The Intracellular Bacterium Wolbachia Uses Parasitoid Wasps as Phoretic Vectors for Efficient Horizontal Transmission

PLoS Pathogens

Volumn 11, Issue 2, 2015, Pages

  Ahmed, Muhammad Z ^a,b   Li, Shao Jian ^a   Xue, Xia ^a   Yin, Xiang Jie ^a   Ren, Shun Xiang ^a   Jiggins, Francis M ^c   Greeff, Jaco M ^b   Qiu, Bao Li ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF PRETORIA   (South Africa)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL INFECTION; BEHAVIOR; CONTROLLED STUDY; DISEASE CARRIER; DISEASE TRANSMISSION; EGG LAYING; ENDOSYMBIONT; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC ANALYSIS; INBRED STRAIN; MALE; MULTI LOCUS SEQUENCE TYPING; MULTILOCUS SEQUENCE TYPING; NONHUMAN; OUTBRED STRAIN; PARASITOID; PHYLOGENY; POLYMERASE CHAIN REACTION; POPULATION DYNAMICS; SAMPLING; SIMULATION; SWEET POTATO WHITEFLY; WASP; WOLBACHIA; ANIMAL; CYTOPLASM; GENETICS; HEMIPTERA; METABOLISM; MICROBIOLOGY; PROCEDURES;

ALEYRODIDAE; APHELINIDAE; ARTHROPODA; BACTERIA (MICROORGANISMS); BEMISIA TABACI; HEXAPODA; VESPOIDEA; WOLBACHIA;

ANIMALS; CYTOPLASM; HEMIPTERA; IN SITU HYBRIDIZATION, FLUORESCENCE; MULTILOCUS SEQUENCE TYPING; WASPS; WOLBACHIA;

EID: 84924363466     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004672     Document Type: Article

References (59)

1. Oliver KM, Degnan PH, Burke GR, Moran NA, (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55: 247–266. doi: 10.1146/annurev-ento-112408-085305 19728837
2. Jiggins FM, Hurst GDD, (2011) Rapid insect evolution by symbiont transfer. Science 332: 185–186. doi: 10.1126/science.1205386 21474745
3. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, et al. (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332: 254–256. doi: 10.1126/science.1199410 21474763
4. Buchner P, (1965) Endosymbiosis of animals with plant microorganisms. New York: John Wiley and Sons Interscience Press. pp. 332–338.
5. Zug R, Hammerstein P, (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 7: e38544. doi: 10.1371/journal.pone.0038544 22685581
6. Russell JA, Latorre A, Sabater-Munoz B, Moya A, Moran NA, (2003) Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol 12: 1061–1075. 12753224
7. Chiel E, Zchori-Fein E, Inbar M, Gottlieb Y, Adachi-Hagimori T, et al. (2009) Almost there: transmission routes of bacterial symbionts between trophic levels. PLoS One 4: e4767. doi: 10.1371/journal.pone.0004767 19274091
8. Vavre F, Fleury F, Lepetit D, Fouillet P, Bouletreau M, (1999) Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol Biol Evol 16: 1711–1723. 10605113
9. Noda H, Miyoshi T, Zhang Q, Watanbe K, Deng K, Hoshizaki S, (2001) Wolbachia infection shared among planthoppers (Homoptera: Delphacidae) and their endoparasite (Strepsiptera: Elenchidae): a probable case of interspecies transmission. Mol Ecol 10: 2101–2106. 11555254
10. Shoemaker DD, Machado CA, Molbo D, Werren JH, Windsor DM, et al. (2002) The distribution of Wolbachia in fig wasps: correlations with host phylogeny, ecology and population structure. Proc R Soc Lond B: Biol Sci 269: 2257–2267.
11. Baldo L, Ayoub NA, Hayashi CY, Russell JA, Stahlhut JK, et al. (2008) Insight into the routes of Wolbachia invasion: high levels of horizontal transfer in the spider genus Agelenopsis revealed by Wolbachia strain and mitochondrial DNA diversity. Mol Ecol 17: 557–569. doi: 10.1111/j.1365-294X.2007.03608.x 18179432
12. Werren JH, Baldo L, Clark ME, (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741–75. doi: 10.1038/nrmicro1969 18794912
13. Ahmed MZ, De Barro PJ, Ren SX, Greeff JM, Qiu BL, (2013a) Evidence for horizontal transmission of secondary endosymbionts in the Bemisia tabaci cryptic species complex. PLoS One 8: e53084 doi: 10.1371/journal.pone.0053084 23308142
14. Boyle L, O’Neill SL, Robertson HM, Karr TL, (1993). Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260: 1796–1799. 8511587
15. Heath BD, Butcher RDJ, Whitfield WGF, Hubbard SF, (1999) Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr Biol 9: 313–316. 10209097
16. Kang L, Ma X, Cai L, Liao S, Sun L, et al. (2003) Superinfection of Laodelphax striatellus with Wolbachia from Drosophila simulans. Heredity 90: 71–76. 12522428
17. Riegler M, Charlat S, Stauffer C, Mercot H, (2004) Wolbachia transfer from Rhagoletis cerasi to Drosophila simulans: investigating the outcomes of host-symbiont coevolution. Appl Environ Microbiol 70: 273–279. 14711652
18. Zabalou S, Riegler M, Theodorakopoulou M, Stauffer C, Savakis C, et al. (2004) Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proc Natl Acad Sci USA 101: 15042–15045. 15469918
19. Huigens ME, de Almeida RP, Boons PA, Luck RF, Stouthamer R, (2004) Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc Biol Sci 1538: 509–15. 15129961
20. Huigens ME, Luck RF, Klaassen RH, Maas MF, Timmermans MJ, et al. (2000) Infectious parthenogenesis. Nature 405: 178–179. 10821272
21. Duron O, Wilkes TE, Hurst GDD, (2010) Interspecific transmission of a male-killing bacterium on an ecological timescale. Ecol Lett1 3: 1139–1148.
22. Moran NA, Dunbar HE, (2006) Sexual acquisition of beneficial symbionts in aphids. Proc Natl Acad Sci U S A 103: 12803–12806. 16908834
23. Caspi-Fluger A, Inbar M, Mozes-Daube N, Katzir N, Portnoy V, et al. (2012) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc R Soc B 279: 1791–1796. doi: 10.1098/rspb.2011.2095 22113034
24. Kikuchi Y, Hosokawa T, Fukatsu T, (2007) Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol 73: 4308–4316. 17483286
25. Gehrer L, Vorburger C, (2012) Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Lett 8: 613–615. doi: 10.1098/rsbl.2012.0144 22417790
26. Jaenike J, Polak M, Fiskin A, Helou M, Minhas M, (2007) Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 3: 23–25. 17443956
27. De Barro PJ, Liu SS, Boykin LM, Dinsdale AB, (2011) Bemisia tabaci: a statement of species status. Ann Rev Entomol 56: 1–19. doi: 10.1146/annurev-ento-112408-085504 20690829
28. Horowitz AR, Kontsedalov S, Khasdan V, Ishaaya I, . (2005) Biotypes B and Q of Bemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance. Arch Insect Biochem Physiol 58(4): 216–225. 15756703
29. Jiao XG, Xie W, Wang SL, Wu QJ, Pan HP, et al. (2013) Differences in host selection and performance between B and Q putative species of Bemisia tabaci on three host plants. Entomol Exp Appl 147(1): 1–8.
30. Su Q, Oliver KM, Pan HP, Jiao X, Liu B, et al. (2013) Facultative symbiont Hamiltonella confers benefits to Bemisia tabaci (Hemiptera: Aleyrodidae), an invasive agricultural pest worldwide. Environ Entomol 42(6): 1265–1271. doi: 10.1603/EN13182 24280594
31. Gottlieb Y, Ghanim M, Gueguen G, Kontsedalov S, Vavre F, et al. (2008) Inherited intracellular ecosystem: Symbiotic bacteria share bacteriocytes in whiteflies. FASEB J. 22:2591–99. doi: 10.1096/fj.07-101162 18285399
32. Qiu BL, Chen YP, Liu L, Peng WL, Li XX, et al. (2009) Identification of three major Bemisia tabaci biotypes in China based on morphological and DNA polymorphisms. Prog Nat Sci 19: 713–718.
33. Qiu BL, Dang F, Li SJ, Ahmed MZ, Jin FL, et al. (2011) Comparison of biological parameters between the invasive B biotype and a new defined Cv biotype of Bemisia tabaci (Hemiptera: Aleyradidae) in China. J Pest Sci 84: 419–427.
34. Qiu BL, De Barro PJ, Ren SX, (2005) Development, survivorship and reproduction of Eretmocerus sp. nr. furuhashii (Hymenoptera: Aphelinidae) parasitizing Bemisia tabaci (Hemiptera: Aleyrodidae) on glabrous and non-glabrous host plants. Bull Entomol Res 95: 313–319. 16048679
35. Li SJ, Xue X, Ahmed MZ, Ren SX, Du YZ, et al. (2011) Host plants and natural enemies of Bemisia tabaci (Homoptera: Aleyrodidae) in China. Insect Sci 18: 101–120.
36. Teixeira L, Ferreira Á, Ashburner M, (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6: e1000002.
37. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH, (2008) How many species are infected with Wolbachia?—A statistical analysis of current data. FEMS Microbiol Lett 281: 215–220. doi: 10.1111/j.1574-6968.2008.01110.x 18312577
38. Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T, (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci USA 107: 769–774. doi: 10.1073/pnas.0911476107 20080750
39. Ahmed MZ, Greyvenstein OFC, Erasmus C, Welch JJ, Greeff JM, (2013b) Consistently high incidence of Wolbachia in global fig wasp communities. Ecol Entomol 38: 147–154.
40. Kittayapong P, Jamnongluk W, Thipaksorn A, Milne JR, Sindhusake C, (2003) Wolbachia infection complexity among insects in the tropical rice-field community. Mol Ecol 12: 1049–60. 12753223
41. Verne S, Johnson M, Bouchon D, Grandjean F, (2012) Effects of parasitic sex-ratio distorters on host genetic structure in the Armadillidium vulgare Wolbachia association. J Evol Biol 25: 264–276. doi: 10.1111/j.1420-9101.2011.02413.x 22188300
42. Qiu BL, De Barro PJ, He YR, Ren SX, (2007) Suitability of Bemisia tabaci (Hemiptera: Aleyrodidae) instars for the parasitization by Encarsia bimaculata and Eretmocerus sp. nr. furuhashii (Hymenoptera: Aphelinidae) on glabrous and hirsute host plants. Biocontrol Sci Tech 17: 823–839.
43. Greenberg SM, Jones WA, Liu TX, (2008) Bemisia tabaci (Homoptera: Aleyrodidae) instar effects on rate of parasitism by Eretmocerus mundus and Encarsia pergandiella (Hymenoptera: Aphelinidae). Entomol Sci 11: 97–103. 20401334
44. McGraw EA, Merrit DJ, Droller JN, O’Neill SL, (2002) Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad Sci U S A 99: 2918–2923. 11880639
45. Chiel E, Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Katzir N, et al. (2007) Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bull Entomol Res 97: 407–413. 17645822
46. Oliver KM, Moran NA, Hunter MS, (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102: 12796–12800.
47. Scarborough CL, Ferrari J, Godfray HCJ, (2005) Aphid protected from pathogen by endosymbiont. Science 310: 1781. 16357252
48. Teixeira L, Ferreira Á, Ashburner M, (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6(12): e1000002. doi: 10.1371/journal.pbio.1000002 19222304
49. Xue X, Li SJ, Ahmed MZ, De Barro PJ, Ren SX, et al. (2012) Inactivation of Wolbachia reveals its biological roles in whitefly host. PLoS One 7: e48148. doi: 10.1371/journal.pone.0048148 23144739
50. Qiu BL, Ren SX, Wen SY, Mandour NS, (2006) Population differentiation of three biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae) in China by DNA polymorphism. J South China Agri Univ 27: 29–33.
51. Dinsdale A, Cook L, Riginos C, Buckley YM, De Barro P, (2010). Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann Entomol Soc Am 103: 196–208.
52. Ahmed MZ, De Barro PJ, Olleka A, Ren SX, Mandour NS, et al. (2012) Use of consensus sequences to identify members of the Bemisia tabaci (Hemiptera: Aleyrodidae) cryptic species complex in Egypt and Syria. J Appl Entomol 136: 510–519.
53. Ahmed MZ, Ren SX, Xue X, Li XX, Jin GH, et al. (2010) Prevalence of endosymbionts in Bemisia tabaci populations and their in vivo sensitivity to antibiotics. Curr Microbiol 61: 322–328. doi: 10.1007/s00284-010-9614-5 20217091
54. Baldo L, Hotopp JCD, Jolley KA, Bordenstein SR, Biber SA, et al. (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 72: 7098–7110. 16936055
55. Sakurai M, Koga R, Tsuchida T, Meng XY, Fukatsu T, (2005) Rickettsia symbiont in the pea aphid Acyrthosiphon pisum: novel cellular tropis, effect on host fitness, and interaction with the essential symbiont Buchnera. Appl Environ Microbiol 71: 4069–4075. 16000822
56. Bates DM, Maechler M, Bolker B, Walker S (2013) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.0–5.
57. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739. doi: 10.1093/molbev/msr121 21546353
58. Swofford DL (2002) PAUP.* Phylogenetic Analysis Using Parsimony (*And Other Methods), version 4, Sinauer Associates, Sunderland, MA.
59. Hoffmann AA, Turelli M, Harshman LG, (1990) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetic 126(4): 933–948. 2076821