A symbiosome is a specialised compartment in a host cell that houses an

endosymbiont 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. (The term endosymbiosis is from the Greek: ἔνδον ''endon'' "withi ...

in a symbiotic relationship. The term was first used in 1983 to describe the vacuole structure in the symbiosis between the animal host the '' Hydra'', and the endosymbiont ''

Chlorella ''Chlorella'' is a genus of about thirteen species of single- celled green algae belonging to the division Chlorophyta. The cells are spherical in shape, about 2 to 10 μm in diameter, and are without flagella. Their chloroplasts contain t ...

''. Symbiosomes are also seen in other

cnidaria Cnidaria () is a phylum under kingdom Animalia containing over 11,000 species of aquatic animals found both in Fresh water, freshwater and Marine habitats, marine environments, predominantly the latter. Their distinguishing feature is cnidocyt ...

dinoflagellate The dinoflagellates (Greek δῖνος ''dinos'' "whirling" and Latin ''flagellum'' "whip, scourge") are a monophyletic group of single-celled eukaryotes constituting the phylum Dinoflagellata and are usually considered algae. Dinoflagellates are ...

symbioses, including those found in

coral Corals are marine invertebrates within the class Anthozoa of the phylum Cnidaria. They typically form compact colonies of many identical individual polyps. Coral species include the important reef builders that inhabit tropical oceans and secre ...

algal Algae ( , ; : alga ) are any of a large and diverse group of photosynthetic, eukaryotic organisms. The name is an informal term for a polyphyletic grouping that includes species from multiple distinct clades. Included organisms range from un ...

symbioses. In 1989 the concept was applied to the similar structure found in the

nitrogen-fixing Nitrogen fixation is a chemical process by which molecular nitrogen (), with a strong triple covalent bond, in the air is converted into ammonia () or related nitrogenous compounds, typically in soil or aquatic systems but also in industry. At ...

root nodule 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 know ...

s of certain plants. The symbiosome in the root nodules has been much more successfully researched due in part to the complexity of isolating the symbiosome membrane in animal hosts. The symbiosome in a

cell in a

plant Plants are predominantly Photosynthesis, photosynthetic eukaryotes of the Kingdom (biology), kingdom Plantae. Historically, the plant kingdom encompassed all living things that were not animals, and included algae and fungi; however, all curr ...

is an organelle-like structure that has formed in a symbiotic relationship with

nitrogen-fixing bacteria Nitrogen fixation is a chemical process by which molecular nitrogen (), with a strong triple covalent bond, in the air is converted into ammonia () or related nitrogenous compounds, typically in soil or aquatic systems but also in industry. At ...

. The plant symbiosome is unique to those plants that produce root nodules. The majority of such symbioses are made between

legume A legume () is a plant in the family Fabaceae (or Leguminosae), or the fruit or seed of such a plant. When used as a dry grain, the seed is also called a pulse. Legumes are grown agriculturally, primarily for human consumption, for livestock fo ...

s and

diazotroph Diazotrophs are bacteria and archaea that fix gaseous nitrogen in the atmosphere into a more usable form such as ammonia. A diazotroph is a microorganism that is able to grow without external sources of fixed nitrogen. Examples of organisms that ...

ic '' Rhizobia''

bacteria Bacteria (; singular: bacterium) are ubiquitous, mostly free-living organisms often consisting of one biological cell. They constitute a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria were am ...

. The ''rhizobia-legume'' symbioses are the most studied due to the importance in agriculture. Each symbiosome in a root nodule cell encloses a single rhizobium that differentiates into a bacteroid. However, in some cases a symbiosome may house several bacteroids. The symbiosome membrane, or peribacteroid membrane, surrounds the bacteroid membrane, separated by a symbiosome space. This unit provides an inter-kingdom, micro-environment for the production of nitrogen for the plant, and the receipt of

malate Malic acid is an organic compound with the molecular formula . It is a dicarboxylic acid that is made by all living organisms, contributes to the sour taste of fruits, and is used as a food additive. Malic acid has two stereoisomeric forms ...

for energy for the bacteroid.

History

The concept of the symbiosome was first described in 1983, by Neckelmann and Muscatine, as seen in the symbiotic relationship between ''

'' ( a class of

green algae The green algae (singular: green alga) are a group consisting of the Prasinodermophyta and its unnamed sister which contains the Chlorophyta and Charophyta/ Streptophyta. The land plants ( Embryophytes) have emerged deep in the Charophyte alg ...

, and '' Hydra'' a

cnidarian Cnidaria () is a phylum under kingdom Animalia containing over 11,000 species of aquatic animals found both in Fresh water, freshwater and Marine habitats, marine environments, predominantly the latter. Their distinguishing feature is cnidocyt ...

animal host. Until then it had been described as a

vacuole A vacuole () is a membrane-bound organelle which is present in plant and fungal cells and some protist, animal, and bacterial cells. Vacuoles are essentially enclosed compartments which are filled with water containing inorganic and organic ...

. A few years later in 1989, Lauren Roth with Gary Stacey as well as

Robert B Mellor Robert B. Mellor (born in Yorkshire, UK) is a British scientist probably best known for his 1989 "unified vacuole theory", although also made significant contributions to environmental technology and to our understanding of the workings of the t ...

applied this concept to the

unit seen in the plant root nodule, previously called an infection

. This has since engendered a great deal of research, one result of this has been the provision of a more detailed description of the symbiosome (peribacteroid) membrane, as well as comparisons with similar structures in Vesicular Arbuscular Mycorrhizal symbioses in plants. In the animal models, the symbiosome has a more complex arrangement of membranes, such that it has proved difficult to isolate, purify and study.

Structure and formation

A symbiosome is formed as a result of a complex and coordinated interaction between the symbiont host and the

. At the point of entry into a symbiont host cell, part of the cell's

membrane A membrane is a selective barrier; it allows some things to pass through but stops others. Such things may be molecules, ions, or other small particles. Membranes can be generally classified into synthetic membranes and biological membranes. ...

envelops the endosymbiont and breaks off into the

cytoplasm In cell biology, the cytoplasm is all of the material within a eukaryotic cell, enclosed by the cell membrane, except for the cell nucleus. The material inside the nucleus and contained within the nuclear membrane is termed the nucleoplasm. ...

as a discrete unit, an organelle-like

called the symbiosome. This is an

endocytosis Endocytosis is a cellular process in which substances are brought into the cell. The material to be internalized is surrounded by an area of cell membrane, which then buds off inside the cell to form a vesicle containing the ingested material. E ...

-like process that forms a symbiosome rather than an

endosome Endosomes are a collection of intracellular sorting organelles in eukaryotic cells. They are parts of endocytic membrane transport pathway originating from the trans Golgi network. Molecules or ligands internalized from the plasma membrane c ...

. In plants this process is unique. The symbiosome membrane is separated from the endosymbiont membrane by a space known as the symbiosome space, which allows for the exchange of solutes between the symbionts. In the plant

the symbiosome membrane is also called the peribacteroid membrane.

In the plant

In the

- rhizobia symbioses the symbiosome is the nitrogen-fixing unit in the plant, formed by an interaction of plant and bacterial signals, and their cooperation. The legumes are protein-rich, and have a high demand for nitrogen that is usually available from

nitrate Nitrate is a polyatomic ion with the chemical formula . Salts containing this ion are called nitrates. Nitrates are common components of fertilizers and explosives. Almost all inorganic nitrates are soluble in water. An example of an insoluble ...

s in the soil. When these are scarce the plant secretes

flavonoid Flavonoids (or bioflavonoids; from the Latin word ''flavus'', meaning yellow, their color in nature) are a class of polyphenolic secondary metabolites found in plants, and thus commonly consumed in the diets of humans. Chemically, flavonoids ...

s that attract free-living

ic (nitrogen-fixing) rhizobia to their

root hair Root hair, or absorbent hairs, are outgrowths of epidermal cells, specialized cells at the tip of a plant root. They are lateral extensions of a single cell and are only rarely branched. They are found in the region of maturation, of the root. Root ...

s. In turn the bacteria release

Nod factor Nod factors (nodulation factors or NF), are signaling molecules produced by soil bacteria known as rhizobia in response to flavonoid exudation from plants under nitrogen limited conditions. Nod factors initiate the establishment of a symbiotic r ...

s that stimulate the infection process in the plant. To enable infection the tip of the root hair curls over the rhizobia and by an inward growth produces an infection thread to carry the endosymbionts into the cortical cells. At the same time the cortical cells divide to produce the tough

s that will house and protect the bacteria. The bacterial production of

extracellular polymeric substance Extracellular polymeric substances (EPSs) are natural polymers of high molecular weight secreted by microorganisms into their environment. EPSs establish the functional and structural integrity of biofilms, and are considered the fundamental comp ...

(EPS) is seen to be necessary for enabling infection. The rhizobia infect the plant in large numbers, only seen to be actively dividing at the tip of the injection thread, where they are released into the cells inside symbiosomes. The symbiosome is formed as a result of an endocytosis-like process that produces an endosome. Typically endosomes target to

lysosome A lysosome () is a membrane-bound organelle found in many animal cells. They are spherical vesicles that contain hydrolytic enzymes that can break down many kinds of biomolecules. A lysosome has a specific composition, of both its membrane ...

s, but the symbiosome re-targets the host-cell proteins. The changes in the plant needed to form the infection thread, the increased division of the cortical cells, the formation of the root nodule, and symbiosome, are brought about by dynamic changes in the

actin Actin is a protein family, family of Globular protein, globular multi-functional proteins that form microfilaments in the cytoskeleton, and the thin filaments in myofibril, muscle fibrils. It is found in essentially all Eukaryote, eukaryotic cel ...

cytoskeleton The cytoskeleton is a complex, dynamic network of interlinking protein filaments present in the cytoplasm of all cells, including those of bacteria and archaea. In eukaryotes, it extends from the cell nucleus to the cell membrane and is comp ...

. Filamentous actin (F-actin) channels the elongation of the injection threads and short F-actin fragments are dotted around the symbiosome membrane. The bacteria are released as injection drops into the host root nodule cells where the plasma membrane encloses them in the organelle-like structure of the symbiosome. In most plants a symbiosome encloses a single endosymbiont bacterium but some types may contain more than one. A negative feedback loop called the autoregulation of nodulation works to balance the need for nitrogen and thus the formation of nodules.

Differentiation

The outer host-cell derived symbiosome membrane encloses a space called the symbisome space or the peribacteroid space that surrounds the endosymbiont. In order for the symbiosome to be established as a nitrogen-fixing unit the enclosed bacterium has to be terminally differentiated into a morphologically changed bacteroid. The bacterium in the soil is free-living and motile. In the symbiosome it has to change its

gene expression Gene expression is the process by which information from a gene is used in the synthesis of a functional gene product that enables it to produce end products, protein or non-coding RNA, and ultimately affect a phenotype, as the final effect. ...

to adapt to a non-motile, non-reproductive form as the bacteroid. This change is noted by an increase in the size of the bacterium and its elongation. The bacterial membrane is also made permeable. The process of differentiation is plant-driven using

peptide Peptides (, ) are short chains of amino acids linked by peptide bonds. Long chains of amino acids are called proteins. Chains of fewer than twenty amino acids are called oligopeptides, and include dipeptides, tripeptides, and tetrapeptides. ...

s known as ''nodule specific cysteine-rich peptides'' (NCR peptides). NCRs are

antimicrobial peptides Antimicrobial peptides (AMPs), also called host defence peptides (HDPs) are part of the innate immune response found among all classes of life. Fundamental differences exist between prokaryotic and eukaryotic cells that may represent targets for a ...

that are similar to the

defensin Defensins are small cysteine-rich cationic proteins across cellular life, including vertebrate and invertebrate animals, plants, and fungi. They are host defense peptides, with members displaying either direct antimicrobial activity, immune sig ...

peptides used in mammals in response to invading pathogens. The NCRs are targeted to the symbiosome where they induce differentiation of the bacterium to the bacteroid. A major effect of NCR targeting is to limit the reproductive ability of the endosymbiont. These changes are controlled, since the bacterium is not killed as a result of exposure to the NCRs. Some of that control comes from the bacterium itself. In order to survive the NCR activities, the bacteria need to produce a protein called BacA. In addition the

lipopolysaccharide Lipopolysaccharides (LPS) are large molecules consisting of a lipid and a polysaccharide that are bacterial toxins. They are composed of an O-antigen, an outer core, and an inner core all joined by a covalent bond, and are found in the outer ...

produced by the bacteria is modified by an unusual

fatty acid In chemistry, particularly in biochemistry, a fatty acid is a carboxylic acid with an aliphatic chain, which is either saturated or unsaturated. Most naturally occurring fatty acids have an unbranched chain of an even number of carbon atoms, ...

that also gives protection against environmental stresses. These defensive measures help the differentiation process and ensures their survival as bacteroids. Some strains of rhizobia produce a

peptidase A protease (also called a peptidase, proteinase, or proteolytic enzyme) is an enzyme that catalyzes (increases reaction rate or "speeds up") proteolysis, breaking down proteins into smaller polypeptides or single amino acids, and spurring the ...

that degrades the NCRs.

Nitrogen-fixing unit

The established bacteroid is able to fix nitrogen into a chemically usable form of ammonium for the plant. This is an energy-demanding process fuelled by the plant's carbohydrates. Transport vesicles form in the symbiosome membrane allowing the passage of ammonium into the symbiosome space from the bacteroid, and the passage of plant nutrients to the bacteroid. The rhizobia infect the plant in large numbers where they are released into the cells inside symbiosomes. They are protected by the tough structure of the root nodule.

In the animal

The most well studied symbiosis involving an animal host is that between the

and the

s, most commonly the single-celled

zooxanthellae Zooxanthellae is a colloquial term for single-celled dinoflagellates that are able to live in symbiosis with diverse marine invertebrates including demosponges, corals, jellyfish, and nudibranchs. Most known zooxanthellae are in the genus '' ...

. The symbiosis of the ''

''–'' Hydra'' first described the ''symbiosome''. The

Zoanthus robustus ''Zoanthus'' is a genus of anthozoans in the family Zoanthidae. It is the type genus for its family and order. Species The following species are recognized in the genus ''Zoanthus'':(2018). Zoanthus Lamarck, 1801. Accessed through: World Regis ...

'' has been used as a model organism to study the symbiosis with its microsymbiont

species of ''

Symbiodinium : ''This is about the genus sometimes called Zoox. For the company, see Zoox (company)'' ''Symbiodinium'' is a genus of dinoflagellates that encompasses the largest and most prevalent group of endosymbiotic dinoflagellates known. These unicellul ...

'', with a focus on the symbiosome and its membranes. Methods for isolating the symbiosome membranes have been looked for – the symbiont in the animal host has a multilayered membrane complex which has proved resistant to disruption making their isolation difficult. The endosymbiont dinoflagellates are used for their ability to photosynthesise and provide energy, giving the host cnidarians such as

s, and

anemone ''Anemone'' () is a genus of flowering plants in the buttercup family Ranunculaceae. Plants of the genus are commonly called windflowers. They are native to the temperate and subtropical regions of all continents except Australia, New Zealand ...

s, plant properties. Free-living dinoflagellates are ingested into the gastrodermal cells of the host, and their symbiosome membrane is derived from the host cell. The process of symbiosome formation is often seen in the animal host to be that of

phagocytosis Phagocytosis () is the process by which a cell uses its plasma membrane to engulf a large particle (≥ 0.5 μm), giving rise to an internal compartment called the phagosome. It is one type of endocytosis. A cell that performs phagocytosis i ...

, and it is hypothesised that the symbiosome is a

phagosome In cell biology, a phagosome is a vesicle formed around a particle engulfed by a phagocyte via phagocytosis. Professional phagocytes include macrophages, neutrophils, and dendritic cells (DCs). A phagosome is formed by the fusion of the cell me ...

that has been subject to early arrest.

Similar structures

A similar structure to the symbiosome is the

parasitophorous vacuole The parasitophorous vacuole (PV) is a structure produced by apicomplexan parasites in the cells of its host. The PV allows the parasite to develop while protected from the phagolysosomes of the host cell. The PV is a bubble-like compartment ma ...

formed within host cells infected by apicomplexan

parasites Parasitism is a close relationship between species, where one organism, the parasite, lives on or inside another organism, the host, causing it some harm, and is adapted structurally to this way of life. The entomologist E. O. Wilson ha ...

. The vacuole is derived from the host cell plasma membrane. It is made safe from the host's endolysomal system by modifying-proteins released by the parasite. The parasitophorous vacuole membrane is greatly remodelled by the parasite.

References

{{Reflist Symbiosis Organelles