Symbiosome

The concept of the symbiosome was first described in 1983, by Neckelmann and Muscatine, as seen in the symbiotic relationship between Chlorella ( a class of green algae, and Hydra a cnidarian animal host.[1] Until then it had been described as a vacuole. A few years later in 1989, Lauren Roth with Gary Stacey [8] as well as Robert B Mellor[9] applied this concept to the nitrogen-fixing unit seen in the plant root nodule,[1] previously called an infection vacuole.[10]

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.[11] In the animal models, the symbiosome has a more complex arrangement of membranes, such that it has proved difficult to isolate, purify and study.[1]

A symbiosome is formed as a result of a complex and coordinated interaction between the symbiont host and the endosymbiont.[5] At the point of entry into a symbiont host cell, part of the cell's membrane envelops the endosymbiont and breaks off into the cytoplasm as a discrete unit, an organelle-like vacuole called the symbiosome.[5][12] This is an endocytosis-like process that forms a symbiosome rather than an endosome. In plants this process is unique.[13]

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.[14][12] In the plant root nodule the symbiosome membrane is also called the peribacteroid membrane.[13]

In the legume-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 nitrates in the soil. When these are scarce the plant secretes flavonoids that attract free-living diazotrophic (nitrogen-fixing) rhizobia to their root hairs. In turn the bacteria release Nod factors that stimulate the infection process in the plant.[1][13]

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 root nodules that will house and protect the bacteria.[15][13] The bacterial production of extracellular polymeric substance (EPS) is seen to be necessary for enabling infection.[13] 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.[15][1] The symbiosome is formed as a result of an endocytosis-like process that produces an endosome. Typically endosomes target to lysosomes, 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 cytoskeleton.[16][13] Filamentous actin (F-actin) channels the elongation of the injection threads and short F-actin fragments are dotted around the symbiosome membrane.[16] 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.[17][18]

The most well studied symbiosis involving an animal host is that between the cnidaria and the dinoflagellates, most commonly the single-celled zooxanthellae. The symbiosis of the Chlorella–Hydra first described the symbiosome. The coral Zoanthus robustus has been used as a model organism to study the symbiosis with its microsymbiont algal species of Symbiodinium, 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.[1][22]

The endosymbiont dinoflagellates are used for their ability to photosynthesise and provide energy, giving the host cnidarians such as corals, and anemones, plant properties.[23] Free-living dinoflagellates are ingested into the gastrodermal cells of the host, and their symbiosome membrane is derived from the host cell.[24] The process of symbiosome formation is often seen in the animal host to be that of phagocytosis,[24] and it is hypothesised that the symbiosome is a phagosome that has been subject to early arrest.[25]

A similar structure to the symbiosome is the parasitophorous vacuole formed within host cells infected by apicomplexan parasites. 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.[26][27] The parasitophorous vacuole membrane is greatly remodelled by the parasite.[28]

• Bacteriome
• Trophosome