Transgenic expression of cif genes from Wolbachia strain wAlbB recapitulates cytoplasmic incompatibility in Aedes aegypti.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
29 Jan 2024
29 Jan 2024
Historique:
received:
24
08
2023
accepted:
16
01
2024
medline:
30
1
2024
pubmed:
30
1
2024
entrez:
29
1
2024
Statut:
epublish
Résumé
The endosymbiotic bacteria Wolbachia can invade insect populations by modifying host reproduction through cytoplasmic incompatibility (CI), an effect that results in embryonic lethality when Wolbachia-carrying males mate with Wolbachia-free females. Here we describe a transgenic system for recreating CI in the major arbovirus vector Aedes aegypti using CI factor (cif) genes from wAlbB, a Wolbachia strain currently being deployed to reduce dengue transmission. CI-like sterility is induced when cifA and cifB are co-expressed in testes; this sterility is rescued by maternal cifA expression, thereby reproducing the pattern of Wolbachia-induced CI. Expression of cifB alone is associated with extensive DNA damage and disrupted spermatogenesis. The strength of rescue by maternal cifA expression is dependent on the comparative levels of cifA/cifB expression in males. These findings are consistent with CifB acting as a toxin and CifA as an antitoxin, with CifA attenuating CifB toxicity in both the male germline and in developing embryos. These findings provide important insights into the interactions between cif genes and their mechanism of activity and provide a foundation for the building of a cif gene-based drive system in Ae. aegypti.
Identifiants
pubmed: 38287029
doi: 10.1038/s41467-024-45238-7
pii: 10.1038/s41467-024-45238-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
869Subventions
Organisme : Wellcome Trust (Wellcome)
ID : 202888/Z/16/Z
Organisme : RCUK | Medical Research Council (MRC)
ID : MC_ST_CVR_2019
Informations de copyright
© 2024. The Author(s).
Références
Beckmann, J. F., Ronau, J. A. & Hochstrasser, M. A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat. Microbiol. 2, 17007 (2017).
doi: 10.1038/nmicrobiol.2017.7
pubmed: 28248294
pmcid: 5336136
LePage, D. P. et al. Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature 543, 243–247 (2017).
doi: 10.1038/nature21391
pubmed: 28241146
pmcid: 5358093
Martinez, J., Klasson, L., Welch, J. J. & Jiggins, F. M. Life and Death of Selfish Genes: Comparative Genomics Reveals the Dynamic Evolution of Cytoplasmic Incompatibility. Mol. Biol. Evol. 38, 2–15 (2021).
doi: 10.1093/molbev/msaa209
pubmed: 32797213
Sicard, M. et al. Cytoplasmic Incompatibility Variations in Relation with Wolbachia cid Genes Divergence in Culex pipiens. mBio 12, e02797-20 (2021).
doi: 10.1128/mBio.02797-20
pubmed: 33563818
pmcid: 7885119
Bonneau, M. et al. Culex pipiens crossing type diversity is governed by an amplified and polymorphic operon of Wolbachia. Nat. Commun. 9, 319 (2018).
doi: 10.1038/s41467-017-02749-w
pubmed: 29358578
pmcid: 5778026
Shropshire, J. D., Rosenberg, R. & Bordenstein, S. R. The impacts of cytoplasmic incompatibility factor (cifA and cifB) genetic variation on phenotypes. Genetics 217, 1–13 (2021).
doi: 10.1093/genetics/iyaa007
pubmed: 33683351
Chen, H., Ronau, J. A., Beckmann, J. F. & Hochstrasser, M. A Wolbachia nuclease and its binding partner provide a distinct mechanism for cytoplasmic incompatibility. Proc. Natl Acad. Sci. 116, 22314–22321 (2019).
doi: 10.1073/pnas.1914571116
pubmed: 31615889
pmcid: 6825299
Horard, B. et al. Paternal transmission of the Wolbachia CidB toxin underlies cytoplasmic incompatibility. Curr. Biol. 32, 1319–1331.e5 (2022).
doi: 10.1016/j.cub.2022.01.052
pubmed: 35134330
Shropshire, J. D. & Bordenstein, S. R. Two-By-One model of cytoplasmic incompatibility: Synthetic recapitulation by transgenic expression of cifA and cifB in Drosophila. PLoS Genet. 15, e1008221 (2019).
doi: 10.1371/journal.pgen.1008221
pubmed: 31242186
pmcid: 6594578
Sun, G., Zhang, M., Chen, H. & Hochstrasser, M. The CinB Nuclease from w No Wolbachia Is Sufficient for Induction of Cytoplasmic Incompatibility in Drosophila. mBio 13, e0317721 (2022).
doi: 10.1128/mbio.03177-21
pubmed: 35073749
Adams, K. L. et al. Wolbachia cifB induces cytoplasmic incompatibility in the malaria mosquito vector. Nat. Microbiol. 6, 1575–1582 (2021).
doi: 10.1038/s41564-021-00998-6
pubmed: 34819638
pmcid: 8612931
Xiao, Y. et al. Structural and mechanistic insights into the complexes formed by Wolbachia cytoplasmic incompatibility factors. Proc. Natl Acad. Sci. 118, e2107699118 (2021).
doi: 10.1073/pnas.2107699118
pubmed: 34620712
pmcid: 8522278
Wang, H. et al. Crystal Structures of Wolbachia CidA and CidB Reveal Determinants of Bacteria-induced Cytoplasmic Incompatibility and Rescue. Nat. Commun. 13, 1608 (2022).
doi: 10.1038/s41467-022-29273-w
pubmed: 35338130
pmcid: 8956670
Beckmann, J. F., Van Vaerenberghe, K., Akwa, D. E. & Cooper, B. S. A single mutation weakens symbiont-induced reproductive manipulation through reductions in deubiquitylation efficiency. Proc. Natl Acad. Sci. 118, e2113271118 (2021).
doi: 10.1073/pnas.2113271118
pubmed: 34548405
pmcid: 8488622
Beckmann, J. F. et al. The Toxin–Antidote Model of Cytoplasmic Incompatibility: Genetics and Evolutionary Implications. Trends Genet. 35, 175–185 (2019).
doi: 10.1016/j.tig.2018.12.004
pubmed: 30685209
pmcid: 6519454
Shropshire, J. D., Leigh, B. & Bordenstein, S. R. Symbiont-mediated cytoplasmic incompatibility: What have we learned in 50 years? Elife 9, e61989 (2020).
doi: 10.7554/eLife.61989
pubmed: 32975515
pmcid: 7518888
Terretaz, K., Horard, B., Weill, M., Loppin, B. & Landmann, F. Functional analysis of Wolbachia Cid effectors unravels cooperative interactions to target host chromatin during replication. PLoS Pathog. 19, e1011211 (2023).
doi: 10.1371/journal.ppat.1011211
pubmed: 36928089
pmcid: 10047532
Kaur R., Shropshire J. D., Leigh B. A., Bordenstein S. R. Nuclease proteins CifA and CifB promote spermatid DNA damage associated with symbiont-induced cytoplasmic incompatibility. bioRxiv https://doi.org/10.1101/2022.04.04.487029 (2022).
Namias, A., Sicard, M., Weill, M. & Charlat, S. From Wolbachia genomics to phenotype: molecular models of cytoplasmic incompatibility must account for the multiplicity of compatibility types. Curr. Opin. Insect Sci. 49, 78–84 (2022).
doi: 10.1016/j.cois.2021.12.005
pubmed: 34954414
Ross, P. A. et al. An elusive endosymbiont: Does Wolbachia occur naturally in Aedes aegypti? Ecol. Evol. 10, 1581–1591 (2020).
doi: 10.1002/ece3.6012
pubmed: 32076535
pmcid: 7029055
Xi, Z., Khoo, C. C. H. & Dobson, S. L. Wolbachia Establishment and Invasion in an Aedes aegypti Laboratory Population. Science 310, 326–328 (2005).
doi: 10.1126/science.1117607
pubmed: 16224027
Fraser, J. E. et al. Novel Wolbachia-transinfected Aedes aegypti mosquitoes possess diverse fitness and vector competence phenotypes. PLoS Pathog. 13, e1006751 (2017).
doi: 10.1371/journal.ppat.1006751
pubmed: 29216317
pmcid: 5736235
McMeniman, C. J. et al. Stable Introduction of a Life-Shortening Wolbachia Infection into the Mosquito Aedes aegypti. Science 323, 141–144 (2009).
doi: 10.1126/science.1165326
pubmed: 19119237
Hughes, G. L. & Rasgon, J. L. Transinfection: a method to investigate Wolbachia -host interactions and control arthropod-borne disease. Insect Mol. Biol. 23, 141–151 (2014).
doi: 10.1111/imb.12066
pubmed: 24329998
Hoffmann, A. A., Ross, P. A. & Rašić, G. Wolbachia strains for disease control: ecological and evolutionary considerations. Evol. Appl. 8, 751–768 (2015).
doi: 10.1111/eva.12286
pubmed: 26366194
pmcid: 4561566
Ryan, P. A. et al. Establishment of wMel Wolbachia in Aedes aegypti mosquitoes and reduction of local dengue transmission in Cairns and surrounding locations in northern Queensland, Australia. Gates Open Res. 3, 1547 (2020).
doi: 10.12688/gatesopenres.13061.2
pubmed: 31667465
pmcid: 6801363
Pinto, S. B. et al. Effectiveness of Wolbachia-infected mosquito deployments in reducing the incidence of dengue and other Aedes-borne diseases in Niterói, Brazil: A quasi-experimental study. PLoS Negl. Trop. Dis. 15, e0009556 (2021).
doi: 10.1371/journal.pntd.0009556
pubmed: 34252106
pmcid: 8297942
Utarini, A. et al. Efficacy of Wolbachia-Infected Mosquito Deployments for the Control of Dengue. N. Engl. J. Med. 384, 2177–2186 (2021).
doi: 10.1056/NEJMoa2030243
pubmed: 34107180
pmcid: 8103655
Nazni, W. A. et al. Establishment of Wolbachia Strain wAlbB in Malaysian Populations of Aedes aegypti for Dengue Control. Curr. Biol. 29, 4241–4248.e5 (2019).
doi: 10.1016/j.cub.2019.11.007
pubmed: 31761702
pmcid: 6926472
Crawford, J. E. et al. Efficient production of male Wolbachia-infected Aedes aegypti mosquitoes enables large-scale suppression of wild populations. Nat. Biotechnol. 38, 482–492 (2020).
doi: 10.1038/s41587-020-0471-x
pubmed: 32265562
Beebe, N. W. et al. Releasing incompatible males drives strong suppression across populations of wild and Wolbachia -carrying Aedes aegypti in Australia. Proc. Natl Acad. Sci. 118, e2106828118 (2021).
doi: 10.1073/pnas.2106828118
pubmed: 34607949
pmcid: 8521666
Martín-Park, A. et al. Pilot trial using mass field-releases of sterile males produced with the incompatible and sterile insect techniques as part of integrated Aedes aegypti control in Mexico. PLoS Negl. Trop. Dis. 16, e0010324 (2022).
doi: 10.1371/journal.pntd.0010324
pubmed: 35471983
pmcid: 9041844
Liu, W.-L. et al. Lab-scale characterization and semi-field trials of Wolbachia Strain wAlbB in a Taiwan Wolbachia introgressed Ae. aegypti strain. PLoS Negl. Trop. Dis. 16, e0010084 (2022).
doi: 10.1371/journal.pntd.0010084
pubmed: 35015769
pmcid: 8752028
Sinha, A., Li, Z., Sun, L. & Carlow, C. K. S. Complete Genome Sequence of the Wolbachia w AlbB Endosymbiont of Aedes albopictus. Genome Biol. Evol. 11, 706–720 (2019).
doi: 10.1093/gbe/evz025
pubmed: 30715337
pmcid: 6414309
Smith, R. C., Walter, M. F., Hice, R. H., O’Brochta, D. A. & Atkinson, P. W. Testis-specific expression of the β2 tubulin promoter of Aedes aegypti and its application as a genetic sex-separation marker. Insect Mol. Biol. 16, 61–71 (2007).
doi: 10.1111/j.1365-2583.2006.00701.x
pubmed: 17257209
Daniels, R. W., Rossano, A. J., Macleod, G. T. & Ganetzky, B. Expression of Multiple Transgenes from a Single Construct Using Viral 2A Peptides in Drosophila. PLoS One 9, e100637 (2014).
doi: 10.1371/journal.pone.0100637
pubmed: 24945148
pmcid: 4063965
Akbari, O. S., Papathanos, P. A., Sandler, J. E., Kennedy, K. & Hay, B. A. Identification of germline transcriptional regulatory elements in Aedes aegypti. Sci. Rep. 2015 4, 3954.
Darren H. E. Identification and characterization of germline-specific promoters for remobilization of transgenes in the mosquitoes, Aedes aegypti and Anopheles gambiae (Texas A&M University, 2007).
Anderson, M. A. E. et al. Closing the gap to effective gene drive in Aedes aegypti by exploiting germline regulatory elements. Nat. Commun. 14, 338 (2023).
doi: 10.1038/s41467-023-36029-7
pubmed: 36670107
pmcid: 9860013
Ant, T. H., Herd, C. S., Geoghegan, V., Hoffmann, A. A. & Sinkins, S. P. The Wolbachia strain wAu provides highly efficient virus transmission blocking in Aedes aegypti. PLoS Pathog. 14, e1006815 (2018).
doi: 10.1371/journal.ppat.1006815
pubmed: 29370307
pmcid: 5784998
Poinsot, D., Bourtzis, K., Markakis, G., Savakis, C. & Merçot, H. Wolbachia Transfer from Drosophila melanogaster into D. simulans: Host Effect and Cytoplasmic Incompatibility Relationships. Genetics 150, 227–237 (1998).
doi: 10.1093/genetics/150.1.227
pubmed: 9725842
pmcid: 1460311
Shropshire, J. D., Hamant, E. & Cooper, B. S. Male Age and Wolbachia Dynamics: Investigating How Fast and Why Bacterial Densities and Cytoplasmic Incompatibility Strengths Vary. mBio 12, e0299821 (2021).
doi: 10.1128/mbio.02998-21
pubmed: 34903056
Li, J. & Champer, J. Harnessing Wolbachia cytoplasmic incompatibility alleles for confined gene drive: A modeling study. PLoS Genet. 19, e1010591 (2023).
Morris, A. C., Eggleston, P. & Crampton, J. M. Genetic transformation of the mosquito Aedes aegypti by micro‐injection of DNA. Med Vet. Entomol. 3, 1–7 (1989).
doi: 10.1111/j.1365-2915.1989.tb00467.x
pubmed: 2519641