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

endosymbiont An endosymbiont or endobiont is an organism that lives within the body or cells of another organism. Typically the two organisms are in a mutualism (biology), mutualistic relationship. Examples are nitrogen-fixing bacteria (called rhizobia), whi ...

in a

symbiotic Symbiosis (Ancient Greek : living with, companionship < : together; and ''bíōsis'': living) is any type of a close and long-term biolo ...

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 or colonial green algae of 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 invertebrates found both in fresh water, freshwater and marine environments (predominantly the latter), including jellyfish, hydroid (zoology), hydroids, ...

dinoflagellate The Dinoflagellates (), also called Dinophytes, are a monophyletic group of single-celled eukaryotes constituting the phylum Dinoflagellata and are usually considered protists. Dinoflagellates are mostly marine plankton, but they are also commo ...

symbioses, including those found in

coral Corals are colonial marine invertebrates within the subphylum Anthozoa of the phylum Cnidaria. They typically form compact Colony (biology), colonies of many identical individual polyp (zoology), polyps. Coral species include the important Coral ...

algal Algae ( , ; : alga ) is an informal term for any organisms of a large and diverse group of photosynthetic organisms that are not plants, and includes species from multiple distinct clades. Such organisms range from unicellular microalgae, s ...

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 dinitrogen () is converted into ammonia (). It occurs both biologically and abiological nitrogen fixation, abiologically in chemical industry, chemical industries. Biological nitrogen ...

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 known ...

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 the eukaryotes that form the Kingdom (biology), kingdom Plantae; they are predominantly Photosynthesis, photosynthetic. This means that they obtain their energy from sunlight, using chloroplasts derived from endosymbiosis with c ...

is an organelle-like structure that has formed in a

symbiotic Symbiosis (Ancient Greek : living with, companionship < : together; and ''bíōsis'': living) is any type of a close and long-term biolo ...

relationship with

nitrogen-fixing bacteria Diazotrophs are organisms capable of nitrogen fixation, i.e. converting the relatively inert diatomic nitrogen (N2) in Earth's atmosphere into bioavailable compound forms such as ammonia. Diazotrophs are typically microorganisms such as bacteria ...

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

legume Legumes are plants in the pea family Fabaceae (or Leguminosae), or the fruit or seeds of such plants. When used as a dry grain for human consumption, the seeds are also called pulses. Legumes are grown agriculturally, primarily for human consum ...

s and

diazotroph Diazotrophs are organisms capable of nitrogen fixation, i.e. converting the relatively inert diatomic nitrogen (N2) in Earth's atmosphere into bioavailable compound forms such as ammonia. Diazotrophs are typically microorganisms such as bacteria ...

ic ''

Rhizobia 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. I ...

bacteria Bacteria (; : bacterium) are ubiquitous, mostly free-living organisms often consisting of one Cell (biology), biological cell. They constitute a large domain (biology), domain of Prokaryote, prokaryotic microorganisms. Typically a few micr ...

. 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 (: green alga) are a group of chlorophyll-containing autotrophic eukaryotes consisting of the phylum Prasinodermophyta and its unnamed sister group that contains the Chlorophyta and Charophyta/ Streptophyta. The land plants ...

, and '' Hydra'' a

cnidarian Cnidaria ( ) is a phylum under kingdom Animalia containing over 11,000 species of aquatic invertebrates found both in fresh water, freshwater and marine environments (predominantly the latter), including jellyfish, hydroid (zoology), hydroids, ...

animal host. Until then it had been described as a

vacuole A vacuole () is a membrane-bound organelle which is present in Plant cell, plant and Fungus, fungal Cell (biology), cells and some protist, animal, and bacterial cells. Vacuoles are essentially enclosed compartments which are filled with water ...

. A few years later in 1989, Lauren Roth with Gary Stacey as well as Robert B Mellor 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 Cell most often refers to: * Cell (biology), the functional basic unit of life * Cellphone, a phone connected to a cellular network * Clandestine cell, a penetration-resistant form of a secret or outlawed organization * Electrochemical cell, a de ...

, 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. Bi ...

envelops the endosymbiont and breaks off into the

cytoplasm The cytoplasm describes all the material within a eukaryotic or prokaryotic cell, enclosed by the cell membrane, including the organelles and excluding the nucleus in eukaryotic cells. The material inside the nucleus of a eukaryotic cell a ...

as a discrete unit, an organelle-like

called the symbiosome. This is an

endocytosis Endocytosis is a cellular process in which Chemical substance, 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 (biology and chem ...

-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 the endocytic membrane transport pathway originating from the trans Golgi network. Molecules or ligands internalized from the plasma membra ...

. 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 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. I ...

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 . salt (chemistry), Salts containing this ion are called nitrates. Nitrates are common components of fertilizers and explosives. Almost all inorganic nitrates are solubility, soluble in wa ...

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 Soil biology Root hairs 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 ...

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 re ...

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 (EPS) are biopolymer, natural polymers of molecular mass, high molecular weight secreted by microorganisms into their environment. EPS establish the functional and structural integrity of biofilms, and are consid ...

(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 that is found in all mammalian cells, with the exception of red blood cells (erythrocytes). There are normally hundreds of lysosomes in the cytosol, where they function as the cell’s degradation cent ...

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 family of globular multi-functional proteins that form microfilaments in the cytoskeleton, and the thin filaments in muscle fibrils. It is found in essentially all eukaryotic cells, where it may be present at a concentration of ...

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 compos ...

. 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 (including its Regulation of gene expression, regulation) by which information from a gene is used in the synthesis of a functional gene product that enables it to produce end products, proteins or non-coding RNA, ...

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. A polypeptide is a longer, continuous, unbranched peptide chain. Polypeptides that have a molecular mass of 10,000 Da or more are called proteins. Chains of fewer than twenty am ...

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 Prokaryote, prokaryotic and eukaryota, eukaryotic cells that may ...

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, antimicrobial activit ...

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 Lipopolysaccharide (LPS), now more commonly known as endotoxin, is a collective term for components of the outermost membrane of the cell envelope of gram-negative bacteria, such as '' E. coli'' and ''Salmonella'' with a common structural archit ...

produced by the bacteria is modified by an unusual

fatty acid In chemistry, in particular in biochemistry, a fatty acid is a carboxylic acid with an aliphatic chain, which is either saturated and unsaturated compounds#Organic chemistry, saturated or unsaturated. Most naturally occurring fatty acids have an ...

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 proteolysis, breaking down proteins into smaller polypeptides or single amino acids, and spurring the formation of new protein products. They do ...

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 (; zooxanthella) is a colloquial term for single-celled photosynthetic organisms that are able to live in symbiosis with diverse marine invertebrates including corals, jellyfish, demosponges, and nudibranchs. Most known zooxanthell ...

. 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 A model organism is a non-human species that is extensively studied to understand particular biological phenomena, with the expectation that discoveries made in the model organism will provide insight into the workings of other organisms. Mo ...

to study the symbiosis with its microsymbiont

species of ''

Symbiodinium ''Symbiodinium'' is a genus of dinoflagellates that encompasses the largest and most prevalent group of endosymbiotic dinoflagellates known and have photosymbiotic relationships with many species. These unicellular microalgae commonly reside in ...

'', 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 regions except Australia, New Zealand, and ...

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 (biology), 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 ph ...

, 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 cel ...

that has been subject to early arrest.

Similar structures

A similar structure to the symbiosome is the parasitophorous vacuole formed within host cells infected by

apicomplexan The Apicomplexa (also called Apicomplexia; single: apicomplexan) are organisms of a large phylum of mainly parasitic alveolates. Most possess a unique form of organelle structure that comprises a type of non-photosynthetic plastid called an apico ...

parasites Parasitism is a close relationship between species, where one organism, the parasite, lives (at least some of the time) on or inside another organism, the host, causing it some harm, and is adapted structurally to this way of life. The en ...

. 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