Endosymbiont

An endosymbiont or endobiont[1] 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 "within", σύν syn "together" and βίωσις biosis "living".) Examples are nitrogen-fixing bacteria (called rhizobia), which live in the root nodules of legumes, single-cell algae inside reef-building corals and bacterial endosymbionts that provide essential nutrients to insects.[2][3]

A representation of the endosymbiotic theory

There are two types of symbiont transmissions. In horizontal transmission, each new generation acquires free living symbionts from the environment. An example is the nitrogen-fixing bacteria in certain plant roots. Vertical transmission takes place when the symbiont is transferred directly from parent to offspring.[4][5] It is also possible for both to be involved in a mix-mode transmission, where symbionts are transferred vertically for some generation before a switch of host occurs and new symbionts are horizontally acquired from the environment.[6][7][8]

In vertical transmissions, the symbionts often have a reduced genome and are no longer able to survive on their own. As a result, the symbiont depends on the host, resulting in a highly intimate co-dependent relationship. For instance, pea aphid symbionts have lost genes for essential molecules, now relying on the host to supply them with nutrients. In return, the symbionts synthesize essential amino acids for the aphid host.[9] Other examples include Wigglesworthia nutritional symbionts of tse-tse flies, or in sponges.[8] When a symbiont reaches this stage, it begins to resemble a cellular organelle, similar to mitochondria or chloroplasts.

Many instances of endosymbiosis are obligate; that is, either the endosymbiont or the host cannot survive without the other, such as the gutless marine worms of the genus Riftia, which get nutrition from their endosymbiotic bacteria. The most common examples of obligate endosymbioses are mitochondria and chloroplasts. Some human parasites, e.g. Wuchereria bancrofti and Mansonella perstans, thrive in their intermediate insect hosts because of an obligate endosymbiosis with Wolbachia spp. They can both be eliminated from hosts by treatments that target this bacterium. However, not all endosymbioses are obligate and some endosymbioses can be harmful to either of the organisms involved.

Two major types of organelle in eukaryotic cells, mitochondria and plastids such as chloroplasts, are considered to be bacterial endosymbionts.[10] This process is commonly referred to as symbiogenesis.

Symbiogenesis and organelles
An overview of the endosymbiosis theory of eukaryote origin (symbiogenesis).

Symbiogenesis explains the origins of eukaryotes, whose cells contain two major kinds of organelle: mitochondria and chloroplasts. The theory proposes that these organelles evolved from certain types of bacteria that eukaryotic cells engulfed through phagocytosis. These cells and the bacteria trapped inside them entered an endosymbiotic relationship, meaning that the bacteria took up residence and began living exclusively within the eukaryotic cells.[4][5][11][12]

Numerous insect species have endosymbionts at different stages of symbiogenesis. A common theme of symbiogenesis involves the reduction of the genome to only essential genes for the host and symbiont collective genome.[13] A remarkable example of this is the fractionation of the Hodgkinia genome of Magicicada cicadas. Because the cicada life cycle takes years underground, natural selection on endosymbiont populations is relaxed for many bacterial generations. This allows the symbiont genomes to diversify within the host for years with only punctuated periods of selection when the cicadas reproduce. As a result, the ancestral Hodgkinia genome has split into three groups of primary endosymbiont, each encoding only a fraction of the essential genes for the symbiosis. The host now requires all three sub-groups of symbiont, each with degraded genomes lacking most essential genes for bacterial viability.[14]

Bacterial endosymbionts of invertebrates

The best-studied examples of endosymbiosis are known from invertebrates. These symbioses affect organisms with global impact, including Symbiodinium of corals, or Wolbachia of insects. Many insect agricultural pests and human disease vectors have intimate relationships with primary endosymbionts.

Endosymbionts of insects
Diagram of cospeciation, where parasites or endosymbionts speciate or branch alongside their hosts. This process is more common in hosts with primary endosymbionts.

Scientists classify insect endosymbionts in two broad categories, 'Primary' and 'Secondary'. Primary endosymbionts (sometimes referred to as P-endosymbionts) have been associated with their insect hosts for many millions of years (from 10 to several hundred million years in some cases). They form obligate associations (see below), and display cospeciation with their insect hosts. Secondary endosymbionts exhibit a more recently developed association, are sometimes horizontally transferred between hosts, live in the hemolymph of the insects (not specialized bacteriocytes, see below), and are not obligate.[15]

Primary endosymbionts

Among primary endosymbionts of insects, the best-studied are the pea aphid (Acyrthosiphon pisum) and its endosymbiont Buchnera sp. APS,[16][9] the tsetse fly Glossina morsitans morsitans and its endosymbiont Wigglesworthia glossinidia brevipalpis and the endosymbiotic protists in lower termites. As with endosymbiosis in other insects, the symbiosis is obligate in that neither the bacteria nor the insect is viable without the other. Scientists have been unable to cultivate the bacteria in lab conditions outside of the insect. With special nutritionally-enhanced diets, the insects can survive, but are unhealthy, and at best survive only a few generations.

In some insect groups, these endosymbionts live in specialized insect cells called bacteriocytes (also called mycetocytes), and are maternally-transmitted, i.e. the mother transmits her endosymbionts to her offspring. In some cases, the bacteria are transmitted in the egg, as in Buchnera; in others like Wigglesworthia, they are transmitted via milk to the developing insect embryo. In termites, the endosymbionts reside within the hindguts and are transmitted through trophallaxis among colony members.

The primary endosymbionts are thought to help the host either by providing nutrients that the host cannot obtain itself or by metabolizing insect waste products into safer forms. For example, the putative primary role of Buchnera is to synthesize essential amino acids that the aphid cannot acquire from its natural diet of plant sap. Likewise, the primary role of Wigglesworthia, it is presumed, is to synthesize vitamins that the tsetse fly does not get from the blood that it eats. In lower termites, the endosymbiotic protists play a major role in the digestion of lignocellulosic materials that constitute a bulk of the termites' diet.

Bacteria benefit from the reduced exposure to predators and competition from other bacterial species, the ample supply of nutrients and relative environmental stability inside the host.

Genome sequencing reveals that obligate bacterial endosymbionts of insects have among the smallest of known bacterial genomes and have lost many genes that are commonly found in closely related bacteria. Several theories have been put forth to explain the loss of genes. It is presumed that some of these genes are not needed in the environment of the host insect cell. A complementary theory suggests that the relatively small numbers of bacteria inside each insect decrease the efficiency of natural selection in 'purging' deleterious mutations and small mutations from the population, resulting in a loss of genes over many millions of years. Research in which a parallel phylogeny of bacteria and insects was inferred supports the belief that the primary endosymbionts are transferred only vertically (i.e., from the mother), and not horizontally (i.e., by escaping the host and entering a new host).[17][18]

Attacking obligate bacterial endosymbionts may present a way to control their insect hosts, many of which are pests or carriers of human disease. For example, aphids are crop pests and the tsetse fly carries the organism Trypanosoma brucei that causes African sleeping sickness.[19] Other motivations for their study involve understanding the origins of symbioses in general, as a proxy for understanding e.g. how chloroplasts or mitochondria came to be obligate symbionts of eukaryotes or plants.

Secondary endosymbionts
Pea aphids are commonly infested by parasitic wasps. Their secondary endosymbionts attack the infesting parasitoid wasp larvae promoting the survival of both the aphid host and its endosymbionts.

The pea aphid (Acyrthosiphon pisum) is known to contain at least three secondary endosymbionts, Hamiltonella defensa, Regiella insecticola, and Serratia symbiotica. Hamiltonella defensa defends its aphid host from parasitoid wasps.[20] This defensive symbiosis improves the survival of aphids, which have lost some elements of the insect immune response.[21]

One of the best-understood defensive symbionts is the spiral bacteria Spiroplasma poulsonii. Spiroplasma sp. can be reproductive manipulators, but also defensive symbionts of Drosophila flies. In Drosophila neotestacea, S. poulsonii has spread across North America owing to its ability to defend its fly host against nematode parasites.[22] This defence is mediated by toxins called "ribosome-inactivating proteins" that attack the molecular machinery of invading parasites.[23][24] These Spiroplasma toxins represent one of the first examples of a defensive symbiosis with a mechanistic understanding for defensive symbiosis between an insect endosymbiont and its host.

Sodalis glossinidius is a secondary endosymbiont of tsetse flies that lives inter- and intracellularly in various host tissues, including the midgut and hemolymph. Phylogenetic studies have not indicated a correlation between evolution of Sodalis and tsetse.[25] Unlike tsetse's primary symbiont Wigglesworthia, though, Sodalis has been cultured in vitro.[26]

Many other insects have secondary endosymbionts not reviewed here.[27][13]

Bacteriocyte-associated symbionts

The most well studied endosymbiont of ants are bacteria of the genus Blochmannia, which are the primary endosymbiont of Camponotus ants. In 2018 a new ant-associated symbiont was discovered in Cardiocondyla ants. This symbiont was named Candidatus Westeberhardia Cardiocondylae and it is also believed to be a primary symbiont.[28]

Endosymbionts of marine invertebrates

Extracellular endosymbionts are also represented in all four extant classes of Echinodermata (Crinoidea, Ophiuroidea, Echinoidea, and Holothuroidea). Little is known of the nature of the association (mode of infection, transmission, metabolic requirements, etc.) but phylogenetic analysis indicates that these symbionts belong to the class Alphaproteobacteria, relating them to Rhizobium and Thiobacillus. Other studies indicate that these subcuticular bacteria may be both abundant within their hosts and widely distributed among the Echinoderms in general.[29]

Some marine oligochaeta (e.g., Olavius algarvensis and Inanidrillus spp.) have obligate extracellular endosymbionts that fill the entire body of their host. These marine worms are nutritionally dependent on their symbiotic chemoautotrophic bacteria lacking any digestive or excretory system (no gut, mouth, or nephridia).[30]

The sea slug Elysia chlorotica lives in endosymbiotic relationship with the algae Vaucheria litorea, and the jellyfish Mastigias have a similar relationship with an algae.

Dinoflagellate endosymbionts

Dinoflagellate endosymbionts of the genus Symbiodinium, commonly known as zooxanthellae, are found in corals, mollusks (esp. giant clams, the Tridacna), sponges, and foraminifera. These endosymbionts drive the formation of coral reefs by capturing sunlight and providing their hosts with energy for carbonate deposition.[31]

Previously thought to be a single species, molecular phylogenetic evidence over the past couple decades has shown there to be great diversity in Symbiodinium. In some cases, there is specificity between host and Symbiodinium clade. More often, however, there is an ecological distribution of Symbiodinium, the symbionts switching between hosts with apparent ease. When reefs become environmentally stressed, this distribution of symbionts is related to the observed pattern of coral bleaching and recovery. Thus, the distribution of Symbiodinium on coral reefs and its role in coral bleaching presents one of the most complex and interesting current problems in reef ecology.[31]

Endosymbionts of phytoplankton

In marine environments, bacterial endosymbionts have more recently been discovered.[32][33][34][35] These endosymbiotic relationships are especially prevalent in oligotrophic or nutrient-poor regions of the ocean like that of the North Atlantic.[32][36][33][34] In these oligotrophic waters, cell growth of larger phytoplankton like that of diatoms is limited by low nitrate concentrations.[37]  Endosymbiotic bacteria fix nitrogen for their diatom hosts and in turn receive organic carbon from photosynthesis.[36] These symbioses play an important role in global carbon cycling in oligotrophic regions.[38][33][34]

One known symbiosis between the diatom Hemialus spp. and the cyanobacterium Richelia intracellularis has been found in the North Atlantic, Mediterranean, and Pacific Ocean.[32][33][39] The Richelia endosymbiont is found within the diatom frustule of Hemiaulus spp., and has a reduced genome likely losing genes related to pathways the host now provides.[40]  Research by Foster et al. (2011) measured nitrogen fixation by the cyanobacterial host Richelia intracellularis well above intracellular requirements, and found the cyanobacterium was likely fixing excess nitrogen for Hemiaulus host cells.[37] Additionally, both host and symbiont cell growth were much greater than free-living Richelia intracellularis or symbiont-free Hemiaulus spp.[37] The Hemaiulus-Richelia symbiosis is not obligatory especially in areas with excess nitrogen (nitrogen replete).[32]

Richelia intracellularis is also found in Rhizosolenia spp., a diatom found in oligotrophic oceans.[36][37][34] Compared to the Hemaiulus host, the endosymbiosis with Rhizosolenia is much more consistent, and Richelia intracellularis is generally found in Rhizosolenia.[32] There are some asymbiotic (occurs without an endosymbiont) Rhizosolenia, however there appears to be mechanisms limiting growth of these organisms in low nutrient conditions.[41] Cell division for both the diatom host and cyanobacterial symbiont can be uncoupled and mechanisms for passing bacterial symbionts to daughter cells during cell division are still relatively unknown.[41]

Other endosymbiosis with nitrogen fixers in open oceans include Calothrix in Chaetocerous spp. and UNCY-A in prymnesiophyte microalga.[42]  The Chaetocerous-Calothrix endosymbiosis is hypothesized to be more recent, as the Calothrix genome is generally intact. While other species like that of the UNCY-A symbiont and Richelia have reduced genomes.[40] This reduction in genome size occurs within nitrogen metabolism pathways indicating endosymbiont species are generating nitrogen for their hosts and losing the ability to use this nitrogen independently.[40] This endosymbiont reduction in genome size, might be a step that occurred in the evolution of organelles (above).[42]

Endosymbionts of protists

Mixotricha paradoxa is a protozoan that lacks mitochondria. However, spherical bacteria live inside the cell and serve the function of the mitochondria. Mixotricha also has three other species of symbionts that live on the surface of the cell.

Paramecium bursaria, a species of ciliate, has a mutualistic symbiotic relationship with green alga called Zoochlorella. The algae live inside the cell, in the cytoplasm.

Paulinella chromatophora is a freshwater amoeboid which has recently (evolutionarily speaking) taken on a cyanobacterium as an endosymbiont.

Many foraminifera are hosts to several types of algae, such as red algae, diatoms, dinoflagellates and chlorophyta.[43] These endosymbionts can be transmitted vertically to the next generation via asexual reproduction of the host, but because the endosymbionts are larger than the foraminiferal gametes, they need to acquire new algae again after sexual reproduction.[44]

Several species of radiolaria have photosynthetic symbionts. In some species the host will sometimes digest algae to keep their population at a constant level.[45]

Hatena arenicola is a flagellate protist with a complicated feeding apparaturs that feed on other microbes. But when it engulfs a green alga from the genus Nephroselmis, the feeding apparatus disappears and it becomes photosynthetic. During mitosis the algae is transferred to only one of the two cells, and the cell without the algae needs to start the cycle all over again.

In 1976, biologist Kwang W. Jeon found that a lab strain of Amoeba proteus had been infected by bacteria that lived inside the cytoplasmic vacuoles.[46] This infection killed all the protists except for a few individuals. After the equivalent of 40 host generations, the two organisms gradually became mutually interdependent. Over many years of study, it has been confirmed that a genetic exchange between the prokaryotes and protists had occurred.[47][48][49]

Endosymbionts of vertebrates

The spotted salamander (Ambystoma maculatum) lives in a relationship with the algae Oophila amblystomatis, which grows in the egg cases.[50]

Endosymbionts of plants

Chloroplasts are primary endosymbionts of plants that provide energy to the plant by generating sugars.

Of all the plants, Azolla has the most intimate relationship with a symbiont, as its cyanobacterium symbiont Anabaena is passed on directly from one generation to the next.[51][52]

Endosymbionts of bacteria

It has been observed that some Betaproteobacteria have Gammaproteobacteria endosymbionts.[53]

Virus-host associations

The human genome project found several thousand endogenous retroviruses, endogenous viral elements in the genome that closely resemble and can be derived from retroviruses, organized into 24 families.[54][55]

See also

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