In mosses, cyanobacteria are major nitrogen fixers and grow mostly epiphytically, aside from two species of Sphagnum which protect the cyanobiont from an acidic-bog environment. [34] In terrestrial Arctic environments, cyanobionts are the primary supplier of nitrogen to the ecosystem whether free-living or epiphytic with mosses. [35] Cyanobacterial associations with liverworts are rare, with only four of 340 genera of liverworts harbouring symbionts. [33] Two of the genera, Marchantia and Porella, are epiphytic, while the genera Blasia and Cavicularia are endophytic. [36] In hornworts however, endophytic cyanobionts have been described in more than triple the number of genera relative to liverworts. [37] Bryophytes and their cyanobacterial symbionts possess different structures depending on the nature of the symbiosis. [36] For instance, colonies of cyanobacterial symbionts in the liverwort Blasia spp. are present as auricles (small dots) between the inner and outer papillae near the ventral surface of the liverworts; whereas, cyanobionts in the hornworts Anthoceros and Phaeoceros are present within the thallus', in specialized slime cavities. [33] However, cyanobacteria first must locate and physically interact with their host in order to form a symbiotic relationship. Members of the cyanobacterial genus Nostoc can become motile through the use of hormogonia, while the host plant excretes chemicals to guide the cyanobacteria via chemotaxis. [33] For instance, liverworts in the genus Blasia can secrete HIF, a strong chemo-attractant for nitrogen-starved and symbiotic cyanobacteria. Cells of Nostoc punctiforme , which have been shown to possess genes encoding proteins that complement chemotaxis-related proteins within flowering plants belonging to the genus Gunnera . [38] [39]

Ascidians

Filamentous cyanobacteria within the genera Synechocystis and Prochloron has been found within the tunic cavity of didemnid sea squirts. The symbiosis is proposed to have originated through the intake of a combination of sand and cyanobacteria which eventually proliferated. [40] The hosts benefit from receiving fixed carbon from the cyanobiont while the cyanobiont may benefit by protection from harsh environments. [40] [41]

Echiuroid worms

Little is known about the symbiotic relationship between echiuroid worms and cyanobacteria. Unspecified cyanobacteria have been found within the subepidermal connective tissue of the worms Ikedosoma gogoshimense and Bonellia fuliginosa. [42]

Coral

Unicellular and symbiotic cyanobacteria were discovered in cells of coral belonging to the species Montastraea cavernosa from Caribbean Islands. These cyanobionts coexisted within the symbiotic dinoflagellates zooxanthellae within the corals, and produce the nitrogen-fixing enzyme nitrogenase. [43] Details on the interaction of the symbionts with their hosts remains unknown.

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 an organism that lives within the body or cells of another organism. Typically the two organisms are in a mutualistic relationship. 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 dinitrogen is converted into ammonia. It occurs both biologically and abiologically in chemical industries. Biological nitrogen fixation or diazotrophy is catalyzed by enzymes called nitrogenases. These enzyme complexes are encoded by the Nif genes and contain iron, often with a second metal.

<span class="mw-page-title-main">Symbiosis</span> Close, long-term biological interaction between distinct organisms (usually species)

Symbiosis is any type of a close and long-term biological interaction, between two organisms of different species. The two organisms, termed symbionts, can be either in a mutualistic, a commensalistic, or a parasitic relationship. In 1879, Heinrich Anton de Bary defined symbiosis as "the living together of unlike organisms".

<span class="mw-page-title-main">Cyanobacteria</span> Phylum of photosynthesising prokaryotes

Cyanobacteria, also called Cyanobacteriota or Cyanophyta, are a phylum of autotrophic gram-negative bacteria that can obtain biological energy via oxygenic photosynthesis. The name "cyanobacteria" refers to their bluish green (cyan) color, which forms the basis of cyanobacteria's informal common name, blue-green algae, although as prokaryotes they are not scientifically classified as algae.

<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 atmospheric nitrogen (N2) in the atmosphere into bioavailable forms such as ammonia.

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.

<span class="mw-page-title-main">Bacterioplankton</span> Bacterial component of the plankton that drifts in the water column

Bacterioplankton refers to the bacterial component of the plankton that drifts in the water column. The name comes from the Ancient Greek word πλανκτος, meaning "wanderer" or "drifter", and bacterium, a Latin term coined in the 19th century by Christian Gottfried Ehrenberg. They are found in both seawater and freshwater.

<i>Ornithocercus</i> Genus of single-celled organisms

Ornithocercus is a genus of planktonic dinoflagellate that is known for its complex morphology that features considerable lists growing from its thecal plates, giving an attractive appearance. Discovered in 1883, this genus has a small number of species currently categorized but is widespread in tropical and sub-tropical oceans. The genus is marked by exosymbiotic bacteria gardens under its lists, the inter-organismal dynamics of which are a current field of research. As they reside only in warm water, the genus has been used as a proxy for climate change and has potential to be an indicator species for environmental change if found in novel environments.

Candidatus Atelocyanobacterium thalassa, also referred to as UCYN-A, is a nitrogen-fixing 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 1-2 μm 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.

<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.

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.

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

A symbiosome is a specialised compartment in a host cell that houses an endosymbiont in a symbiotic relationship.

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

All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal–microbial relationships were historically explored in single host–symbiont systems. However, new explorations into the diversity of marine microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and a more multi-member microbiome. The potential for microbiomes to influence the health, physiology, behavior, and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment.

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.

<span class="mw-page-title-main">Photosymbiosis</span> Type of symbiotic relationship

Photosymbiosis is a type of symbiosis where one of the organisms is capable of photosynthesis.

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

Sponge microbiomes are diverse communities of microorganisms in symbiotic association with marine sponges as their hosts. These microorganisms include bacteria, archaea, fungi, viruses, among others. The sponges have the ability to filter seawater and recycle nutrients while providing a safe habitat to many microorganisms, which provide the sponge host with fixed nitrogen and carbon, and stimulates the immune system. Together, a sponge and its microbiome form a holobiont, with a single sponge often containing more than 40 bacterial phyla, making sponge microbial environments a diverse and dense community. Furthermore, individual holobionts work hand in hand with other near holobionts becoming a nested ecosystem, affecting the environment at multiple scales.

References

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