RNA virome diversity and Wolbachia infection in individual Drosophila simulans flies

The endosymbiont bacterium Wolbachia is associated with multiple mutualistic effects on insect biology, including nutritional and antiviral properties. Wolbachia naturally occurs in Drosophila fly species, providing an operational model host to study how virome composition may be impacted by its presence. Drosophila simulans populations can carry a variety of Wolbachia strains. In particular, the wAu strain of Wolbachia has been associated with strong antiviral protection under experimental conditions. We used D. simulans sampled from the Perth Hills, Western Australia, to investigate the potential virus protective effect of the wAu strain on individual wild-caught flies. Our data revealed no appreciable variation in virus composition and abundance between Wolbachia infected/uninfected individuals associated with the presence/absence of wAu. However, it remains unclear whether wAu might impact viral infection and host survival by increasing tolerance rather than inducing complete resistance. These data also provide new insights into the natural virome diversity of D. simulans. Despite the small number of individuals sampled, we identified a repertoire of RNA viruses, including Nora virus, Galbut virus, Chaq virus, Thika virus and La Jolla virus, that have been identified in other Drosophila species. In addition, we identified five novel viruses from the families Reoviridae, Tombusviridae, Mitoviridae and Bunyaviridae. Overall, this study highlights the complex interaction between Wolbachia and RNA virus infections and provides a baseline description of the natural virome of D. simulans.

[1]  N. Segata,et al.  Large scale genome reconstructions illuminate Wolbachia evolution , 2020, Nature Communications.

[2]  E. McBryde,et al.  Modeling the potential of wAu-Wolbachia strain invasion in mosquitoes to control Aedes-borne arboviral infections , 2020, Scientific Reports.

[3]  M. T. Hague,et al.  Pervasive Effects of Wolbachia on Host Temperature Preference , 2020, mBio.

[4]  M. Shi,et al.  Unmapped RNA Virus Diversity in Termites and Their Symbionts , 2020, Viruses.

[5]  Ewa Chrostek,et al.  Wolbachia-Conferred Antiviral Protection Is Determined by Developmental Temperature , 2020, bioRxiv.

[6]  B. Foy,et al.  Partitiviruses Infecting Drosophila melanogaster and Aedes aegypti Exhibit Efficient Biparental Vertical Transmission , 2020, Journal of Virology.

[7]  P. Ryan,et al.  Stable establishment of wMel Wolbachia in Aedes aegypti populations in Yogyakarta, Indonesia , 2020, PLoS neglected tropical diseases.

[8]  M. Turelli,et al.  Evolutionary Ecology of Wolbachia Releases for Disease Control. , 2019, Annual review of genetics.

[9]  A. Hoffmann,et al.  Wolbachia supplement biotin and riboflavin to enhance reproduction in planthoppers , 2019, The ISME Journal.

[10]  S. Sinkins,et al.  Wolbachia strain wAu efficiently blocks arbovirus transmission in Aedes albopictus , 2019, bioRxiv.

[11]  Vanessa R. Marcelino,et al.  CCMetagen: comprehensive and accurate identification of eukaryotes and prokaryotes in metagenomic data , 2019, Genome Biology.

[12]  A. Hoffmann,et al.  Life History Effects Linked to an Advantage for wAu Wolbachia in Drosophila , 2019, Insects.

[13]  M. Shi,et al.  No detectable effect of Wolbachia wMel on the prevalence and abundance of the RNA virome of Drosophila melanogaster , 2018, Proceedings of the Royal Society B: Biological Sciences.

[14]  M. Eisen,et al.  Rapid Global Spread of wRi-like Wolbachia across Multiple Drosophila , 2018, Current Biology.

[15]  S. Sinkins,et al.  The Wolbachia strain wAu provides highly efficient virus transmission blocking in Aedes aegypti , 2018, PLoS pathogens.

[16]  P. Beard,et al.  Isolation of a natural DNA virus of Drosophila melanogaster, and characterisation of host resistance and immune responses , 2017, bioRxiv.

[17]  A. von Haeseler,et al.  UFBoot2: Improving the Ultrafast Bootstrap Approximation , 2017, bioRxiv.

[18]  E. McGraw,et al.  The RNAi pathway plays a small part in Wolbachia-mediated blocking of dengue virus in mosquito cells , 2017, Scientific Reports.

[19]  E. Kiseleva,et al.  Drosophila melanogaster brain invasion: pathogenic Wolbachia in central nervous system of the fly , 2016, Insect science.

[20]  J. Ballard,et al.  Wolbachia Associations with Insects: Winning or Losing Against a Master Manipulator , 2016, Front. Ecol. Evol..

[21]  Karyn N. Johnson.  The Impact of Wolbachia on Virus Infection in Mosquitoes , 2015, Viruses.

[22]  P. Hammerstein,et al.  Wolbachia and the insect immune system: what reactive oxygen species can tell us about the mechanisms of Wolbachia–host interactions , 2015, Front. Microbiol..

[23]  Claire L. Webster,et al.  The Discovery, Distribution, and Evolution of Viruses Associated with Drosophila melanogaster , 2015, bioRxiv.

[24]  P. Hammerstein,et al.  Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts , 2015, Biological reviews of the Cambridge Philosophical Society.

[25]  Chao Xie,et al.  Fast and sensitive protein alignment using DIAMOND , 2014, Nature Methods.

[26]  A. von Haeseler,et al.  IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies , 2014, Molecular biology and evolution.

[27]  F. Jiggins,et al.  Symbionts Commonly Provide Broad Spectrum Resistance to Viruses in Insects: A Comparative Analysis of Wolbachia Strains , 2014, PLoS pathogens.

[28]  M. Hattori,et al.  Evolutionary origin of insect–Wolbachia nutritional mutualism , 2014, Proceedings of the National Academy of Sciences.

[29]  J. Sánchez-González,et al.  Susceptibility of Drosophila suzukii Matsumura (Diptera: Drosophilidae) to Entomophatogenic Fungi , 2014 .

[30]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[31]  A. Weeks,et al.  Rapid Sequential Spread of Two Wolbachia Variants in Drosophila simulans , 2013, PLoS pathogens.

[32]  James Angus Chandler,et al.  Discovery of Trypanosomatid Parasites in Globally Distributed Drosophila Species , 2013, PloS one.

[33]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[34]  Karyn N. Johnson,et al.  Antiviral Protection and the Importance of Wolbachia Density and Tissue Tropism in Drosophila simulans , 2012, Applied and Environmental Microbiology.

[35]  M. Woolfit,et al.  The Relative Importance of Innate Immune Priming in Wolbachia-Mediated Dengue Interference , 2012, PLoS pathogens.

[36]  Karyn N. Johnson,et al.  Solving the Wolbachia Paradox: Modeling the Tripartite Interaction between Host, Wolbachia, and a Natural Enemy , 2011, The American Naturalist.

[37]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

[38]  N. Friedman,et al.  Trinity : reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2016 .

[39]  F. Jiggins,et al.  Trypanosomatids are common and diverse parasites of Drosophila , 2011, Parasitology.

[40]  Peter A. Ryan,et al.  A Wolbachia Symbiont in Aedes aegypti Limits Infection with Dengue, Chikungunya, and Plasmodium , 2009, Cell.

[41]  T. Fukatsu,et al.  Wolbachia as a bacteriocyte-associated nutritional mutualist , 2009, Proceedings of the National Academy of Sciences.

[42]  Karyn N. Johnson,et al.  Variation in Antiviral Protection Mediated by Different Wolbachia Strains in Drosophila simulans , 2009, PLoS pathogens.

[43]  A. Failloux,et al.  Persistent Wolbachia and Cultivable Bacteria Infection in the Reproductive and Somatic Tissues of the Mosquito Vector Aedes albopictus , 2009, PloS one.

[44]  D. Hultmark,et al.  The Drosophila Nora virus is an enteric virus, transmitted via feces. , 2009, Journal of invertebrate pathology.

[45]  E. Feil,et al.  How Diverse Is the Genus Wolbachia? Multiple-Gene Sequencing Reveals a Putatively New Wolbachia Supergroup Recovered from Spider Mites (Acari: Tetranychidae) , 2008, Applied and Environmental Microbiology.

[46]  M. Ashburner,et al.  The Bacterial Symbiont Wolbachia Induces Resistance to RNA Viral Infections in Drosophila melanogaster , 2008, PLoS biology.

[47]  Karyn N. Johnson,et al.  Wolbachia and Virus Protection in Insects , 2008, Science.

[48]  S. O'Neill,et al.  Wolbachia-host interactions: connecting phenotype to genotype. , 2007, Current opinion in microbiology.

[49]  Drew N. Robson,et al.  Somatic stem cell niche tropism in Wolbachia , 2006, Nature.

[50]  J. Werren,et al.  Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. , 2005, Microbiology.

[51]  A. Weeks,et al.  Microsatellites isolated from diamondback moth, Plutella xylostella (L.), for studies of dispersal in Australian populations , 2005 .

[52]  Wen-Jer Wu,et al.  Molecular (Sub)Grouping of Endosymbiont Wolbachia Infection Among Mosquitoes of Taiwan , 2004, Journal of medical entomology.

[53]  J. Marlowe,et al.  Protozoan and intracellular fungal gut endosymbionts in Drosophila: prevalence and fitness effects of single and dual infections. , 2003, Journal of invertebrate pathology.

[54]  Rolf Apweiler,et al.  InterProScan - an integration platform for the signature-recognition methods in InterPro , 2001, Bioinform..

[55]  M. Hochberg,et al.  Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[56]  I. Longden,et al.  EMBOSS: the European Molecular Biology Open Software Suite. , 2000, Trends in genetics : TIG.

[57]  F. Rousset,et al.  Wolbachia infections are distributed throughout insect somatic and germ line tissues. , 1999, Insect biochemistry and molecular biology.

[58]  B. Lemaître,et al.  The Dorsoventral Regulatory Gene Cassette spätzle/Toll/cactus Controls the Potent Antifungal Response in Drosophila Adults , 1996, Cell.

[59]  M. Turelli,et al.  Rapid spread of an inherited incompatibility factor in California Drosophila , 1991, Nature.

[60]  P. Parsons,et al.  The Population Biology of Australian Drosophila , 1979 .

[61]  A. Hoffmann,et al.  Book Reviews , 1949, Heredity.

[62]  J. Felsenstein.  Evolutionary trees from DNA sequences: A maximum likelihood approach , 2005, Journal of Molecular Evolution.

[63]  J. Marlowe,et al.  Trypanosomatid prevalence and host habitat choice in woodland Drosophila. , 2001, Journal of invertebrate pathology.

[64]  M. Blaxter,et al.  Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. , 1999, The Journal of clinical investigation.

[65]  John H. Werren,et al.  Influential passengers: inherited microorganisms and arthropod reproduction , 1997 .

[66]  A. Hoffmann,et al.  Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility , 1996, Heredity.

[67]  M. Ashburner,et al.  Historical Biogeography of the Drosophila melanogaster Species Subgroup , 1988 .

[68]  W. B. Mather.  Additions to the Drosophila fauna of Australia , 1969 .