Infection Dynamics and Immune Response in a Newly Described Drosophila-Trypanosomatid Association

Trypanosomatid parasites are significant causes of human disease and are ubiquitous in insects. Despite the importance of Drosophila melanogaster as a model of infection and immunity and a long awareness that trypanosomatid infection is common in the genus, no trypanosomatid parasites naturally infecting Drosophila have been characterized. Here, we establish a new model of trypanosomatid infection in Drosophila-Jaenimonas drosophilae, gen. et sp. nov. As far as we are aware, this is the first Drosophila-parasitic trypanosomatid to be cultured and characterized. Through experimental infections, we find that Drosophila falleni, the natural host, is highly susceptible to infection, leading to a substantial decrease in host fecundity. J. drosophilae has a broad host range, readily infecting a number of Drosophila species, including D. melanogaster, with oral infection of D. melanogaster larvae resulting in the induction of numerous immune genes. When injected into adult hemolymph, J. drosophilae kills D. melanogaster, although interestingly, neither the Imd nor the Toll pathway is induced and Imd mutants do not show increased susceptibility to infection. In contrast, mutants deficient in drosocrystallin, a major component of the peritrophic matrix, are more severely infected during oral infection, suggesting that the peritrophic matrix plays an important role in mediating trypanosomatid infection in Drosophila. This work demonstrates that the J. drosophilae-Drosophila system can be a powerful model to uncover the effects of trypanosomatids in their insect hosts. IMPORTANCE Trypanosomatid parasites are ubiquitous in insects and are significant causes of disease when vectored to humans by blood-feeding insects. In recent decades, Drosophila has emerged as the predominant insect model of infection and immunity and is also known to be infected by trypanosomatids at high rates in the wild. Despite this, there has been almost no work on their trypanosomatid parasites, in part because Drosophila-specific trypanosomatids have been resistant to culturing. Here, we present the first isolation and detailed characterization of a trypanosomatid from Drosophila, finding that it represents a new genus and species, Jaenimonas drosophilae. Using this parasite, we conducted a series of experiments that revealed many of the unknown aspects of trypanosomatid infection in Drosophila, including host range, transmission biology, dynamics of infection, and host immune response. Taken together, this work establishes J. drosophilae as a powerful new opportunity to study trypanosomatid infections in insects

The inherited symbionts of <i>Drosophila</i>.

<p>The inherited symbionts of <i>Drosophila</i>.</p

Hamilton_etal_2018_Liposcelis_Data

Compiled data from 'Genetics and genomics of an unusual selfish sex ratio distortion in an insect'. Contains seven files, including genome and transcriptome assemblies, as well as read mappings. See included outline for more details

Data from: Genetics and genomics of an unusual selfish sex ratio distortion in an insect

Diverse selfish genetic elements have evolved the ability to manipulate reproduction to increase their transmission, and this can result in highly distorted sex ratios. Indeed, one of the major explanations for why sex determination systems are so dynamic is because they are shaped by ongoing coevolutionary arms races between sex ratio distorting elements and the rest of the genome. Here, we use genetic crosses and genome analysis to describe an unusual sex ratio distortion with striking consequences on genome organization in a booklouse species, Liposcelis sp. (Insecta: Psocodea), in which two types of females coexist. Distorter females never produce sons but must mate with males (the sons of nondistorting females) to reproduce. Although they are diploid and express the genes inherited from their fathers in somatic tissues, distorter females only ever transmit genes inherited from their mothers. As a result, distorter females have unusual chimeric genomes, with distorter-restricted chromosomes diverging from their nondistorting counterparts and exhibiting features of a giant nonrecombining sex chromosome. The distorter-restricted genome has also acquired a gene from the bacterium Wolbachia, a well-known insect reproductive manipulator; we found that this gene has independently colonized the genomes of two other insect species with unusual reproductive systems suggesting possible roles in sex ratio distortion in this remarkable genetic system

Data from: Transcriptional responses in a Drosophila defensive symbiosis

Inherited symbionts are ubiquitous in insects and can have important consequences for the fitness of their hosts. Many inherited symbionts defend their hosts against parasites or other natural enemies; however, the means by which most symbionts confer protection is virtually unknown. We examine the mechanisms of defence in a recently discovered case of symbiont-mediated protection, where the bacterial symbiont Spiroplasma defends the fly Drosophila neotestacea from a virulent nematode parasite, Howardula aoronymphium. Using quantitative PCR of Spiroplasma infection intensities and whole transcriptome sequencing, we attempt to distinguish between the following modes of defence: symbiont–parasite competition, host immune priming and the production of toxic factors by Spiroplasma. Our findings do not support a model of exploitative competition between Howardula and Spiroplasma to mediate defence, nor do we find strong support for host immune priming during Spiroplasma infection. Interestingly, we recovered sequence for putative toxins encoded by Spiroplasma, including a novel putative ribosome-inactivating protein, transcripts of which are up-regulated in response to nematode exposure. Protection via the production of toxins may be a widely used and important mechanism in heritable defensive symbioses in insects

Data from: Infectious adaptation: potential host range of a defensive endosymbiont in Drosophila

Maternally transmitted symbionts persist over macroevolutionary time scales by undergoing occasional lateral transfer to new host species. To invade a new species, a symbiont must survive and reproduce in the new host, undergo maternal transmission, and confer a selective benefit sufficient to overcome losses due to imperfect maternal transmission. Drosophila neotestacea is naturally infected with a strain of Spiroplasma that restores fertility to nematode-parasitized females, which are otherwise sterilized by parasitism. We experimentally transferred Spiroplasma from D. neotestacea to four other species of mycophagous Drosophila that vary in their ability to resist and/or tolerate nematode parasitism. In all four species, Spiroplasma achieved within-host densities and experienced rates of maternal transmission similar to that in D. neotestacea. Spiroplasma restored fertility to nematode-parasitized females in one of these novel host species. Based on estimates of maternal transmission fidelity and the expected benefit of Spiroplasma infection in the wild, we conclude that Spiroplasma has the potential to spread and become abundant within D. putrida, which is broadly sympatric with D. neotestacea and in which females are rendered completely sterile by nematode parasitism. Thus, a major adaptation within D. putrida could arise via lateral transmission of a heritable symbiont from D. neotestacea

Data from: Dynamics of the continent-wide spread of a Drosophila defensive symbiont

Facultative symbionts can represent important sources of adaptation for their insect hosts and thus have the potential for rapid spread. Drosophila neotestacea harbors a heritable symbiont, Spiroplasma, that confers protection against parasitic nematodes. We previously found a cline in Spiroplasma prevalence across central Canada, ending abruptly at the Rocky Mountains. Resampling these populations nine years later revealed that Spiroplasma had increased substantially across the region, resembling a Fisherian wave of advance. Associations between Spiroplasma infection and host mitochondrial DNA indicate that the increase was due to local increase of Spiroplasma-infected flies. Finally, we detected Spiroplasma west of the Rocky Mountains for the first time and showed that defense against nematodes occurs in flies with a western genetic background. Because nematode infection is common throughout D. neotestacea’s range, we expect Spiroplasma to spread to the Pacific coast

All data

This is an Excel workbook containing spreadsheets on restoration of fertility (female egg count), Spiroplasma density (qPCR-Spiroplasma), Howardula motherworm size (Motherworm size), and maternal transmission (Maternal transmission). These data were collected in either the Perlman (University of Victoria) or Jaenike (University of Rochester), as indicated in the file