Wolbachia

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Wolbalchia
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, a species of mosquito. Hertig formally described the species in 1936 as Wolbachia pipientis.[6] Interest waned after the discovery[citation needed] 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 present 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 woodlice showed the broods of infected organisms had a higher proportion of females than their uninfected counterparts.[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]

Wolbachia infections confer fitness advantages

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] In the parasitic filarial nematode species Brugia malayi, Wolbachia has become an obligate endosymbiont and provides the host with chemicals necessary to its survival.[26]

Horizontal gene transfer and genomics

The first Wolbachia genome to be determined was that of one that infects Drosophila melanogaster flies.[27] 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.[28] 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.[29]

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.[30] As a result, Wolbachia can cause misleading results in molecular cladistical analyses.[31]

Wolbachia also harbor a temperate bacteriophage called WO.[32] 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.[33] 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.[34] Consequently, current strategies for control of filarial nematode diseases include elimination of Wolbachia via the simple doxycycline antibiotic rather than far more toxic anti-nematode medications.[35]

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.[36][37] 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.[38] 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.[39] [40] Wolbachia strains that are able to reduce dengue transmission include wAllbB and wMelPop with Aedes aegypti, wMel with Aedes albopictus.[41]

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.[42] 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.[43]

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. ↑ Dumler et al. and Lo et al. argue that W. melophagi should be transferred to the genus Bartonella.
  3. ↑ Forsman et al., Noda et al., and Niebylski et al. argue that W. persica should be transferred to the genus Francisella.
  4. ↑ Werren, J.H.; Guo, L; Windsor, D. W. (1995). "Distribution of Wolbachia among neotropical arthropods". Proceedings of the Royal Society B 262: 197–204. Bibcode:1995RSPSB.262..197W. doi:10.1098/rspb.1995.0196. 
  5. ↑ Kozek, Wieslaw J.; Rao, Ramakrishna U. (2007). "The Discovery of Wolbachia in Arthropods and Nematodes – A Historical Perspective". Issues in Infectious Diseases. Issues in Infectious Diseases 5 (Wolbachia: A Bug’s Life in another Bug): 1–14. doi:10.1159/000104228. ISBN 3-8055-8180-7. 
  6. ↑ Hertig, Marshall; Wolbach, S. Burt (1924). "Studies on Rickettsia-Like Micro-Organisms in Insects". Journal of Medical Research 44 (3): 329–74. PMC 2041761. PMID 19972605. 
  7. ↑ Yen JH; Barr AR (1971). "New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens". Nature 232 (5313): 657–658. Bibcode:1971Natur.232..657Y. doi:10.1038/232657a0. PMID 4937405. 
  8. ↑ Kostas Bourtzis, Thomas A. Miller (ed.). "14: Insect pest control using Wolbachia and/or radiation". Insect Symbiosis. p. 230. ISBN 9780849341946. 
  9. ↑ 9.0 9.1 Knight J (5 July 2001). "Meet the Herod Bug". Nature 421 (6842): 12–14. doi:10.1038/35083744. PMID 11452274. 
  10. ↑ Hurst G., Jiggins F. M., Graf von Der Schulenburg J. H., Bertrand D. et al. (1999). "Male killing Wolbachia in two species of insects". Proceedings of the Royal Society B 266 (1420): 735–740. doi:10.1098/rspb.1999.0698. 
  11. ↑ Tortora, Gerard J.; Funke, Berdell R.; Case, Cristine L. (2007). Microbiology: an introduction. Pearson Benjamin Cummings. ISBN 0-8053-4790-9. 
  12. ↑ Murray, Todd. "Garden Friends & Foes: Trichogramma Wasps". Weeder's Digest (Washington State University Whatcom County Extension). Retrieved 16 July 2009. 
  13. ↑ Werren, John H. (February 2003). "Invasion of the Gender Benders: by manipulating sex and reproduction in their hosts, many parasites improve their own odds of survival and may shape the evolution of sex itself" (Reprint). Natural History 112 (1): 58. ISSN 0028-0712. OCLC 1759475. Retrieved 15 November 2008. 
  14. ↑ Rigaud, Thierry; Moreau, Jérôme; Juchault, Pierre (October 1999). "Wolbachia infection in the terrestrial isopod Oniscus asellus: sex ratio distortion and effect on fecundity". Heredity 83 (4): 469–475. doi:10.1038/sj.hdy.6885990. ISSN 0018-067X. OCLC 1752017. PMID 10583549. Retrieved 16 July 2009.  However, the broods also often consisted of fewer eggs than the broods of the uninfected Oniscus asellus.
  15. ↑ Bordenstein, Seth R.; Patrick, O'Hara; Werren, John H. (2001). "Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia". Nature 409 (6821): 675–677. Bibcode:2001Natur.409..707B. doi:10.1038/35055543. PMID 11217858. 
  16. ↑ Zimmer, Carl (2001). "Wolbachia: A Tale of Sex and Survival". Science 292 (5519): 1093–5. doi:10.1126/science.292.5519.1093. PMID 11352061. 
  17. ↑ Telschow, Arndt; Flor, Matthias; Kobayashi, Yutaka; Hammerstein, Peter; Werren, John H. (2007). "Wolbachia-Induced Unidirectional Cytoplasmic Incompatibility and Speciation: Mainland-Island Model". In Rees, Mark. PLOS ONE 2 (1): e701. Bibcode:2007PLoSO...2..701T. doi:10.1371/journal.pone.0000701. PMC 1934337. PMID 17684548. 
  18. ↑ Charlat S., Reuter M., Dyson E.A., Hornett E.A., Duplouy A.M.R., Davies N., Roderick G., Wedell N., Hurst G.D.D. (2006). "Male-killing bacteria trigger a cycle of increasing male fatigue and female promiscuity". Current Biology 17 (3): 273–277. doi:10.1016/j.cub.2006.11.068. PMID 17276921. 
  19. ↑ JIGGINS F. M.; Hurst, G. D. D.; Majerus, M. E. N. (2000). "Sex ratio distorting Wolbachia cause sex role reversal in their butterfly hosts". Proceedings of the Royal Society B 267 (1438): 69–73. doi:10.1098/rspb.2000.0968. 
  20. ↑ Charlat, S.; Hornett, E. A.; Fullard, J. H.; Davies, N.; Roderick, G. K.; Wedell, N.; Hurst, G. D. D. (2007). "Extraordinary Flux in Sex Ratio". Science 317 (5835): 214. Bibcode:2007Sci...317..214C. doi:10.1126/science.1143369. PMID 17626876. 
  21. ↑ Teixeira, Luis; Ferreira, Alvaro; Ashburner, Michael (2008). "The Bacterial Symbiont Wolbachia Induces Resistance to RNA Viral Infections in Drosophila melanogaster". In Keller, Laurent. PLOS Biology 6 (12): e2. doi:10.1371/journal.pbio.1000002. PMC 2605931. PMID 19222304. 
  22. ↑ Hedges, Lauren; Brownlie, Jeremy; O'Neill, Scott; Johnson, Karyn (2008). "Wolbachia and Virus Protection in Insects". Science 322 (5902): 702. Bibcode:2008Sci...322..702H. doi:10.1126/science.1162418. 
  23. ↑ Glaser, Robert L.; Meola, Mark A. (2010). "The Native Wolbachia Endosymbionts of Drosophila melanogaster and Culex quinquefasciatus Increase Host Resistance to West Nile Virus Infection". In Liu, Ding Xiang. PLOS Biology 5 (6): e11977. Bibcode:2010PLoSO...511977G. doi:10.1371/journal.pone.0011977. PMC 2916829. PMID 20700535. 
  24. ↑ Berticat, Claire; Rousset, Francois. "High Wolbachia density in insecticide-resistant mosquitoes". The Royal Society 269: 1413–1416. 
  25. ↑ Kaiser, Wilfried; Huguet, Elisabeth. "Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts". The Royal Society 77: 2311–2319. 
  26. ↑ Foster, Jeremy; Ganatra, Mehul; Kamal, et al.; Ware, Jennifer; Makarova, Kira; Ivanova, Natalia; Bhattacharyya, Anamitra; Kapatral, Vinayak et al. (2005). "The Wolbachia Genome of Brugia malayi: Endosymbiont Evolution within a Human Pathogenic Nematode". PLos Biology 3 (4): e121. doi:10.1371/journal.pbio.0030121. PMC 1069646. PMID 15780005. 
  27. ↑ Wu M, Sun LV, Vamathevan J, et al. (2004). "Phylogenomics of the Reproductive Parasite Wolbachia pipientis wMel: A Streamlined Genome Overrun by Mobile Genetic Elements". PLOS Biology 2 (3): E69. doi:10.1371/journal.pbio.0020069. PMC 368164. PMID 15024419. 
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  29. ↑ Dunning Hotopp, J.C, Clark ME, Oliveira DC, Foster JM, Fischer P, Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S, Ingram J, Nene RV, Shepard J, Tomkins J, Richards S, Spiro DJ, Ghedin E, Slatko BE, Tettelin H, Werren J.H. (2007). "Widespread Lateral Gene Transfer from Intracellular Bacteria to Multicellular Eukaryotes". Science 317 (5845): 1753–1756. Bibcode:2007Sci...317.1753H. doi:10.1126/science.1142490. PMID 17761848. 
  30. ↑ Whitworth, TL; Dawson, RD; Magalon, H; Baudry, E (2007). "DNA barcoding cannot reliably identify species of the blowfly genus Protocalliphora (Diptera: Calliphoridae)". Proceedings of the Royal Society B 274 (1619): 1731–1739. doi:10.1098/rspb.2007.0062. PMC 2493573. PMID 17472911. 
  31. ↑ Johnstone, RA; Hurst, GDD (1996). "Maternally inherited male-killing microorganisms may confound interpretation of mitochondrial DNA variability". Biological Journal of the Linnean Society 58 (4): 453–470. doi:10.1111/j.1095-8312.1996.tb01446.x. 
  32. ↑ Kent, Bethany N.; Bordenstein, Seth R. (2010). "Phage WO of Wolbachia: lambda of the endosymbiont world". Trends in Micro 8 (10): 173–181. doi:10.1016/j.tim.2009.12.011. PMC 2862486. PMID 20083406. 
  33. ↑ Kent, Bethany N.; Salichos, Leonidas; Gibbons, John G.; Rokas, Antonis; Newton, Irene L.; Clark, Michael E.; Bordenstein, Seth R. (2011). "Complete Bacteriophage Transfer in a Bacterial Endosymbiont (Wolbachia) Determined by Targeted Genome Capture". Genome in Biology and Evolution 3: 209–218. doi:10.1093/gbe/evr007. PMC 3068000. PMID 21292630. 
  34. ↑ Hoerauf A, Mand S, Fischer K, et al. (2003). "Doxycycline as a novel strategy against bancroftian filariasis-depletion of Wolbachia endosymbionts from Wuchereria bancrofti and stop of microfilaria production". Med. Microbiol. Immunol. 192 (4): 211–6. doi:10.1007/s00430-002-0174-6. PMID 12684759. 
  35. ↑ Taylor, MJ; Makunde, WH; McGarry, HF; Turner, JD; Mand, S; Hoerauf, A (2005). "Macrofilaricidal activity after doxycycline treatment of Wuchereria bancrofti: a double-blind, randomised placebo-controlled trial". Lancet 365 (9477): 2116–21. doi:10.1016/S0140-6736(05)66591-9. PMID 15964448. 
  36. ↑ Xi, Z; Dean JL, Khoo C, Dobson SL. (2005). "Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection.". Insect Biochem Mol Biol 35 (8): 903–10. PMC 1410910. 
  37. ↑ Moreira, LA; Iturbe-ormaetxe I, Jeffery JA, et al. (2009). "A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium". Cell 139 (7): 1268–78. PMID 20064373. 
  38. ↑ Hancock, PA; Sinkins SP, Godfray HC. (2011). "Strategies for introducing Wolbachia to reduce transmission of mosquito-borne diseases.". PLoS Negl Trop Dis. 5 (4): e1024. PMC 3082501. 
  39. ↑ Mcmeniman, CJ; Lane RV, Cass BN, et al. (2009). "Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti". Science 323 (5910): 141–4. PMID 19119237. 
  40. ↑ "'Bug' could combat dengue fever". BBC NEWS (British Broadcasting Corporation). 2 January 2009. 
  41. ↑ Blagrove, MS; Arias-goeta C, Failloux AB, Sinkins SP. (2012). "Wolbachia strain wMel induces cytoplasmic incompatibility and blocks dengue transmission in Aedes albopictus". Proc Natl Acad Sci USA 109 (1): 255–60. PMC 3252941. 
  42. ↑ Pan, X; Zhou G, Wu J, et al. (2012). "Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti.". Proc Natl Acad Sci USA 109 (1): E23–31. PMC 3252928. 
  43. ↑ Bian, G; Joshi D, Dong Y, et al. (2013). "Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection". Science 340 (6133): 748–51. PMID 23661760. 

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