Wolbachia enhances the survival of Drosophila infected with fungal pathogens

Perlmutter, jessamyn I. Et AL “Wolbachia enhances the survival of drosophila infected with fungal pathogens.” biorxiv (2023): 2023.09.30.560320. web. 22 oct. 2023

Wolbachia bacteria of arthropods are at the forefront of basic and translational research on multipartite host-symbiont-pathogen interactions. These microbes are vertically inherited from mother to offspring via the cytoplasm. They are the most widespread endosymbionts on the planet due to their infamous ability to manipulate the reproduction of their hosts to spread themselves in a population, and to provide a variety of fitness benefits to their hosts. Importantly, some strains of Wolbachia can inhibit viral pathogenesis within and between arthropod hosts. Mosquitoes carrying the wMel Wolbachia strain of Drosophila melanogaster have a greatly reduced capacity to spread viruses like dengue and Zika to humans. Therefore, Wolbachia are the basis of several global vector control initiatives. While significant research efforts have focused on viruses, relatively little attention has been given to Wolbachia-fungal interactions despite the ubiquity of fungal entomopa thogens in nature. Here, we demonstrate that Wolbachia increase the longevity of their Drosophila melanogaster hosts when challenged with a spectrum of yeast and filamentous fungal pathogens. We find that this pattern can vary based on host genotype, sex, and fungal species. Further, Wolbachia correlates with higher fertility and reduced pathogen titers during initial fungal infection, indicating a significant fitness benefit. This study demonstrates Wolbachia’s role in diverse fungal pathogen interactions and determines that the phenotype is broad, but with several variables that influence both the presence and strength of the phenotype. These results enhance our knowledge of the strategies Wolbachia uses that likely contribute to such a high global symbiont prevalence.Importance Wolbachia bacteria of arthropods are at the forefront of global initiatives to fight arthropod-borne viruses. Despite great success in using the symbiont to fight viruses, little research has foc used on Wolbachia-fungal interactions. Here, we find that Wo! lbachia of Drosophila melanogaster, the same strain widely used in antiviral initiatives, can also increase the longevity of flies systemically infected with a panel of yeast and filamentous fungal pathogens. The symbiont also partially increases host fertility and reduces fungal titers during early infection, indicating a significant fitness benefit. This represents a major step forward in Wolbachia research since its pathogen blocking abilities can now be extended to a broad diversity of another major branch of microbial life. This discovery may inform basic research on pathogen blocking and has potential translational applications in areas including biocontrol in agriculture.Competing Interest StatementThe authors have declared no competing interest.

PREPRINTS

  • Unckless, RL, PA Lansdon and BD Ackley. 2020. A comparative analysis of Caenorhabditis and Drosophila transcriptional changes in response to pathogen infection. biorXiv: 977595. PDF

  • Gupta, Anjali, and Robert L. Unckless. "Autosomal suppression of meiotic drive can prevent sex chromosome cycling." bioRxiv (2023): 2023.09.28.559847. bioRxiv

  • Perlmutter, Jessamyn I. et al "Wolbachia enhances the survival of Drosophila infected with fungal pathogens." bioRxiv (2023): 2023.09.30.560320. PDF

  • Hernández, José Fabricio López et al "Modeling the Evolution of Populations with Multiple Killer Meiotic Drivers." bioRxiv (2023): 2023.09.28.560003. PDF

  • Mullinax, Sarah R. et al "A suite of selective pressures supports the maintenance of alleles of a Drosophila immune peptide." bioRxiv (2023): 2023.08.18.553899. PubMed

  • Perlmutter, Jessamyn I. et al "A single amino acid polymorphism in natural Metchnikowin alleles of Drosophila results in systemic immunity and life history tradeoffs." bioRxiv (2023): 2023.01.16.524277. PDF

Prior publications

2023

  • YM Alhammad, S Parthasarathy, R Ghimire, CM Kerr, JJ O’Connor, JJ Pfannenstiel, D Chanda, CA Miller, N Baumlin, M Salathe, RL Unckless, S Zuñiga, L Enjuanes, S More, R Channappanavar, AR Fehr. 2023. SARS-CoV-2 Mac1 is required for IFN antagonism and efficient virus replication in cell culture and in mice. PNAS. Doi: 10.1073/pnas.2302083120 (link to PNAS)

  • KL Vertacnik, DK Herrig, RK Godfrey, T Hill, SM Geib, RL Unckless, DR Nelson, CR Linnen. 2023. Ecological correlates of gene family size in a pine-feeding sawfly genome and across Hymenoptera. bioRxiv. Doi: 10.1101/2021.03.14.435331. (PDF)

  • BR Smith, KB Patch, RL Unckless. 2023. The genetic basis of variation immune defense against Lysinibacillus fusiformis infection in Drosophila melanogaster. PLOS Pathogens. Doi: 10.1101/2022.10.19.512815. (link to PLOS Pathogens)

2022

  • W Ma, EM Knoles, KB Patch, MM Shoaib, and RL Unckless, 2021. Hoisted with his own petard: how sex-ratio meiotic drive in Drosophila affinis creates resistance alleles that limit its spread. Journal of Evolutionary Biology. Doi:10.1111/jeb.14077. (link to JEB)

  • RP Meisel, D Asgari, F Schlamp, and RL Unckless, 2021. Induction and inhibition of Drosophila X chromosome gene expression are both impeded by the dosage compensation complex. G3: jkac165. Doi: 10.1093/g3journal/jkac165. (link to G3)

  • CR Linnen, Y Brandvain, and RL Unckless. 2022. Theme: Recent work in speciation research by women authors. Evolution 76: 1100-1103. doi:10.1111/evo.14444. (link to Evolution)

  • ME Ochs, RM McWhirter, RL Unckless, DM Miller III, EA Lundquist. 2021. Caenorhabditis elegans ETR-1/CELF has broad effects on the muscle cell transcriptome, including genes that regulate translation and neuroblast migration. BMC Genomics: 23,1 13. doi:10.1186/s12864-021-08217-6. (link to BMC Genomics)

  •  Hill, T, RL Unckless and JI Perlmutter. 2020. Positive selection and horizontal gene transfer in the genome of a male-killing Wolbachia. Molecular Biology and Evolution: 39: msab303. Doi: 10.1093/molbev/msab303. (link to MBE)

2021

  • Hill, T, HL Rosales-Stephens, and RL Unckless. 2021. Rapid divergence of the copulation proteins in the Drosophila dunni group is associated with hybrid post-mating-prezygotic incompatibilities. G3: 11:jkab050. PDF

  • Hill, T and RL Unckless. 2021. Adaptation, ancestral variation and gene flow in a ‘Sky Island’ Drosophila species. Molecular Ecology 30:83-99. doi: 10.1111/mec.15701. PDF

2020

  • Hill, T and RL Unckless. 2020. Recurrent evolution of two competing haplotypes in an insect DNA virus. bioRXiv: 10.1101/2020.0514.096024. eLife: e58931. doi: 10.7554/elife.58931. PDF

  • Price, TA, Windbichler, N, RL Unckless, et al. 2020. Resistance to natural and synthetic gene drive systems. Journal of Evolutionary Biology 33: 1345-1360. (link to Journal of Evolutionary Biology)

  • Bravo Nunez, MA, IM Sabbarini, LE Eide, RL Unckless and SE Zanders. 2020. Atypical meiosis can be adaptive in outcrossed S. pombe due to wtf meiotic drivers. eLife: 9:e57936. (link to eLife)

  • Chapman, JR, MA Dowell, R Chan and RL Unckless. 2020. The genetic basis of natural variation in Drosophila melanogaster immune defence against Enterococcus faecalis. Genes: 11:234. (link to Genes)

  • Unckless, RL and HA Orr. 2020. The population genetics of evolutionary rescue in diploids: X chromosomal vs. autosomal rescue. The American Naturalist: 195: 561-568. (link to The American Naturalist)

2019

  • Hanson, MA, B Lemaitre, and RL Unckless. 2019. Dynamic evolution of antimicrobial peptides underscores trade-offs between immunity and ecological fitness. Frontiers in immunology 10: 2620. (link to Frontiers)

  • Chapman, JR, T Hill and RL Unckless. 2019. Balancing selection drives the maintenance of genetic variation in Drosophila antimicrobial peptides. Genome Biology and Evolution: 11: 2691-2701. (doi: 10.1093/gbe/evz191) (link to GBE)

  • Hill, T and RL Unckless. 2019. A deep learning approach for detecting copy number variation in next generation sequencing. G3: Genes, Genomes, Genetics 9: 3575-3582. doi: 10.1534/g3.119.400596. (link to G3)

  • Benomar, S, KC Evans, RL Unckless and JR Chandler. 2019. Efflux pumps in Chromobacterium species increase antibiotic resistance and promote survival in a co-culture competition model. Appled and environmental microbiology: 85: e00908-19. doi: 10.1128/AEM.00908-19. (link to AEM)

  • Lea, JK and RL Unckless. 2019. An assessment of the immune costs associated with meiotic drive chromosomes in Drosophila. Proceedings of the Royal Society B. 286: 20191534 (doi: 10.1098/rspb.2019.1534) (link to PRSB)

  • Perlmutter, JI, SR Bordenstein, RL Unckless, DP LePage, J Metcalf, T Hill, J Martinez, FM Jiggins, SR Bordenstein. 2019. The phage gene wmk is a candidate for male killing by a bacterial endosymbiont. PLOS Pathogens 15(9): e1007936. (doi: 10.1371/journal.ppat.1007936) (link to PLOS Pathogens)

  • Hill, T, BS Koseva and RL Unckless. 2019. The genome of Drosophila innubila reveals lineage-specific patterns of selection in immune genes. Molecular Biology and Evolution Advanced access. doi: 10.1093/molbev/msz059 (link to MBE)

  • Zanders, SE and RL Unckless. 2019. Fertility costs of meiotic drivers. Current Biology 29:R512-R520. doi: 10.1016/j.cub.2019.03.046. (link to Current Biology)

  • Duxbury, EML, JP Day, DM Vespasiani, Y Thuringer, I Tolosana, SCL Smtih, L Tagliaferri, A KAacioglu, I Lindsley, L Love, RL Unckless, FM Jiggins and B Longdon. 2019. Host-pathogen coevolution increases genetic variation in susceptibility to infection. eLife 8: e46440. doi:10.7554/eLife.46440. (link to eLife)

2018

  • Pieper, KM, RL Unckless and KA Dyer. 2018. A fast-evolving X-linked duplicate of importin-a2 is overexpressed in sex-ratio drive in Drosophila neotestacea. Molecular ecology 27(24): 5165-5179. doi:10.1111/mec.14928.

  • Smith, BR and RL Unckless. 2018. Draft genome of Lysinibacillus fusiformis Strain Juneja, a laboratory-derived pathogen of Drosophila melanogaster. Genome Announcements 6(5), e01571-17. doi:10.1128/genomeA.01571-17.

  • Hill, T and R.L. Unckless. 2018. The dynamic evolution of the Drosophila innubila Nudivirus. Infection, Genetics and Evolution 57: 151-157. doi:10.1016/j.meegid.2017.11.013.

2017

  • Hill, T. and R.L. Unckless. 2017. 2017. Baculovirus molecular evolution via gene turnover and recurrent positive selection of key genes. Journal of Virology 91: e01319-17. doi: 10.1128/JVI.01319-17.

  • Ahmed-Braimah, Y.H., R.L. Unckless and A.G. Clark. 2017. Evolutionary dynamics of male reproductive genes in the Drosophila virilis subgroup. G3: Genes, Genomes, Genetics 2017;7(9):3145-55. doi:10.1534/g3.117.1136.

2016

  • Akhund-Zade, J., A.O. Bergland and R.L. Unckless. 2016. The genetic basis of natural variation in virgin egg retention in Drosophila melanogaster (Diptera: Drosophilidae). Journal of Insect Science 17(1). doi:10.1093/jisesa/iew094.

  • Lindholm, AK, … RL Unckless, et al. (22 authors). 2016. The ecology and evolutionary dynamics of meiotic drive. Trends in Ecology and Evolution 31:315-326. doi:10.1016/j.tree.2016.02.001.

  • Unckless, RL and BP Lazzaro. 2016. The potential for adaptive maintenance of diversity in insect antimicrobial peptides. Philisophical Transactions of the Royal Society B 371:20150291. doi: 10.1098/rstb.2015.0291.

  • Unckless, RL, VM Howick and BP Lazzaro. 2016. Convergent balancing selection on an antimicrobial peptide in Drosophila. Current Biology 26:257-262. Doi: 10.1016/j.cub.2015.11.063

2015

  • Unckless, RL and AG Clark. 2015. Driven to extinction: on the probability of evolutionary rescue from sex-ratio meiotic drive. bioRxiv doi: http://dx.doi.org/10.1101/018820.

  • Unckless, RL, PW Messer T Connallon and AG Clark. 2015. Modeling the Manipulation of Natural Populations by the Mutagenic Chain Reaction. Genetics 201:425-431. doi: 10.1534/genetics.115.177592 (Highlighted article).

  • Unckless, RL, SM Rottschaefer and BP Lazzaro. 2015. The Complex Contributions of Genetics and Nutrition to Immunity in Drosophila melanogaster. PLoS Genet 11: e1005030. doi:10.1371/journal.pgen.1005030

  • Unckless, RL, SM Rottschaefer and BP Lazzaro. 2015. A genome-wide association study for nutritional indices in Drosophila. Genes, Genomes and Genetics 5:417-425. doi: 10.1534/g3.114.016477.

  • Unckless, RL, AM Larracuente and AG Clark. 2015. Sex-ratio meiotic drive and Y-linked resistance in Drosophila affinis. Genetics 199:831-840. doi:10.1534/genetics.114.173948.

2014

  • Orr, HA and RL Unckless. 2014. The population genetics of evolutionary rescue. PLoS Genetics 10(8): e104551.

  • Unckless, RL and AG Clark. 2014. Sex-ratio meiotic drive and interspecific competition. Journal of Evolutionary Biology 27(8): 1513-1521.

Prior to 2014

  • Unckless, RL and J Jaenike. 2012. Maintenance of a male-killing Wolbachia in Drosophila innubila by male-killing dependent and male-killing independent mechanisms. Evolution 66(3):678-689.

  • Unckless, RL. 2011. The potential role of the X chromosome in the emergence of male-killing from mutualistic endosymbionts. Journal of Theoretical Biology 291: 99-104.

  • Unckless, RL. 2011. A DNA virus of Drosophila. PLoS ONE 6: e26564.

  • Jaenike J, RL Unckless, SN Cockburn, LM Boelio, and SJ Perlman. 2010. Adaptive evolution via symbiosis: recent spread of a defensive symbiont in Drosophila. Science 329: 212-215.

  • Unckless, RL and HA Orr. 2009. The population genetics of adaptation: multiple substitutions on a smooth fitness landscape. Genetics 183: 1079-1086.

  • Jaenike J, JK Stahlhut, LM Boelio and RL Unckless. 2009. Association between Wolbachia and Spiroplasma within Drosophila neotestacea: an emerging symbiotic mutualism. Molecular Ecology 19: 414-425.

  • Unckless, RL and JK Herren. 2009. Population genetics of sexually antagonistic mitochondrial mutants under inbreeding. Journal of Theoretical Biology 260: 132-136.

  • Unckless, RL, LM Boelio, JK Herren and J Jaenike. 2009. Wolbachia as populations within individual insects: causes and consequences of density variation in natural populations. Proceedings of the Royal Society B 276: 2805-2811.

  • Unckless, RL, LM Boelio, C Cornish and KA Dyer. 2008. Isolation and characterization of 30 polymorphic microsatellite loci from the mycophagous fly Drosophila innubila. Molecular Ecology Research 8: 939-942.

  • Unckless, RL and HA Orr. 2009. Dobzhansky-Muller incompatibilities and adaptation to a shared environment. Heredity 102: 214-217.

  • Orr, HA and RL Unckless. 2008. Population extinction and the genetics of adaptation. American Naturalist 172: 160-169.

  • Unckless, RL and J Makarewicz. 2007. The impact of nutrient loading from Canada Geese (Branta canadensis) on water quality, a mesocosm approach. Hydrobiologia 586: 391-401.