Wolbachia
Transmission electron micrograph of Wolbachia within an insect cell.
Credit:Public Library of Science / Scott O'Neill
Scientific classification
Kingdom: Bacteria
Phylum: Proteobacteria
Class: Alphaproteobacteria
Order: Rickettsiales
Family: Rickettsiaceae
Genus: Wolbachia
Species[1]

Wolbachia melophagi (Nöller 1917) Philip 1956[2] Wolbachia persica Suitor and Weiss 1961[3] Wolbachia pipientis Hertig 1936

Wolbachia is a genus of bacteria which infects arthropod species, including a high proportion of insects, as well as some nematodes. It is one of the world's most common parasitic microbes and is possibly the most common reproductive parasite in the biosphere. Its interactions with its hosts are often complex, and in some cases have evolved to be mutualistic rather than parasitic. Some host species cannot reproduce, or even survive, without Wolbachia infection. One study concluded that more than 16% of neotropical insect species carry bacteria of this genus,[4] and as many as 25 to 70 percent of all insect species are estimated to be potential hosts.[5]

History

The genus was first identified in 1924 by Marshall Hertig and S. Burt Wolbach in Culex pipiens, the common house mosquito. Hertig formally described the species in 1936 as Wolbachia pipientis.[6] Interest waned after the discovery until 1971, when Janice Yen and A. Ralph Barr of UCLA discovered Culex mosquito eggs were killed by a cytoplasmic incompatibility when the sperm of Wolbachia-infected males fertilized infection-free eggs.[7][8] In 1990, Richard Stouthamer of the University of California, Riverside discovered Wolbachia can make males dispensable in some species.[9] It is today of considerable interest due to its ubiquitous distribution and many different evolutionary interactions.

Role in sexual differentiation of hosts

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

  • Male killing: infected males die during larval development, which increase the rate of born, infected, females.[10]
  • Feminization: infected males develop as females or infertile pseudo-females.
  • Parthenogenesis: reproduction of infected females without males. Some scientists have suggested that parthenogenesis may always be attributable to the effects of Wolbachia.[11] An example of a parthenogenic species is the Trichogramma wasp,[9] which has evolved to procreate without males with the help of Wolbachia. Males are rare in this tiny species of insect, possibly because many have been killed by that very same strain of Wolbachia.[12]
  • Cytoplasmic incompatibility: the inability of Wolbachia-infected males to successfully reproduce with uninfected females or females infected with another Wolbachia strain.

Several species are so dependent on Wolbachia, they are unable to reproduce effectively without the bacteria in their bodies, and some might even be unable to survive uninfected.[13]

One study on infected [14]

Wolbachia, especially Wolbachia-caused cytoplasmic incompatibility, may be important in promoting speciation.[15][16][17] Wolbachia strains that distort the sex ratio may alter their host's pattern of sexual selection in nature,[18][19] and also engender strong selection to prevent their action, leading to some of the fastest examples of natural selection in natural populations.[20]

Fitness advantages conferred by Wolbachia infections

Wolbachia has been linked to viral resistance in Drosophila melanogaster and mosquito species. Flies infected with the bacteria are more resistant to RNA viruses such as Drosophila C virus, Nora virus, Flock house virus, Cricket paralysis virus, Chikungunya virus, and West Nile virus.[21][22][23] In the common house mosquito, higher levels of Wolbachia density were correlated with more insecticide resistance.[24] In leafminers of the species Phyllonorycter blancardella, Wolbachia bacteria help their hosts produce green islands on yellowing tree leaves, allowing the hosts to continue feeding while growing to their adult forms. Larvae treated with tetracycline, which kills Wolbachia, lose this ability and subsequently only 13% emerge successfully as adult moths.[25]

Wolbachia is also found to provide the host with a benefit of increasing fecundity. Weeks et al. found that the Wolbachia strains captured from 1988 in southern California still induce a fecundity deficit, but nowadays the fecundity deficit is replaced with a fecundity advantage such that infected Drosophila simulans produces more offspring than the uninfected ones.[26]

In the parasitic filarial nematode species Brugia malayi, Wolbachia has become an obligate endosymbiont and provides the host with chemicals necessary to its survival.[27] However, Wolbachia that infects arthropods is also found to provide some metabolic provisioning to its host recently. In Drosophila melanogaster, Wolbachia is found to mediate iron metabolism;[28] and in Climex lectularis, Wolbachia strain cCle is helping the host to synthesize B Vitamins.[29]

Horizontal gene transfer and genomics

The first Wolbachia genome to be determined was that of one that infects Drosophila melanogaster flies.[30] This genome was sequenced at The Institute for Genomic Research in a collaboration between Jonathan Eisen and Scott O'Neill. The second Wolbachia genome to be determined was one that infects Brugia malayi nematodes.[31] Genome sequencing projects for several other Wolbachia strains are in progress. A nearly complete copy of the Wolbachia genome sequence was found within the genome sequence of the fruit fly Drosophila ananassae and large segments were found in 7 other Drosophila species.[32]

In an application of DNA barcoding to the identification of species of Protocalliphora flies, it was found that several distinct morphospecies had identical cytochrome c oxidase I gene sequences, most likely through horizontal gene transfer by Wolbachia species as they jump across host species.[33] As a result, Wolbachia can cause misleading results in molecular cladistical analyses.[34]

Wolbachia also harbor a temperate bacteriophage called WO.[35] Comparative sequence analyses of bacteriophage WO offer some of the most compelling examples of large-scale horizontal gene transfer between Wolbachia coinfections in the same host.[36] It is the first bacteriophage implicated in frequent lateral transfer between the genomes of bacterial endosymbionts. Gene transfer by bacteriophages could drive significant evolutionary change in the genomes of intracellular bacteria that are typically considered highly stable and prone to genomic degradation.

Applications to human health

Outside of insects, Wolbachia infects a variety of isopod species, spiders, mites, and many species of filarial nematodes (a type of parasitic worm), including those causing onchocerciasis ("River Blindness") and elephantiasis in humans as well as heartworms in dogs. Not only are these disease-causing filarial worms infected with Wolbachia, but Wolbachia seem to play an inordinate role in these diseases. A large part of the pathogenicity of filarial nematodes is due to host immune response toward their Wolbachia. Elimination of Wolbachia from filarial nematodes generally results in either death or sterility of the nematode.[37] Consequently, current strategies for control of filarial nematode diseases include elimination of their symbiotic Wolbachia via the simple doxycycline antibiotic, rather than directly killing the nematode with far more toxic anti-nematode medications.[38]

Naturally existing strains of Wolbachia have been shown to be a route for vector control strategies because of their presence in arthropod populations, such as mosquito populations.[39][40] Due to the unique traits of Wolbachia that cause cytoplasmic incompatibility, this strain is useful as a promoter of genetic drive within a population. Wolbachia-infected females are not able to produce offspring with non-infected males, keeping the genome free from mixing with arthropods carrying diseases. Computational models predict that introducing Wolbachia strains into natural populations will reduce pathogen transmission and reduce overall disease burden.[41] An example includes Wolbachia that can be used to control dengue and malaria by eliminating the older insects that contain more parasites. Promoting the survival and reproduction of younger insects lessens selection pressure for evolution of resistance.[42][43] Wolbachia strains that are able to reduce dengue transmission include wAllbB and wMelPop with Aedes aegypti, wMel with Aedes albopictus.[44] and Aedes aegypti.[45] In addition to inhibit the DENV (Dengue Virus) in some species of gender Aedes, Wolbachia has been identified to inhibit replication of CHIKV (Chikungunya virus) in Aedes aegypti. It was found that Wmel strain of Wolbachia pipientis reduced significantly infection and dissemination rates of CHIKV in mosquitoes, compared to Wolbachia uninfected controls and the same phenomenon was observed in YFV (Yellow Fever Virus) infection converting this bacteria in an excellent promise for YFV and CHIKV suppression.[46]

Another study tested the effect of Wolbachia on the replication of WNV (West Nile Virus) but in cell lin Aag2 derived from Aedes aegypti cells, suggesting that despite the exist an enhancement of viral genomic RNA replication in the cell line Wolbachia infected, the production of secreted virus was significantly inhibited. It also was found that the antiviral effect in intrathoracically infected mosquitoes depends on the strain of Wolbachia, and the replication of the virus in orally fed mosquitoes was completely inhibited in wMelPop strain of Wolbachia.[47]

However, cases where Wolbachia reduces transmission of pathogens must be studied carefully. Indeed, a recent study demonstrated that the West Nile virus could be improved by the presence of the Wolbachia strain wAlbB in the mosquito Culex tarsalis. The rate of virus appears significantly higher than in uninfected mosquitoes. Indeed, wAlbB inhibits REL1, which is an activator of the antiviral Toll immune pathway. The release of artificially infected mosquitoes in the environment, for a vector-borne disease control program, should be made with caution, because it is the first case of improvement of a human disease in the mosquito.[48]

It has been suggested that Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll (gene family) pathway. This pathway is essential for activation of antimicrobial peptides, defensins, and cecropins that help to inhibit dengue virus proliferation.[49] Wolbachia infection can also increase mosquito resistance to malaria, as shown in Anopheles stephensi where the wAlbB strain of Wolbachia hindered the life cycle of Plasmodium falciparum.[50]

See also

References

  1. ^ Most Wolbachia species cannot be cultured outside of their eukaryotic host and so have not been given formal latin names.
  2. ^ Arguing that W. melophagi should be transferred to the genus Bartonella
  3. ^ Arguing that W. persica should be transferred to the genus Francisella
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  6. ^ Hertig, Marshall; Wolbach, S. Burt (1924). "Studies on Rickettsia-Like Micro-Organisms in Insects". Journal of Medical Research 44 (3): 329–74.  
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Further reading

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