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Wolbachia

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Wolbachia
Transmission electron micrograph ofWolbachiawithin an insect cell
Credit:Public Library of Science/ Scott O'Neill
Scientific classificationEdit this classification
Domain: Bacteria
Phylum: Pseudomonadota
Class: Alphaproteobacteria
Order: Rickettsiales
Family: Ehrlichiaceae
Genus: Wolbachia
Hertig 1936 (Approved Lists 1980)
Species
  • "Candidatus Wolbachia bourtzisii"Ramirez-Puebla et al. 2015
  • "Candidatus Wolbachia brugii"Ramirez-Puebla et al. 2015
  • "Candidatus Wolbachia collembolicola"Ramirez-Puebla et al. 2015
  • "Candidatus Wolbachia ivorensis"Ehounoud et al. 2016
  • Wolbachia melophagi(Nöller 1917) Philip 1956 (Approved Lists 1980)
  • "Candidatus Wolbachia multihospitum"Ramirez-Puebla et al. 2015
  • "Candidatus Wolbachia onchocercicola"Ramirez-Puebla et al. 2015
  • Wolbachia pipientisHertig 1936 (Approved Lists 1980)

Wolbachiais agenusofgram-negative bacteriathat can either infect many species ofarthropodas anintracellular parasite,or act as amutualisticmicrobe infilarial nematodes.[1][2]It is one of the most commonparasiticmicrobesof arthropods, and is possibly the most commonreproductiveparasite in thebiosphere.[3]Its interactions with its hosts are often complex. Some host species cannot reproduce, or even survive, withoutWolbachiacolonisation.One study concluded that more than 16% ofneotropicalinsect species carry bacteria of this genus,[4]and as many as 25 to 70% of all insect species are estimated to be potential hosts.[5]

History[edit]

The genus was first identified in 1924 by Marshall Hertig andSimeon Burt Wolbachin thecommon house mosquito.They described it as "a somewhatpleomorphic,rodlike,Gram-negative,intracellular organism [that] apparently infects only theovariesandtestes".[6]Hertig formally described the species in 1936, and proposed both thegenericandspecificnames:Wolbachia pipientis.[7]Research onWolbachiaintensified after 1971, when Janice Yen and A. Ralph Barr ofUCLAdiscovered thatCulexmosquito eggs were killed by acytoplasmic incompatibilitywhen the sperm ofWolbachia-infected males fertilized infection-free eggs.[8][9]The genusWolbachiais of considerable interest today due to its ubiquitous distribution, its many different evolutionary interactions, and its potential use as abiocontrol agent.

Phylogenetic studies have shown thatWolbachia persica(nowFrancisella persica) was closely related to species in the genusFrancisella[10][11][12][13]and thatWolbachia melophagi(nowBartonella melophagi) was closely related to species in the genusBartonella,[14][15][16]leading to a transfer of these species to these respective genera. Furthermore, unlike trueWolbachia,which needs a host cell to multiply,F. persicaandB. melophagican be cultured onagar plates.[17][16]

Method of sexual differentiation in hosts[edit]

These bacteria can infect many different types of organs, but are most notable for the infections of thetestesandovariesof their hosts.Wolbachiaspecies are ubiquitous in mature eggs, but not mature sperm. Only infected females, therefore, pass the infection on to their offspring.Wolbachiabacteria maximize their spread by significantly altering the reproductive capabilities of their hosts, with four differentphenotypes:

  • Male killing occurs when infected males die during larval development, which increases the rate of born, infected females.[18]
  • Feminizationresults in infected males that develop as females or infertile pseudofemales. This is especially prevalent inLepidopteraspecies such as the adzuki bean borer (Ostrinia scapulalis).[19]
  • Parthenogenesisis reproduction of infected females without males. Some scientists have suggested that parthenogenesis may always be attributable to the effects ofWolbachia,[20]though this is not the case for themarbled crayfish.[21]An example of parthenogenesis induced by presence ofWolbachiaare some species within theTrichogrammaparasitoid wasp genus,[22]which have evolved to procreate without males due to the presence ofWolbachia.Males are rare in this genus of wasp, possibly because many have been killed by that same strain ofWolbachia.[23]
  • Cytoplasmic incompatibilityis the inability ofWolbachia-infected males to successfully reproduce with uninfected females or females infected with anotherWolbachiastrain.This reduces the reproductive success of those uninfected females and therefore promotes the infecting strain. In the cytoplasmic incompatibility mechanism,Wolbachiainterferes with the parental chromosomes during the firstmitoticdivisions to the extent that they can no longer divide in synchrony.[24]

Effects of sexual differentiation in hosts[edit]

Several host species, such as those within the genusTrichogramma,are so dependent on sexual differentiation ofWolbachiathat they are unable to reproduce effectively without the bacteria in their bodies, and some might even be unable to survive uninfected.[25]

One study on infectedwoodliceshowed the broods of infected organisms had a higher proportion of females than their uninfected counterparts.[26]

Wolbachia,especiallyWolbachia-caused cytoplasmic incompatibility, may be important in promoting speciation.[27][28][29]Wolbachiastrains that distort the sex ratio may alter their host's pattern of sexual selection in nature,[30][31]and also engender strong selection to prevent their action, leading to some of the fastest examples of natural selection in natural populations.[32]

The male killing and feminization effects ofWolbachiainfections can also lead to speciation in their hosts. For example, populations of the pill woodlouse,Armadillidium vulgarewhich are exposed to the feminizing effects ofWolbachia,have been known to lose their female-determining chromosome.[33]In these cases, only the presence ofWolbachiacan cause an individual to develop into a female.[33]Cryptic species of ground wētā (Hemiandrus maculifronscomplex) are host to different lineages ofWolbachiawhich might explain their speciation without ecological or geographical separation.[34][35]

Effect on aromatase[edit]

The enzymearomataseis found to mediate sex-change in many species of fish.Wolbachiacan affect the activity of aromatase in developing fish embryos.[36]

Mechanism of Host Transfer[edit]

Step 1: physical transfer[edit]

a. Predator-prey interactions[edit]

Wolbachiamay transfer from prey to predator through the digestive system. To do so,Wolbachianeeds to first survive through the lumen secretion and then enter the host tissue through the gut epithelium.[37]This route does not seem to occur frequently due to little evidence.[38]

b. Host–parasitoid/parasite interactions[edit]

This may be one of the most common routes ofWolbachiahost shifts. Compared to predator-prey interactions, the physical association between the host and parasites typically lasts longer, occurs at various developmental stages, and enablesWolbachiato directly contact various tissues.

Since this interaction may expose both sides to microbial exchange, one strategy for understanding the direction of transfer is to assessWolbachia's presence in close relatives on both sides, as the donor side generally has a larger diversity of infection.[39]

One parasitoid species can infect multiple shared hosts, and one host species can infect multiple parasitoids. For instance, parthenogenesis-inducingWolbachiacan spread betweenTrichogrammaparasitoid wasps sharing host eggs.[40]

Parasites can also serve as a vector between infected and uninfected hosts without being infected. When the mouthparts and ovipositors ofaphelinidparasitoid wasps become contaminated through feedingWolbachia-infectedBemisia tabaci,it can infect the next host.[41]

c. Shared plant and other food sources[edit]

This route applies to microbes that can survive either within or on the surface of the food. Experiments demonstrated that theWolbachiawAlbB strain can survive extracellularly for up to 7 days,[42]and up to 50 days for some strains in cotton leafphloemvessels.[43]

Plants are one of the best platforms for this route. By physical contact between arthropod mouthparts and plant tissue, theWolbachiainhabiting the salivary glands of some insects may be transferred to the plants.[44]As a result, arthropod species feeding on the same plants may share commonWolbachiastrains.

Other insect food sources may also mediateWolbachiahorizontal transfer, such as the sharing of dung patches between two Malagasy dung beetle species.[45]

Step 2: survival and proliferation in the new host[edit]

Thepathogen-associated molecular patterns(PAMPs) in the bacteria, such aspeptidoglycan,can activate the host's innate immune responses.[46][47]In response, someWolbachiastrains have a unique functional peptidoglycan amidase (AmiDwol) that cleaves its bacterial cell wall so that it can escape from immune responses.[48][49]Besides the peptidoglycans, cell-to-cell movements ofWolbachiacan also cause oxidative stress to the host and trigger the host's immune response.[50]Therefore,Wolbachiahas a triple-layer vacuole that acts as a mechanical shield to protect it from cellular immune responses.[37]

Step 3: vertical transmission[edit]

Vertical transmission requiresWolbachiato reach germ line cells and maintain in the zygote.Wolbachiamay initially occupy somatic stem cells as a stable reservoir[51]and then use the host'svitellogenintransovarial transportation system to enter theoocyte.[52]OnceWolbachiaenter the zygote, they need to reach important host tissues without disrupting the embryo's development. This can be achieved using the host cytoskeleton, by bundlingWolbachiaprotein WD0830 to host actin filaments. They can also increase the division rate of germ-line stem cells to localize and increase their titer.[53][54][55]Under natural conditions, successful vertical transmission ofWolbachiais challenging.

Step 4: spread within the host population[edit]

Invasion of a new population likely stems from specific phenotypic effects, including reproductive manipulations and/or providing direct fitness benefits to their female hosts.[56][57][58][59]

Upon transferring into a new host,Wolbachiamay retain its original phenotypic effects, induce a different phenotype, or have no detectable effect. For instance, a strain that induce male killing in the mothCadra cautellainduced Cytoplasmic incompatibility in a novel moth hostEphestia kuehniella.[60]

Fitness advantages byWolbachiainfections[edit]

Wolbachiainfection has been linked to viral resistance inDrosophila melanogaster,Drosophila simulans,and mosquito species. Flies, including mosquitoes,[61]infected with the bacteria are more resistant to RNA viruses such asDrosophila C virus,norovirus,flock house virus,cricket paralysis virus,chikungunya virus,andWest Nile virus.[62][63][64]

In the common house mosquito, higher levels ofWolbachiawere correlated with more insecticide resistance.[65]

Inleafminersof the speciesPhyllonorycter blancardella,Wolbachiabacteria help their hosts produce green islands on yellowing tree leaves, that is, small areas of leaf remaining fresh, allowing the hosts to continue feeding while growing to their adult forms. Larvae treated withtetracycline,which killsWolbachia,lose this ability and subsequently only 13% emerge successfully as adult moths.[66]

Muscidifurax uniraptor,aparasitoid wasp,also benefits from hostingWolbachiabacteria.[67]

In the parasiticfilarial nematodespecies responsible forelephantiasis,such asBrugia malayiandWuchereria bancrofti,Wolbachiahas become an obligateendosymbiontand provides the host with chemicals necessary for its reproduction and survival.[68]Elimination of theWolbachiasymbionts through antibiotic treatment therefore prevents reproduction of the nematode, and eventually results in its premature death.

SomeWolbachiaspecies that infect arthropods also provide some metabolic provisioning to their hosts. InDrosophila melanogaster,Wolbachiais found to mediate iron metabolism under nutritional stress[69]and inCimex lectularius,theWolbachiastraincClehelps the host to synthesizeB vitamins.[70]

SomeWolbachiastrains have increased their prevalence by increasing their hosts' fecundity.Wolbachiastrains captured from 1988 in southern California still induce afecunditydeficit, but nowadays the fecundity deficit is replaced with a fecundity advantage such that infectedDrosophila simulansproduces more offspring than the uninfected ones.[71]

Life-history consequences ofWolbachiainfection[edit]

Wolbachiaoften manipulates host reproduction and life-history in a way that favours its own propagation. In thePharaoh ant,Wolbachiainfection correlates with increased colony-level production of reproductives (i.e., greater reproductive investment), and earlier onset of reproductive production (i.e., shorter life-cycle). Infected colonies also seem to grow more rapidly.[72]There is substantial evidence that the presence ofWolbachiathat induce parthenogenesis have put pressure on species to reproduce primarily or entirely this way.[73]

Additionally,Wolbachiahas been seen to decrease the lifespan ofAedes aegypti,carriers of mosquito-borne diseases, and it decreases their efficacy of pathogen transmission because older mosquitoes are more likely to have become carriers of one of those diseases.[74]This has been exploited as a method for pest control.

Genomics[edit]

The firstWolbachiagenome to be determined was that of strain wMel, which infectsD. melanogasterfruit flies.[75]This genome was sequenced atThe Institute for Genomic Researchin a collaboration betweenJonathan Eisenand Scott O'Neill. The secondWolbachiagenome to be determined was of strain wBm, which infectsBrugia malayinematodes.[68]Genome sequencing projects for several otherWolbachiastrains are in progress.

Horizontal gene transfer[edit]

Wolbachiaspecies also harbor abacteriophagecalledbacteriophage WOor phage WO.[76]Comparative sequence analyses of bacteriophage WO offer some of the most compelling examples of large-scale horizontal gene transfer betweenWolbachiacoinfections in the same host.[77]It is the first bacteriophage implicated in frequent lateral transfer between the genomes of bacterialendosymbionts.Gene transfer by bacteriophages could drive significant evolutionary change in the genomes of intracellular bacteria that were previously considered highly stable or prone to loss of genes over time.[77]

Wolbachiaalso transfers genes to the host. A nearly complete copy of theWolbachiagenome sequence was found within the genome sequence of the fruit flyDrosophila ananassaeand large segments were found in seven otherDrosophilaspecies.[78]

In an application ofDNA barcodingto the identification of species ofProtocalliphoraflies, several distinct morphospecies had identical cytochrome c oxidase I gene sequences, most likely throughhorizontal gene transfer(HGT) byWolbachiaspecies as they jump across host species.[79]As a result,Wolbachiacan cause misleading results inmolecularcladisticalanalyses.[80]It is estimated that between 20 and 50 percent of insect species have evidence of HGT fromWolbachia—passing from microbes to animal (i.e. insects).[81]

Small RNA[edit]

The smallnon-coding RNAsWsnRNA-46andWsnRNA-59inWolbachiawere detected inAedes aegyptimosquitoes andDrosophila melanogaster.Thesmall RNAs(sRNAs) may regulate bacterial and host genes.[82]Highly conserved intragenic region sRNA calledncrwmel02was also identified inWolbachia pipientis.It is expressed in four different strains in a regulated pattern that differs according to the sex of the host and the tissue localisation. This suggested that the sRNA may play important roles in the biology ofWolbachia.[83]

Relation to human-related infections[edit]

Role in parasites[edit]

Outside of insects,Wolbachiainfects a variety ofisopodspecies,spiders,mites,and many species of filarialnematodes(a type ofparasitic worm), including those causingonchocerciasis(river blindness) andelephantiasisin humans, as well asheartwormsin dogs. Not only are these disease-causing filarial worms infected withWolbachia,butWolbachiaalso seems to play an inordinate role in these diseases.

A large part of the pathogenicity of filarial nematodes is due to host immune response toward theirWolbachia.Elimination ofWolbachiafrom filarial nematodes generally results in either death or sterility of the nematode.[84]Consequently, current strategies for control of filarial nematode diseases include elimination of their symbioticWolbachiavia the simpledoxycyclineantibiotic, rather than directly killing the nematode with often more toxic antinematode medications.[85]

Disease prevention[edit]

Further information:Biological pest control
Indonesian research ministerMohamad Nasirduring a visit to aWolbachiamosquito lab of the Eliminate Dengue Project.

Naturally existing strains ofWolbachiahave been shown to be a route forvector controlstrategies because of their presence in arthropod populations, such as mosquitoes.[86][87]Due to the unique traits ofWolbachiathat causecytoplasmic incompatibility,some strains are useful to humans as a promoter of genetic drive within an insect population.Wolbachia-infected females are able to produce offspring with uninfected and infected males; however, uninfected females are only able to produce viable offspring with uninfected males. This gives infected females a reproductive advantage that is greater the higher the frequency ofWolbachiain the population. Computational models predict that introducingWolbachiastrains into natural populations will reduce pathogen transmission and reduce overall disease burden.[88]An example includes a life-shorteningWolbachiathat can be used to controldenguevirus andmalariaby eliminating the older insects that contain more parasites. Promoting the survival and reproduction of younger insects lessens selection pressure for evolution of resistance.[89][90]

Adi Utarini,research lead of theWolbachiatrial inYogyakarta,Indonesia

In addition, someWolbachiastrains are able to directly reduce viral replication inside the insect. For dengue they include wAllbB and wMelPop withAedes aegypti,wMel withAedes albopictus[91]andAedes aegypti.[92]

Wolbachiahas also been identified to inhibit replication of chikungunya virus (CHIKV) inA. aegypti.ThewMel strain ofWolbachia pipientissignificantly reduced infection and dissemination rates of CHIKV in mosquitoes, compared toWolbachiauninfected controls and the same phenomenon was observed in yellow fever virus infection converting this bacterium in an excellent promise for YFV and CHIKV suppression.[93]

Wolbachiaalso inhibits the secretion of West Nile virus (WNV) in cell line Aag2 derived fromA. aegypticells. The mechanism is somewhat novel, as the bacteria actually enhances the production of viral genomic RNA in the cell lineWolbachia.Also, the antiviral effect in intrathoracically infected mosquitoes depends on the strain ofWolbachia,and the replication of the virus in orally fed mosquitoes was completely inhibited in wMelPop strain ofWolbachia.[94]

The effect ofWolbachiainfection on virus replication in insect hosts is complex and depends on theWolbachiastrain and virus species.[95]While several studies have indicated consistent refractory phenotypes ofWolbachiainfection on positive-sense RNA viruses inDrosophila melanogaster,[96][97]the yellow fever mosquitoAedes aegypti[98]and the Asian tiger mosquitoAedes albopictus,[99][100]this effect is not seen in DNA virus infection[97]and in some casesWolbachiainfection has been associated or shown to increase single stranded DNA[101]and double-stranded DNA virus infection.[102]There is also currently no evidence thatWolbachiainfection restricts any tested negative-sense RNA viruses[103][104][105][106]indicatingWolbachiawould be unsuitable for restriction of negative-sense RNA arthropod borne viruses.

Wolbachiainfection can also increase mosquito resistance to malaria, as shown inAnopheles stephensiwhere thewAlbB strain ofWolbachiahindered the lifecycle ofPlasmodium falciparum.[107]

However,Wolbachiainfections can also enhance pathogen transmission.Wolbachiahas enhanced multiplearbovirusesinCulex tarsalismosquitoes.[108]In another study, West Nile Virus (WNV) infection rate was significantly higher inWolbachia(strain wAlbB)-infectedC. tarsaliscompared to controls.[109]

Wolbachiamay inducereactive oxygen species–dependent activation of theToll (gene family)pathway, which is essential for activation of antimicrobialpeptides,defensins,andcecropinsthat help to inhibit virus proliferation.[110]Conversely, certain strains actually dampen the pathway, leading to higher replication of viruses. One example is with strain wAlbB inCulex tarsalis,where infected mosquitoes actually carried the west nile virus (WNV) more frequently. This is because wAlbB inhibits REL1, an activator of the antiviral Toll immune pathway. As a result, careful studies of theWolbachiastrain and ecological consequences must be done before releasing artificially-infected mosquitoes in the environment.[109]

Techniques and deployments[edit]

Strain wMel, mixed-sex[edit]

The World Mosquito Program (WMP) usesWolbachiastrain wMel to infectAedesmosquitos. The mixed-sex mosquitos are intended to infect the local population with wMel, giving them transmission resistance.[111]

In 2014, WMP released infected mosquitos inTownsville,an Australia city with 187,000 inhabitants plagued by dengue. For four years after introduction, no cases of dengue were reported.[112]Trials in much smaller areas had been carried out, but a larger area had not been tested. No environmental ill-effects were reported. The cost wasA$15 per inhabitant, but it was hoped that it could be reduced toUS$1 in poorer countries with lower labor costs.[113]

In 2016, WMP scientist Scott Ritchie proposed using wMel mosquitos to combat the spread of theZika virus.[114]A study reported thatWolbachiawMel has the ability to block Zika in Brazil.[115]In October 2016, it was announced that US$18 million in funding was being allocated for the use ofWolbachia-infected mosquitoes to fight Zika and dengue viruses. Deployment is slated for early 2017 in Colombia and Brazil.[116]

Between 2016 and 2020, WMP conducted its firstrandomized controlled trialinYogyakarta,an Indonesian city of about 400,000 inhabitants. In August 2020, the trial's Indonesian lead scientistAdi Utariniannounced that the trial showed a 77% reduction in dengue cases compared to the control areas. This trial was the "strongest evidence yet" for the technique.[117][118]

In 2017–2019, WMP released mosquitos in Niterói, Brazil.[119]

In March 2023, Brazil'sOswaldo Cruz Foundationsigned an agreement with WMP to provide funds for a large "mosquito factory" producing infected insects.[120]

Male incompatibility[edit]

Another method to useWolbachiain mosquitos exploits the cytoplamic incompatibility between infected males and uninfected females. If an uninfected female mates with an infected male, her eggs become infertile. With enough infected males released, the mosquito population would be reduced temporarily.[121]

Verily,the life sciences arm of Google's parent companyAlphabet Inc.,uses this method. In July 2017, it announced a plan to release about 20 millionWolbachia-infected maleAedes aegyptimosquitoes inFresno,California,in an attempt to combat theZikavirus.[121][122]Singapore's National Environment Agency has teamed up with Verily to come up with an advanced, more efficient way to release maleWolbachiamosquitoes for Phase 2 of its study to suppress the urbanAedes aegyptimosquito population and fight dengue.[123]

On November 3, 2017, theUS Environmental Protection Agency(EPA) registered Mosquito Mate, Inc. to releaseWolbachiastrain "ZAP" -infected male mosquitoes in 20 US states and the District of Columbia.[124]

See also[edit]

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Further reading[edit]

External links[edit]

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