The nature of the immune response in novel Wolbachia-host associations
- 423 Downloads
Wolbachia is an obligate, intracellular symbiont that is commonly found in insects and causes a diverse array of reproductive manipulations. Normally transmitted vertically, the occasional horizontal host species jump can be seen in the lack of concordance between Wolbachia and host phylogenies. In the laboratory, the symbiont can be artificially introduced into novel hosts and selected to produce persistent infections. In the case of the vector of dengue virus, Aedes aegypti, the symbiont was successfully introduced with the aim of developing the bacterium for biocontrol. In this insect and others, Wolbachia limits co-infection with pathogens including viruses, bacteria and parasites. Here we have novelly infected cell lines derived from diverse insect species with Wolbachia in an attempt to determine if there are commonalities in the early host response to the symbiont. We then monitored the expression of genes in the antibacterial Toll and Imd pathways in the first several passages. We focused on immunity gene expression as it underpins the bulk of the transcriptional response to Wolbachia and because it may play a role in the pathogen blocking effect. We found that successful cell infections of Wolbachia were difficult to achieve and often required repeated rounds of reinfection. We saw significant variation in the nature of the transcriptional changes across cell lines and no attenuation of gene expression changes in the first several passages. These results suggest that insect species are likely to exhibit distinct responses to Wolbachia infection. They also reveal that any evolution of an attenuated transcriptional response, as predicted by long-standing Wolbachia x host associations, is not likely to occur rapidly. The findings will have implications for biocontrol programs that rely on the novel infection of naïve hosts.
KeywordsEvolution Innate immunity Wolbachia Dengue Endosymbiont Insects
The authors wish to thank Yi Dong for advice on cell infection approaches. We thank Hilaria Amuzu, Bradley Borges and Emily Kerton for assistance with RNA extraction and qPCR procedures.
This work was supported by an Australian Research Council Project Grant (DP1601000588) to EM.
Compliance with ethical standards
Conflict of interest
RIH and EM declare that they have no conflict of interest.
- Axford JK, Ross PA, Yeap HL, Callahan AG, Hoffmann AA (2016) Fitness of wAlbB Wolbachia infection in Aedes aegypti: parameter estimates in an outcrossed background and potential for population invasion. Am J Trop Med Hyg 94:507–516. https://doi.org/10.4269/ajtmh.15-0608 CrossRefPubMedPubMedCentralGoogle Scholar
- Bonferroni CE (1935) Il calcolo delle assicurazioni su gruppi di teste. Studi in Onore del Professore Salvatore Ortu Carboni. Rome, ItalyGoogle Scholar
- Caragata EP, Pais FS, Baton LA, Silva JB, Sorgine MH, Moreira LA (2017) The transcriptome of the mosquito Aedes fluviatilis (Diptera: Culicidae), and transcriptional changes associated with its native Wolbachia infection. BMC Genomics 18:6. https://doi.org/10.1186/s12864-016-3441-4 CrossRefPubMedPubMedCentralGoogle Scholar
- Kambris Z, Cook PE, Phuc HK, Sinkins SP (2009) Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 326:134-136 https://doi.org/10.1126/Science.1177531
- Kambris Z, Blagborough AM, Pinto SB, Blagrove MS, Godfray HC, Sinden RE, Sinkins SP (2010) Wolbachia stimulates immune gene expression and inhibits plasmodium development in Anopheles gambiae. PLoS Pathog 6:e1001143. https://doi.org/10.1371/journal.ppat.1001143 CrossRefPubMedPubMedCentralGoogle Scholar
- Kremer N, Charif D, Henri H, Gavory F, Wincker P, Mavingui P, Vavre F (2012) Influence of Wolbachia on host gene expression in an obligatory symbiosis. BMC Microbiol 12 Suppl 1:S7 https://doi.org/10.1186/1471-2180-12-S1-S7
- McMeniman CJ, Lane RV, Cass BN, Fong AWC, Sidhu M, Wang YF, O'Neill SL (2009) Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323:141-144 https://doi.org/10.1126/Science.1165326
- Pan X, Zhou G, Wu J, Bian G, Lu P, Raikhel AS, Xi Z (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 U S A 109:E23–E31. https://doi.org/10.1073/pnas.1116932108 CrossRefPubMedGoogle Scholar
- Pinto SB, Mariconti M, Bazzocchi C, Bandi C, Sinkins SP (2012) Wolbachia surface protein induces innate immune responses in mosquito cells. BMC Microbiol 12 Suppl 1:S11 https://doi.org/10.1186/1471-2180-12-S1-S11
- Terradas G, Joubert DA, McGraw EA (2017) The RNAi pathway plays a small part in Wolbachia-mediated blocking of dengue virus in mosquito cells. Sci Rep 7:43847Google Scholar