Endosymbiosis played key roles in the development of
eukaryotes and plants. Roughly 2.2 billion years ago an
archaea absorbed a
bacterium through
phagocytosis that eventually became the
mitochondria that provide energy to all living cells. Approximately 1 billion years ago, other cells absorbed
cyanobacteria that eventually became
chloroplasts,
organelles that produce energy from sunlight.[4] Some 100 million years ago, UCYN-A, a nitrogen-fixing bacteria became an endosymbiont of marine algae Braarudosphaera bigelowii, eventually evolving into a
nitroplast.[5] Similarly,
Diatoms in the family Rhopalodiaceae have evolved a diazoplast, a nitrogen-fixing organelle.[6]
Symbionts are either obligate (require their host to survive) or facultative (can survive independently).[7] The most common examples of obligate endosymbiosis are
mitochondria and
chloroplasts, which reproduce via
mitosis in tandem with their host cells. Some human parasites, e.g. Wuchereria bancrofti and Mansonella perstans, thrive in their intermediate insect hosts because of an obligate endosymbiosis with Wolbachia spp.[8] They can both be eliminated by treatments that target their bacterial host.[9]
Etymology
Endosymbiosis comes from the
Greek: ἔνδον endon "within", σύν syn "together" and βίωσις biosis "living".
Symbiogenesis
Symbiogenesis theory holds that eukaryotes evolved via absorbing
prokaryotes. Typically, one organism envelopes a bacteria and the two evolve a mutualistic relationship. The absorbed bacteria (the endosymbiont) eventually lives exclusively within the host cells. This fits the concept of observed organelle development.[10][11][12][13][14]
Typically the endosymbiont's genome shrinks, discarding genes whose roles are displaced by the host.[15] For example the Hodgkinia genome of Magicicadacicadas is much different from the prior freestanding bacteria. The cicada life cycle involves years of stasis underground. The symbiont produces many generations during this phase, experiencing little
selection pressure, allowing their genomes to diversify. Selection is episodic (when the cicadas reproduce). The original Hodgkinia genome split into three much simpler endosymbionts, each encoding only a few genes—an instance of
punctuated equilibrium producing distinct lineages. The host requires all three symbionts.[16]
Symbiont transmission is the process where the host acquires its symbiont. Since symbionts are not produced by host cells, they must find their own way to reproduce and populate daughter cells as host cells divide. Horizontal, vertical, and mixed-mode (hybrid of horizonal and vertical) transmission are the three paths for symbiont transfer.
Horizontal
Horizontal symbiont transfer (
horizontal transmission) is a process where a host acquires a facultative symbiont from the environment or another host.[7] The Rhizobia-Legume symbiosis (bacteria-plant endosymbiosis) is a prime example of this modality.[17] The Rhizobia-legume symbiotic relationship is important for processes such as the formation of root nodules. It starts with flavonoids released by the legume host, which causes the rhizobia species (endosymbiont) to activate its Nod genes.[17] These Nod genes generate
lipooligosaccharide signals that the legume detects, leading to root nodule formation.[18] This process bleeds into other processes such as nitrogen fixation in plants.[17] The evolutionary advantage of such an interaction allows genetic exchange between both organisms involved to increase the propensity for novel functions as seen in the plant-bacterium interaction (
holobiont formation).[19]
Vertical
Vertical transmission takes place when the symbiont moves directly from parent to offspring.[20][21] In horizontal transmission each generation acquires symbionts from the environment. An example is nitrogen-fixing bacteria in certain plant roots, such as
pea aphid symbionts. A third type is mixed-mode transmission, where symbionts move horizontally for some generations, after which they are acquired vertically.[22][23][24]
Wigglesworthia, a tsetse fly symbiont,[24] is vertically transmitted (via mother's milk).[25] When a symbiont reaches this stage, it resembles a cellular
organelle, similar to
mitochondria or
chloroplasts. In
vertical transmission, the symbionts do not need to survive independently, often leading them to have a reduced genome. For instance,
pea aphid symbionts have lost genes for essential molecules and rely on the host to supply them. In return, the symbionts synthesize essential
amino acids for the aphid host.[18] When a symbiont reaches this stage, it begins to resemble a cellular
organelle, similar to
mitochondria or
chloroplasts. Such dependent hosts and symbionts form a
holobiont. In the event of a bottleneck, a decrease in symbiont diversity could compromise host-symbiont interactions, as deleterious mutations accumulate.[26]
Hosts
Invertebrates
The best-studied examples of endosymbiosis are in
invertebrates. These symbioses affect organisms with global impact, including Symbiodinium (corals), or Wolbachia (insects). Many insect agricultural pests and human disease vectors have intimate relationships with primary endosymbionts.[27]
Insects
Scientists classify insect endosymbionts as Primary or Secondary. Primary endosymbionts (P-endosymbionts) have been associated with their
insect hosts for millions of years (from ten to several hundred million years). They form obligate associations and display
cospeciation with their insect hosts. Secondary endosymbionts more recently associated with their hosts, may be horizontally transferred, live in the
hemolymph of the insects (not specialized bacteriocytes, see below), and are not obligate.[28]
Primary
Among primary endosymbionts of insects, the best-studied are the pea
aphid (Acyrthosiphon pisum) and its endosymbiont Buchnera sp. APS,[29][18] the
tsetse flyGlossina 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. Nutritionally-enhanced diets allow symbiont-free specimens to survive, but they are unhealthy, and at best survive only a few generations.[citation needed]
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 embryo. In termites, the endosymbionts reside within the hindguts and are transmitted through
trophallaxis among colony members.[30]
Primary endosymbionts are thought to help the host either by providing essential nutrients 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 diet of plant sap. The primary role of Wigglesworthia 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.
Primary endosymbionts of insects have among the smallest of known bacterial genomes and have
lost many genes commonly found in closely related bacteria. One theory claimed 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 primary endosymbionts are transferred only vertically.[31][32]
Attacking obligate bacterial endosymbionts may present a way to control their hosts, many of which are pests or human disease carriers. For example, aphids are crop pests and the tsetse fly carries the organism Trypanosoma brucei that causes African
sleeping sickness.[33] Studying insect endosymbionts can aid understanding the origins of symbioses in general, as a proxy for understanding endosymbiosis in other species.
The best-studied ant endosymbionts are Blochmannia bacteria, which are the primary endosymbiont of Camponotus ants. In 2018 a new ant-associated symbiont, Candidatus Westeberhardia Cardiocondylae, was discovered in Cardiocondyla. It is reported to be a primary symbiont.[34]
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.[37] This defence is mediated by toxins called "
ribosome-inactivating
proteins" that attack the molecular machinery of invading parasites.[38][39] These toxins represent one of the first understood examples of a defensive symbiosis with a mechanistic understanding for defensive symbiosis between an insect endosymbiont and its host.[40]
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 do not report a correlation between evolution of Sodalis and tsetse.[41] Unlike Wigglesworthia,Sodalis has been cultured in vitro.[42]
Cardinium and many other insects have secondary endosymbionts.[43][15]
Marine
Extracellular endosymbionts are 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.[44]
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).[45]
The sea slug Elysia chlorotica's endosymbiont is the
algaeVaucheria litorea. The
jellyfishMastigias have a similar relationship with an algae. Elysia chlorotica forms this relationship intracellularly with the algae's chloroplasts. These chloroplasts retain their photosynthetic capabilities and structures for several months after entering the slug's cells.[46]
Trichoplax have two bacterial endosymbionts. Ruthmannia lives inside the animal's digestive cells. Grellia lives permanently inside the
endoplasmic reticulum (ER), the first known symbiont to do so.[47]
Paracatenula is a
flatworm which have lived in symbiosis with an endosymbiotic bacteria for 500 million years. The bacteria produce numerous small, droplet-like vesicles that provide the host with needed nutrients.[48]
Previously thought to be a single species, molecular
phylogenetic evidence reported diversity in Symbiodinium. In some cases, the host requires a specific Symbiodiniumclade. More often, however, the distribution is ecological, with symbionts switching among hosts with ease. When reefs become environmentally stressed, this distribution 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 is an important in coral reef ecology.[49]
In marine environments,[50][51][52][53] endosymbiont relationships are especially prevalent in
oligotrophic or nutrient-poor regions of the ocean like that of the North Atlantic.[50][54][51][52] In such waters, cell growth of larger
phytoplankton such as
diatoms is limited by (insufficient)
nitrate concentrations.[55] Endosymbiotic bacteria fix nitrogen for their hosts and in turn receive organic carbon from photosynthesis.[54] These symbioses play an important role in global
carbon cycling.[56][51][52]
One known symbiosis between the diatom Hemialus spp. and the cyanobacterium Richelia intracellularis has been reported in North Atlantic, Mediterranean, and Pacific waters.[50][51][57]Richelia is found within the
diatom frustule of Hemiaulus spp., and has a reduced genome.[58] A 2011 study measured nitrogen fixation by the
cyanobacterial host Richelia intracellularis well above intracellular requirements, and found the cyanobacterium was likely fixing nitrogen for its host.[55] Additionally, both host and symbiont cell growth were much greater than free-living Richelia intracellularis or symbiont-free Hemiaulus spp.[55] The Hemaiulus-Richelia symbiosis is not obligatory, especially in nitrogen-replete areas.[50]
Richelia intracellularis is also found in Rhizosolenia spp., a diatom found in oligotrophic oceans.[54][55][52] Compared to the Hemaiulus host, the endosymbiosis with Rhizosolenia is much more consistent, and Richelia intracellularis is generally found in Rhizosolenia.[50] There are some asymbiotic (occurs without an endosymbiont) Rhizosolenia, however there appears to be mechanisms limiting growth of these organisms in low nutrient conditions.[59] 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.[59]
Other endosymbiosis with nitrogen fixers in open oceans include Calothrix in Chaetoceros spp. and UNCY-A in
prymnesiophyte microalga.[60] The Chaetoceros-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.[58] 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.[58] This endosymbiont reduction in genome size, might be a step that occurred in the evolution of organelles (above).[60]
Protists
Mixotricha paradoxa is a
protozoan that lacks mitochondria. However, spherical bacteria live inside the cell and serve the function of the mitochondria. Mixotricha has three other species of symbionts that live on the surface of the cell.[61]
Many
foraminifera are hosts to several types of algae, such as
red algae,
diatoms,
dinoflagellates and
chlorophyta.[67] 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 algae horizontally following sexual reproduction.[68]
Several species of
radiolaria have photosynthetic symbionts. In some species the host digests algae to keep the population at a constant level.[69]
Hatena arenicola is a flagellate
protist with a complicated feeding apparatus that feeds on other microbes. When it engulfs a green Nephroselmis alga, the feeding apparatus disappears and it becomes photosynthetic. During
mitosis the algae is transferred to only one of the daughter cells, while the other cell restarts the cycle.
In 1966, biologist Kwang W. Jeon found that a lab strain of Amoeba proteus had been infected by bacteria that lived inside the cytoplasmic
vacuoles.[70] This infection killed almost all of the infected protists. After the equivalent of 40 host generations, the two organisms become mutually interdependent. A genetic exchange between the
prokaryotes and protists occurred.[71][72][73]
All vascular plants harbor endosymbionts or endophytes in this context. They include
bacteria,
fungi,
viruses,
protozoa and even
microalgae. Endophytes aid in processes such as growth and development, nutrient uptake, and defense against biotic and abiotic stresses like
drought,
salinity, heat, and herbivores.[75]
Plant symbionts can be categorized into
epiphytic,
endophytic, and
mycorrhizal. These relations can also be categorized as beneficial,
mutualistic, neutral, and
pathogenic.[76][77]Microorganisms living as endosymbionts in plants can enhance their host's primary productivity either by producing or capturing important resources.[78] These endosymbionts can also enhance plant productivity by producing toxic metabolites that aid plant defenses against
herbivores.[79][80]
Plants are dependent on
plastid or
chloroplast organelles. The chloroplast is derived from a cyanobacterial primary endosymbiosis that began over one billion years ago. An oxygenic, photosynthetic free-living
cyanobacterium was engulfed and kept by a heterotrophic
protist and eventually evolved into the present intracellular organelle.[81]
Typically, plant endosymbiosis studies focus on a single category or species to better understand their individual biological processes and functions.[82]
Fungal endophytes
Fungal endophytes can be found in all plant tissues. Fungi living below the ground amidst plant roots are known as
mycorrhiza, but are further categorized based on their location inside the root, with prefixes such as ecto, endo, arbuscular, ericoid, etc. Fungal endosymbionts that live in the roots and extend their extraradical
hyphae into the outer
rhizosphere are known as ectendosymbionts.[83][84]
Arbuscular Mycorrhizal Fungi (AMF)
Arbuscular mycorrhizal fungi or AMF are the most diverse plant microbial endosymbionts. With exceptions such as the
Ericaceae family, almost all vascular plants harbor
AMF endosymbionts as endo and ecto as well. AMF plant endosymbionts systematically colonize
plant roots and help the plant host acquire soil
nutrients such as nitrogen. In return it absorbs plant organic carbon products.[83]Plant root exudates contain diverse secondary metabolites, especially
flavonoids and
strigolactones that act as
chemical signals and attracts the AMF.[85] AMF Gigaspora margarita lives as a plant endosymbiont and also harbors further endosymbiont intracytoplasmic bacterium-like organisms.[86] AMF generally promote plant health and growth and alleviate
abiotic stresses such as salinity, drought, heat, poor nutrition, and
metal toxicity.[87] Individual AMF species have different effects in different hosts – introducing the AMF of one plant to another plant can reduce the latter's growth.[88]
Endophytic fungi
Endophytic fungi in
mutualistic relations directly benefit and benefit from their host plants. They also can help their hosts succeed in polluted environments such as those contaminated with toxic metals.[89] Fungal
endophytes are taxonomically diverse and are divided into categories based on mode of transmission,
biodiversity, in planta colonization and host plant type.[90][91] Clavicipitaceous fungi systematically colonize temperate season grasses. Non-clavicipitaceous fungi colonize higher plants and even roots and divide into subcategories.[92]Bacillus amyloliquefaciens is a seed-born endophytic fungi that produces
gibberellins and promotes physiology. Bacillus amyloliquefaciens promotes the taller height of
transgenic dwarf rice plants.[93] Similarly, Aureobasidiumand preussia species of endophytic fungi isolated from Boswellia sacra produce
indole acetic acidhormone to promote plant health and development.[94]
Endophytic bacteria belong to a diverse group of plant endosymbionts characterized by systematic colonization of plant tissues. The most common genera include Pseudomonas, Bacillus, Acinetobacter, Actinobacteria, Sphingomonas. Some endophytic bacteria genera additionally belong to the
Enterobacteriaceae family.[95] Endophytic bacteria typically colonize the leaf tissues from plant roots, but can also enter the plant through the leaves through leaf
stomata.[96] Generally, the endophytic bacteria are isolated from the plant tissues by surface
sterilization of the plant tissue in a sterile environment.[97] Passenger endophytic bacteria eventually colonize inner tissue of plant by
stochastic events while True endophytes possess adaptive traits because of which they live strictly in association with plants.[98] The in vitro-cultivated endophytic
bacteria association with plants is considered a more intimate relationship that helps plants acclimatize to conditions and promotes health and growth. Endophytic bacteria are considered to be plant's essential endosymbionts because virtually all plants harbor them, and these endosymbionts play essential roles in host survival.[99] This endosymbiotic relation is important in terms of
ecology,
evolution and diversity. Endophytic bacteria such as Sphingomonas sp. and Serratia sp. that are isolated from arid land plants regulate endogenous
hormone content and promote growth.[100]
Archaea endosymbionts
Archaea are members of most
microbiomes. While archaea are abundant in extreme environments, they are less abundant and diverse in association with eukaryotic hosts. Nevertheless, archaea are a substantial constituent of plant-associated ecosystems in the aboveground and belowground phytobiome, and play a role in host plant’s health, growth and survival amid biotic and abiotic stresses. However, few studies have investigated the role of archaea in plant health and its symbiotic relationships.[101] Most plant endosymbiosis studies focus on fungal or bacteria using
metagenomic approaches.[102]
The characterization of archaea includes crop plants such as
rice[103] and
maize, but also aquatic plants.[101] The abundance of archaea varies by tissue type; for example archaea are more abundant in the
rhizosphere than the
phyllosphere and
endosphere.[104] This archaeal abundance is associated with plant species type, environment and the plant’s developmental stage.[105] In a study on plant
genotype-specific archaeal and bacterial endophytes, 35% of archaeal sequences were detected in overall sequences (achieved using
amplicon sequencing and verified by
real time-PCR). The archaeal sequences belong to the phyla Thaumarchaeota, Crenarchaeota, and Euryarchaeota.[106]
Fungi host endohyphal bacteria;[108] the effects of the bacteria are not well studied. Many such fungi in turn live within plants.[108] These fungi are otherwise known as fungal
endophytes. It is hypothesized that the fungi offers a safe haven for the
bacteria, and the diverse bacteria that they attract create a micro-ecosystem.[109]
These interactions may impact the way that fungi interact with the environment by modulating their
phenotypes.[108] The bacteria do this by altering the fungi's
gene expression.[108] For example, Luteibacter sp. has been shown to naturally infect the
ascomycetousendophytePestalotiopsis sp. isolated from Platycladus orientalis.[108] The Luteibacter sp. influences the
auxin and enzyme production within its host, which, in turn, may influence the effect the fungus has on its plant host.[108] Another interesting example of a bacteria living in symbiosis with a fungus is the fungus Mortierella. This soil-dwelling fungus lives in close association with a toxin-producing bacteria, Mycoavidus, which helps the fungus defend against
nematodes.[110]
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