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, 8 (3), 218-30

A Complex Journey: Transmission of Microbial Symbionts


A Complex Journey: Transmission of Microbial Symbionts

Monika Bright et al. Nat Rev Microbiol.


The perpetuation of symbioses through host generations relies on symbiont transmission. Horizontally transmitted symbionts are taken up from the environment anew by each host generation, and vertically transmitted symbionts are most often transferred through the female germ line. Mixed modes also exist. In this Review we describe the journey of symbionts from the initial contact to their final residence. We provide an overview of the molecular mechanisms that mediate symbiont attraction and accumulation, interpartner recognition and selection, as well as symbiont confrontation with the host immune system. We also discuss how the two main transmission modes shape the evolution of the symbiotic partners.


Figure 1
Figure 1. Symbiont transmission pathways
a | Horizontal transmission from the environment. Host reproduction leads to aposymbiotic descendants, which at a certain life stage are infected with symbionts from the environment; often symbionts are translocated from the initial site of host contact to a putative symbiont housing organ; sometimes the environmental pool is replenished by symbiont release. b | Vertical transmission through the female germ line. Prior to host reproduction, symbionts are typically translocated from the symbiont housing organ to the female gonad, resulting in symbiotic descendants; often symbionts are then translocated from the colonization site to the symbiont housing organ. c | Mixed mode of transmission. Vertical transmission and occasional horizontal transmission can occur through host switching. Besides vertical transmission, occasional horizontal transfer of new symbionts (magenta) from a host population within the same species, but not the parent (intraspecific host switching; not shown), from a different host species (interspecific host switching; shown in brown) or from a free-living population (not shown) occurs.
Figure 2
Figure 2. Simplified host life cycles of horizontally transmitted symbionts
a | Legumes and intracellular rhizobia in root nodules (the example shown is the soybean Glycine max and Bradyrhizobium spp.). Aposymbiotic germ cells are produced by the flower; internal fertilization leads to aposymbiotic seeds in which the embryo develops. After germination, symbiont uptake occurs through infection threads in the roots of seedlings, as long as the plant grows (reviewed in REF. 11). b | The bobtail squid Euprymna scolopes and its extracellular endosymbiont Vibrio fischeri in the light organ crypts. Male and female hosts copulate, egg clutches are laid in the environment and they develop into aposymbiotic juveniles. Free-living V. fischeri is selectively taken up from the environment, and colonization of the light organ is completed within 12 hours after hatching (reviewed in REF. 31). c | The vestimentiferan tubeworm Riftia pachyptila harbours endosymbiotic Candidatus Endoriftia persephone in the trophosome. Sperm are released from males and migrate to females, where eggs are fertilized internally; zygotes are released into the water column, disperse and develop to larvae that settle, and metamorphosis is initiated. Symbionts infect the larval skin, migrate to the mesoderm surrounding the gut, and the trophosome develops. Environmental bacteria are shown in purple.
Figure 3
Figure 3. Simplified host life cycles of vertically transmitted extracellular endosymbionts
a | In the colonial, hermaphroditic ascidian Didemnum molle the extracellular endosymbiont Prochloron didemni covers the tunic surface of the cloacal cavity. Sperm uptake into each zooid is followed by internal fertilization and embryonic development. The embryos migrate into the tunic and develop into larvae. When the larvae hatch into the cloacal cavity, they pick up the symbiont onto the posterior part of the body; larvae are then released from the cavity into the water column, settle after dispersal and undergo metamorphosis, during which the symbiont finally ends up on the surface of the cloacal cavity again. b | The colonial, hermaphroditic bryozoan Bugula neritina harbours the extracellular endosymbiont Candidatus Endobugula sertula in the funicular cords of adult colonies and the pallial sinus of larvae. Sperm uptake and internal fertilization result in transfer of the zygote into the ovicell, in which the endosymbiont is most likely taken up through the funicular cords during embryonic development (not shown). The embryo develops into larvae which are then released and can disperse and settle. Following metamorphosis into preancestrula and ancestrula stages (first zooid), the symbionts migrate and end up in the funicular cords of the developing colony again. c | The hermaphroditic earthworm Eisenia foetida harbours the extracellular endosymbiont Verminephrobacter eiseniae in the lumen of nephridial ampullae. During copulation and release of eggs and sperm, symbionts and albumin are released into the egg capsule, which is concurrently also infected with environmental bacteria (shown in purple). The egg is externally fertilized and develops into a juvenile in the egg capsule. During this time the symbionts are selected and taken up through a pore, they migrate through a canal to the ventral pore that leads into the nephridia, where they establish in the ampullae. The juveniles then hatch and develop into adults,.
Figure 4
Figure 4. Simplified host life cycles of vertically or pseudovertically transmitted intracellular endosymbionts
a | The head louse Pediculus humanus harbours the intracellular Candidatus Riesia pediculicola in the stomach disc and ovarial ampullae. Male and female lice reproduce through copulation and internal fertilization. The symbionts colonize the eggs through hydrophyles in eggshells and reside extracellularly in the periplasm. Individual eggs are laid in which embryonic development proceeds until the first instar nymphs hatch. During this development the bacteriome goes through three maturation stages (embryonic basket bacteriome with extracellular symbionts, embryonic bacteriome with intracellular symbionts and stomach disc bacteriome). After hatching and the development of two further instar nymph stages, in females symbionts are released and migrate to the oviducts to build a new bacteriome in the ovarial ampullae; from there, oocytes are infected and the male stomach disc bacteriome degenerates,,. b | The rice weevil Sitophilus oryzae principal symbiont (SOPE) resides in the caeca and ovaries in females and in the caeca in males. Males and females reproduce through copulation and internal fertilization. Eggs containing endosymbionts are laid and sealed with a gelatinous plug. During early embryonic development, the SOPE population is split into two parts, one becoming associated with the primordial germ cells, which later constitute the intraovarian bacteriocytes that infect the next generation oocytes, and the other associates with the future bacteriome. Larvae develop, moult four times, pupate, and adults hatch; in young females symbionts in the caeca are reduced by unknown mechanisms so that in older females symbionts are found only in the ovaries. c | Pseudovertical transmission of the entomopathogenic nematode Steinernema carpocapsae and its symbiont, Xenorhabdus nematophila. The male and female reproduce through copulation and internal fertilization, and the embryo develops indirectly, with four juvenile stages. Some juveniles that develop into the infective stage are colonized by symbionts entering the mouth and migrating through the pharynx to the vesicle (the gut lumen between two most anterior intestinal cells). Infective juveniles infected by the bacteria leave the insect cadaver and find a new host. Symbionts are released from the vesicle into a new insect host by passing through the intestine into the insect blood, where they reproduce and kill the insect. Symbionts within an insect cadaver originate from the infected nematode population; it is unknown how many nematodes infect a single insect (reviewed in REFS 21,146). This transmission mode has been termed pseudovertical because more than one nematode can be found within a single insect, and therefore the symbionts transmitted to the nematode progeny could come from the parent (vertical) or from the co-occurring nematodes in the insect (host switching). Environmental bacteria are shown in purple.

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