1887

Abstract

Insects are frequently infected with inherited facultative symbionts known to provide a range of conditionally beneficial services, including host protection. Pea aphids () often harbour the bacterium which together with its associated bacteriophage secondary endosymbiont (APSE) confer protection against an important natural enemy, the parasitic wasp . Previous studies showed that spontaneous loss of phage APSE resulted in the complete loss of the protective phenotype. Here, we demonstrate that APSEs can be experimentally transferred into phage-free (i.e. non-protecting) strains. Unexpectedly, trials using injections of phage particles alone failed, with successful transfer occurring only when APSE and were simultaneously injected. After transfer, stable establishment of APSE fully restored anti-parasitoid defenses. Thus, phages associated with heritable bacterial symbionts can move horizontally among symbiont strains facilitating the rapid transfer of ecologically important traits although natural barriers may preclude regular exchange.

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2019-09-01
2019-09-18
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References

  1. Touchon M, Moura de Sousa JA, Rocha EPC. Embracing the enemy: the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer. Curr Opin Microbiol 2017;38:66–73 [CrossRef]
    [Google Scholar]
  2. Moran NA, Degnan PH, Santos SR, Dunbar HE, Ochman H. The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci USA 2005;102:16919–16926 [CrossRef]
    [Google Scholar]
  3. Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L et al. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 2008;6:27 [CrossRef]
    [Google Scholar]
  4. Oliver KM, Martinez AJ. How resident microbes modulate ecologically-important traits of insects. Curr Opin Insect Sci 2014;4:1–7 [CrossRef]
    [Google Scholar]
  5. Kent BN, Bordenstein SR. Phage WO of Wolbachia: lambda of the endosymbiont world. Trends Microbiol 2010;18:173–181 [CrossRef]
    [Google Scholar]
  6. Weldon SR, Oliver KM. Diverse bacteriophage roles in an aphid-bacterial defensive mutualism In the Mechanistic Benefits of Microbial Symbionts Springer, Cham; 2016; pp173–206
    [Google Scholar]
  7. LePage DP, Metcalf JA, Bordenstein SR, On J, Perlmutter JI et al. Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature 2017;543:243–247 [CrossRef]
    [Google Scholar]
  8. Oliver KM, Degnan PH, Hunter MS, Moran NA. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 2009;325:992–994 [CrossRef]
    [Google Scholar]
  9. Weldon SR, Strand MR, Oliver KM. Phage loss and the breakdown of a defensive symbiosis in aphids. Proc Biol Sci 2013;280:20122103 [CrossRef]
    [Google Scholar]
  10. Degnan PH, Moran NA. Diverse phage-encoded toxins in a protective insect endosymbiont. Appl Environ Microbiol 2008;74:6782–6791 [CrossRef]
    [Google Scholar]
  11. Martinez AJ, Weldon SR, Oliver KM. Effects of parasitism on aphid nutritional and protective symbioses. Mol Ecol 2014;23:1594–1607 [CrossRef]
    [Google Scholar]
  12. Oliver KM, Higashi CHV. Variations on a protective theme: Hamiltonella defensa infections in aphids variably impact parasitoid success. Curr Opin Insect Sci 2019;32:1–7 [CrossRef]
    [Google Scholar]
  13. Degnan PH, Moran NA. Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage. Mol Ecol 2008;17:916–929 [CrossRef]
    [Google Scholar]
  14. Duron O. Arsenophonus insect symbionts are commonly infected with APSE, a bacteriophage involved in protective symbiosis. FEMS Microbiol Ecol 2014;90:184–194 [CrossRef]
    [Google Scholar]
  15. Brandt JW, Chevignon G, Oliver KM, Strand MR. Culture of an aphid heritable symbiont demonstrates its direct role in defence against parasitoids. Proc Biol Sci 2017;284:20171925 [CrossRef]
    [Google Scholar]
  16. Mira A, Moran NA. Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb Ecol 2002;44:137–143 [CrossRef]
    [Google Scholar]
  17. Russell JA, Weldon S, Smith AH, Kim KL, Hu Y et al. Uncovering symbiont-driven genetic diversity across North American pea aphids. Mol Ecol 2013;22:2045–2059 [CrossRef]
    [Google Scholar]
  18. Chevignon G, Boyd BM, Brandt JW, Oliver KM, Strand MR. Culture-facilitated comparative genomics of the facultative symbiont Hamiltonella defensa. Genome Biol Evol 2018;10:786–802 [CrossRef]
    [Google Scholar]
  19. Martinez AJ, Ritter SG, Doremus MR, Russell JA, Oliver KM. Aphid-encoded variability in susceptibility to a parasitoid. BMC Evol Biol 2014;14:127 [CrossRef]
    [Google Scholar]
  20. Koga R, Meng XY, Tsuchida T, Fukatsu T. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. Proc Natl Acad Sci USA 2012;109:E1230–E1237 [CrossRef]
    [Google Scholar]
  21. Oliver KM, Noge K, Huang EM, Campos JM, Becerra JX et al. Parasitic wasp responses to symbiont-based defense in aphids. BMC Biol 2012;10:11 [CrossRef]
    [Google Scholar]
  22. Doremus MR, Smith AH, Kim KL, Holder AJ, Russell JA et al. Breakdown of a defensive symbiosis, but not endogenous defences, at elevated temperatures. Mol Ecol 2018;27:2138–2151 [CrossRef]
    [Google Scholar]
  23. Chafee ME, Funk DJ, Harrison RG, Bordenstein SR. Lateral phage transfer in obligate intracellular bacteria (Wolbachia): verification from natural populations. Mol Biol Evol 2010;27:501–505 [CrossRef]
    [Google Scholar]
  24. Kent BN, Funkhouser LJ, Setia S, Bordenstein SR. Evolutionary genomics of a temperate bacteriophage in an obligate intracellular bacteria (Wolbachia). PLoS One 2011;6:e24984 [CrossRef]
    [Google Scholar]
  25. Gehrer L, Vorburger C. Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Lett 2012;8:613–615 [CrossRef]
    [Google Scholar]
  26. Oliver KM, Campos J, Moran NA, Hunter MS. Population dynamics of defensive symbionts in aphids. Proc Biol Sci 2008;275:293–299 [CrossRef]
    [Google Scholar]
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